Environmental Management DOI 10.1007/s00267-017-0896-2

Polycyclic Aromatic Hydrocarbons: A Critical Review of Environmental Occurrence and Bioremediation

1 2 Oluwadara Oluwaseun Alegbeleye ● Beatrice Oluwatoyin Opeolu ● Vanessa Angela Jackson3

Received: 19 August 2015 / Accepted: 23 May 2017 © Springer Science+Business Media New York 2017

Abstract The degree of polycyclic aromatic hydrocarbon hydrocarbons, as well as the pathways and mechanisms contamination of environmental matrices has increased over through which they enter the soil, river systems, drinking the last several years due to increase in industrial activities. water, groundwater and food are succinctly examined. Their Interest has surrounded the occurrence and distribution of effects on human health, other living organisms, the aquatic polycyclic aromatic hydrocarbons for many decades ecosystem, as well as soil microbiota are also elucidated. because they pose a serious threat to the health of humans The persistence and bioavailability of polycyclic aromatic and ecosystems. The importance of the need for sustainable hydrocarbons are discussed as well, as they are important abatement strategies to alleviate contamination therefore factors that influence the rate, efficiency and overall success cannot be overemphasised, as daily human activities con- of remediation. Bioremediation (aerobic and anaerobic), use tinue to create pollution from polycyclic aromatic hydro- of biosurfactants and bioreactors, as well as the roles of carbons and impact the natural environment. Globally, biofilms in the biological treatment of polycyclic aromatic attempts have been made to design treatment schemes for hydrocarbons are also explored. the remediation and restoration of contaminated sites. Several techniques and technologies have been proposed Keywords Polycyclic aromatic hydrocarbons (PAHs) ● and tested over time, the majority of which have significant Environment ● Bioremediation ● Microorganisms limitations. This has necessitated research into envir- onmentally friendly and cost-effective clean-up techniques. Bioremediation is an appealing option that has been extensively researched and adopted as it has been proven to be relatively cost-effective, environmentally friendly and is Introduction publicly accepted. In this review, the physicochemical properties of some priority polycyclic aromatic Polycyclic aromatic hydrocarbons (PAHs) are a group of persistent, semi-volatile, organic pollutants that are ubiqui- tous in the environment and enter environmental matrices via natural and anthropogenic sources, including several * Oluwadara Oluwaseun Alegbeleye [email protected] industrial and certain agricultural activities (Wick et al. 2011). They are composed of two or more fused aromatics 1 Department of Environmental and Occupational Studies, Cape (benzene rings) and a system of hydrophobic and lipophilic Peninsula University of Technology, Cape Town, Western Cape, double bonds throughout their hydrocarbon rings. They South Africa fi 2 have been detected in signi cant concentrations in terres- Extended Curriculum Programmes, Faculty of Applied Sciences, trial and aquatic ecosystems, in air, as well as in food Cape Peninsula University of Technology, Cape Town, Western Cape, South Africa (Sojinu et al. 2011; Fernández-Luqueño et al. 2011; Ola- tunji et al. 2014). These groups of compounds have 3 Department of Biotechnology and Consumer Science, Cape Peninsula University of Technology, Cape Town, Western Cape, potential harmful effects on ecosystems as well as human South Africa health, as many of them have been shown to be Environmental Management carcinogenic, teratogenic and mutagenic (Skupinska et al environment because of low water solubility, low volatility, 2004; Srogi 2007; Quinn et al. 2009). resistance to leaching and their recalcitrant nature (Wild and Several approaches and strategies, including physical and Jones 1995; Jones et al. 1996). chemical, have been developed, optimised and utilised to Alkyl (CH2− group) substitution of the aromatic ring mitigate the effects of these contaminants and remediate results in an overall decrease in the PAH solubility, polluted sites. Some of these conventional remediation although there are some exceptions to this rule, such as techniques have significant limitations, such as their tech- benzo(a)anthracene, which is less soluble than either methyl nological complexity, high cost and the lack of public or ethylbenzo(a)anthracene (Luch 2005). Molecules with a acceptance. Most of the techniques are invasive and merely linear arrangement tend to be less soluble than angular or relocate the contamination problem to a different site, often perifused molecules. For instance, anthracene is less soluble requiring further waste management. than phenanthrene, and naphthalene is less soluble than A cheaper and more effective approach than these tradi- chrysene or benzo(a)anthracene (Okere and Semple 2012). tional methods is to adopt an environmentally sustainable The solubility of PAHs in water is enhanced three- to four- technique that will either completely destroy the pollutants or fold by a rise in temperature from 5 to 30 °C. Dissolved and transform them into harmless substances (Lundestedt 2003; colloidal organic fractions also enhance the solubility of Castaldini 2008). Bioremediation is a biological approach PAHs, which are incorporated into micelles (Luch 2005). that is an appealing alternative because it has been proven to The United States Environmental Protection Agency (US be relatively cost-effective, environmentally friendly and is EPA) has designated 16 PAH compounds as priority pol- publicly accepted. Bioremediation is a pollution control lutants (Luch 2005), including the HMW PAHs (benzo(a) strategy that uses biological systems to convert various toxic pyrene, dibenz(ah)anthracene and indeno(1,2,3-cd)pyrene compounds into innocuous forms (Vidali 2001). among others) and the LMW PAHs (naphthalene, ace- naphthene, fluorene and phenanthrene among others), which are often monitored for measurement in environ- Properties of PAHs mental samples. Table 1 shows the properties of the US EPA priority PAH compounds. PAHs are a class of organic compounds containing two or more fused benzene rings with various structural config- urations (Prabhu and Phale 2003), where the rings could be Sources and Occurrence of PAHs in linear, angular or clustered arrangements (Lundestedt 2003). PAHs are lipophilic, have low vapour pressure and PAHs are products of pyrolysis of organic material (Wild low water solubility, as well as high melting and boiling and Jones 1995; Lenicek et al. 1997); they are formed by points (Skupinska et al. 2004). They contain only carbon the incomplete combustion of organic substances such as and hydrogen atoms, but nitrogen, sulphur and oxygen coal, oil, garbage, agricultural wastes, wood and tobacco atoms may readily substitute in the benzene ring to form (Sowa 2011). Major sources of PAHs for environmental heterocyclic aromatic compounds, which are usually matrices include production and use of carbon black, coal grouped with PAHs (Lundestedt 2003). Also, PAHs sub- tar and asphalt, coke production, catalytic cracking, gasifi- stituted with alkyl groups are normally found together with cation or liquefaction of fossil fuels, refining/distillation of PAHs in environmental matrices (Lundestedt 2003; Nkan- crude oil and crude oil-derived products, heat and power sah 2012). generation by using fuels, wood treatment processes, wood PAHs are classified as low molecular weight (LMW) if preservative (for example, anthracene oil, creosote) pro- they have two or three fused rings, and as high molecular duction and many others (Wilson and Jones 1993; Baek weight (HMW) if they have four or more fused rings (Wick et al. 1991; Zhang and Tao 2009; Sojinu et al. 2011). Other et al. 2011). LMW PAHs are more susceptible to degra- sources include volcanoes, natural losses or seepage of dation and volatilisation compared to their HMW counter- petroleum or coal deposits, bush and prairie fires, as well as parts (Harvey 1998). As molecular weight increases, exhaust fumes from vehicles and other engines. PAHs hydrophobicity/lipophilicity increases, water solubility generally occur as complex mixtures (for example, as decreases and vapour pressure decreases, which makes the components of coal tar, crude oil or as part of combustion structure more recalcitrant (Maliszewska-Kordybach 1999; products such as soot), not as single compounds. However, Luch 2005). To illustrate this, research has shown that the they may be manufactured as individual compounds for average half-life of the tricyclic phenanthrene ranges from research purposes, or for use in certain industrial processes 16 to 126 days in soil, whereas for the five-ringed HMW such as production of medicines, dyes, plastics and pesti- PAH benzo(a)pyrene the half-life may range from 229 to cides (ATSDR 1995). In this case, the pure PAH com- 1500 days (Sojinu et al. 2011). HMW PAHs persist in the pounds exist as colourless, white, or pale yellow-green Environmental Management

Table 1 Properties of US EPA PAH Molecular Melting Water solubility Vapour pressure Log priority PAHs (Coover and weight point (°C) (mg/l) (mmHg) Kow Simms 1987; Yalkowsky and Dannenfelser 1992; Howard and Naphthalene 128.2 79–82 320 ND 3.5 Meylan 1997; Pazos et al. 2010; × −3 Okere and Semple 2012) Acenaphthene 152.2 95 5.3 4.47 10 3.95 Acenaphtylene 152.2 72–82 3.93 0.029 3.94 Fluorene 166.2 115–116 1.85 5.0 × 10−6 4.28 Phenanthrene 178.2 99 1.24 6.8 × 10−4 5.62 Anthracene 178.2 218 0.64 1.7 × 10−5 5.33 Fluoranthene 202.3 110 0.25 5.0 × 10−6 4.62 Pyrene 202.3 156 0.14 2.5 × 10−6 4.47 Benzo(a)anthracene 228.3 158 0.01 2.2 × 10−8 5.30 Chrysene 228.3 255 0.002 6.3 × 10−7 5.30 Benzo(b) 252.3 168 0.0015 5.0 × 10−7 5.74 fluoranthene Benzo(K) 252.31 215 ND 9.7 × 10−10 6.06 fluoranthene Benzo(a)pyrene 252.3 179 0.0038 5.6 × 10−9 5.74 Benzo(ghi)perylene 276.3 273 0.00026 1.3 × 10−10 6.20 Dibenzo(ah) 278.35 262 0.0005 ND 6.84 anthracene Indeno 1,2,3-c,d 276.3 163 Insoluble 10−11–10−6 6.20 pyrene Log Kow octanol–water partition coefficient, ND not determined crystalline solids with a faint, pleasant odour (ATSDR properties of the PAH compound and several other envir- 1995; Haritash and Kaushik 2009; Kim et al. 2013). In onmental factors. They have been found occurring in air, contaminated sites, PAHs occur either in the particulate or soil, surface water, groundwater as well as sediments. in the gaseous phase depending on their volatility. LMW PAHs occur predominantly in the vapour phase, while HMW compounds are largely bound to particles. Four- Sources and Occurrence in Soil ringed compounds are usually found occurring between the vapour and particulate phases depending on atmospheric PAHs enter the soil through atmospheric deposition from conditions like temperature, relative humidity, as well as the long-range transport, industrial contamination (aluminium nature (ie. the origin and properties) of the aerosol and the and coke production, petrochemical processes, wood pre- properties of the individual PAH (Zhang and Tao 2009; servation, rubber tyre and cement manufacturing, as well as Byeong-Kyu 2010; Choi et al. 2010). In the atmosphere, many other industrial processes), waste incineration, irri- PAHs may occur (react) with pollutants such as ozone, gation with contaminated water and bush fires (Wick et al. nitrogen oxides and sulphur dioxide, yielding diones, nitro 2011). and dinitro-PAHs, and sulphonic acids, respectively (Srogi Several researchers have observed greater amounts of 2007). Although many studies regarding the characteristics, PAHs in urban soils as they are more exposed to the PAHs toxicity and biodegradability of PAHs have been conducted produced by both stationary (power plants, industries and on single (often solid, crystal) compounds to minimise the residential heating) and mobile sources (traffic emissions, number of variables, research has shown that PAHs exist in and road by-products such as wearing of tyres and asphalt environmental samples as complex mixtures (Cerniglia constituents) (Kamaljit et al. 2010). Maisto et al. (2006) 1992). It is thus uncertain to what extent PAHs occur in the reported that total PAHs were 2–20 times greater in the environment as the solid crystals that most studies regard urban areas of Naples (Italy) than the park soils that were (Rice and Suuberg 2010; Choi et al. 2010; Ruby et al. 12 km away. Similarly, Baek et al. (1991)reportedthaturban 2016). soils near the highways were highly contaminated. Another The fate of PAHs in the environment and the routes of study in Ontario, Canada, by Environment Ontario (1992) wildlife or human exposure are influenced by the environ- showed that a higher concentration of PAHs was associated mental medium (air, food, water or soil) in which the PAHs with locations close to airports, highways, rail stations and reside (Arey and Atkinson 2003), the physico-chemical heavy industries. In New Orleans, Wang et al. (2008) Environmental Management observed the highest amounts of PAHs in soils close to the Acenaphthene (0.88317 mg/l), acenaphthylene (0.18837 roads (7189 µg/kg) than open spaces that were 10 m away mg/l), naphthalene (0.52510 mg/l), fluorene (0.20438 mg/l), from the roads (2404 µg/kg). Similar results were shown by phenanthrene (0.26732 mg/l) and anthracene (0.25084 mg/l) Wilcke (2000), who reported that PAH levels declined were detected in the groundwater sources of a coastal set- exponentially with increase in distance from the roads due to tlement near the Port Harcourt refinery company situated at the reduced vehicular emissions (Kamaljit et al. 2010). Old Okrika Mainland, Port Harcourt, Nigeria (Okoli et al. 2011). coal gasification sites have been shown to be contaminated However, it has been reported that PAH concentrations in with PAH levels as high as 300 g/kg(Bamforth and Singleton near surface groundwater may increase after periods of rain, 2005). indicating that a quick transfer from rainwater into Due to their hydrophobicity, PAHs present in soil occur groundwater is possible (Manoli and Samara 1999). mainly in the nonaqueous phases, where they adsorb unto The presence of PAHs in drinking water may be attrib- soil organic matter and particles, or in an oily phase, mainly uted to raw water sources from surface or groundwater or to occurring as crystals or solids (Boonchan et al. 2000; Srogi the use of coal tar-coated pipes in public water supply 2007; Peng et al. 2008). The formation of non-extractable systems (Vega et al. 2011). It has been shown that chlor- bound residues is another significant sink of PAHs in soils. ination of drinking water may lead to the formation of PAH metabolites may also be incorporated into soil organic oxygenated and chlorinated PAHs, which are more toxic matter to form bound residues (Srogi 2007). than the parent PAH compounds (Shiraishi et al. 1985; Manoli and Samara 1999). Many investigators have repor- ted the occurrence of PAHs in drinking water (Vega et al. Sources and Occurrence in Water 2011; Karyab et al. 2013; Pan et al. 2015). According to the World Health Organisation (WHO), results obtained from a Concentrations of PAHs in the aquatic environment are survey conducted to establish guidelines for the assessment generally highest in sediment, intermediate in biota and of drinking water quality revealed elevated concentrations lowest in the water column (Canadian Council of Ministers of PAHs (predominantly fluoranthene, benzo(b)fluor- of the Environment (CCME) 1999, 2008). They generally anthene, pyrene, indeno(1,2,3-cd) pyrene, phenanthrene) in accumulate in sediments because they tend to adsorb to rainwater and especially in snow and fog. This is probably a particulate matter that settle at the bottom of aquatic eco- result of the adsorption of the compounds to air particulate systems (Juhasz and Naidu 2000; Perelo 2010) and are often matter, which is finely dispersed into the water during wet encountered in more significant concentrations in water deposition (WHO 2003). bodies close to point sources of contamination such as industries (Juhasz and Naidu 2000). PAHs enter surface waters mainly via atmospheric par- Sources and Occurrence in Food ticulate matter deposition (including wet and dry deposition of particles and vapours), runoff from polluted ground PAHs enter plants essentially through atmospheric deposi- sources, urban runoff, municipal wastewater discharges, tion on grains, fruits and vegetables, especially those with industrial effluents, as well as oil spills and seeps (Srogi broad leaves such as spinach, and via uptake from con- 2007; Latimar and Zheng 2003; Yanyangwu 2012). taminated soil and groundwater (Fismes et al. 2002). Atmospheric deposition is considered to be an important Vegetation in urban areas, especially those close to roads input of PAHs to surface waters, with 10–80% of PAH and industries, have been reported to have higher con- inputs to the world’s oceans estimated to be from atmo- centrations of PAHs (Gomes et al. 2013). Grazing cattle spheric sources (Motelay-massei et al. 2006; Srogi 2007). and poultry, which may ingest particulate matter from Rainwater has been shown to contain many organic com- soil, are susceptible to contamination by PAHs adsorbed pounds, including PAHs, where the concentration of PAHs to particles (Scientific Committee on Food, European in rainfall can sometimes be much higher than in the Commission 2002). Aquatic foods such as fish, mussels, receiving water body (Manoli and Samara 1999). shellfish and shrimp are contaminated through absorption of PAHs in groundwater may originate from polluted sur- contaminated fluvial and marine waters (Mackay and Fraser face water bodies, irrigation with contaminated water, lea- 2000; Menichini and Bocca 2003). The extent of accumu- chates from solid waste disposal sites or contaminated soil lation and retention of PAHs in marine organisms are (Manoli and Samara 1999). Groundwater concentrations of influenced by several factors and mechanisms, such as carcinogenic PAHs reported for US groundwater ranged physicochemical, organismal physiology, the available from 0.2 to 6.9 ng/l, while the corresponding concentrations fraction of the PAH compound that can be readily absorbed in surface waters were between 0.1 and 800 ng/l and most by the organism, the distribution and profile of PAH frequently between 2 and 50 ng/l (Nigam and Singh 2011). compounds in the aquatic ecosystem, their uptake and Environmental Management partitioning in different tissues, their rates of elimination, as come into contact with combustion gases, increases the well as their potential for persistence in varying species PAH content (Scientific Committee on Food, European (Meador et al. 1995). A study by Perugini et al. (2007) Commission 2002). analyzed PAHs in fish in several pools coming from PAHs have also been detected in milk; a study by Zanieri the Central Adriatic Sea. The study reported that Atlantic et al. (2007) in Italy showed significant levels of PAHs in mackerel, European hake and blue whiting showed breast milk, especially in women residing in urban areas, the highest PAH concentrations, ranging from 44.1 to and even higher concentrations were detected in women 63.3 ng/g wt. who smoke. Individual PAH concentrations ranging from 5 Common sources in processed foods are thermal treat- to 15 ng/kg human milk were reported by a survey in ments such as grilling, barbecuing, smoking, frying, baking Germany in 1984. In another German study, PAH levels and charbroiling (Menichini and Bocca 2003). Contamina- ranging from 3 to 30 ng/kg human milk were found (Sci- tion levels of smoked foods depend on product character- entific Committee on Food, European Commission 2002). istics and factors related to smoking procedures, such as PAHs have also been reported to occur in fresh milk, wood type and composition, type of heat generator, commercial milk formulae and infant cereals (Rey-Sal- moisture content, oxygen availability and combustion gueiro et al. 2009; Garcia Londono et al. 2013; Sanagi et al. temperature, all of which influence the quantity and profile 2013; Girellia et al. 2014). Kishikawa et al. (2003) reported of PAHs formed (Guillen et al. 2000; Gomes et al. 2013). that the average concentrations of total PAHs in commercial High combustion temperatures (McGrath et al. 2003) and milk, infant formula and human milk in Japan were 0.99, the use of softwoods (Guillen et al. 2000; Stumpe-Viksna 2.01 and 0.75 lg/kg, respectively. Eight individual PAH et al. 2008) have been reported to enhance the formation of compounds were detected at low concentrations in milk HMW PAHs; therefore, instead of using conventional kilns, samples collected from the tanks at farms located near alternative strategies such as the use of external smoke potential emission sources from industries in France. Con- generators (Duedahl-olesen et al. 2006; Simon et al. 2010; centrations of 12 selected PAHs were estimated in milk, Gomes et al. 2013), where the smoke is filtered before milk powder and some other dairy products in Canada introduction into the smoking room, have been devised (Lawrence and Weber 1984), the Netherlands (de Vos et al. (Roseiro et al. 2011). PAHs have been detected in smoked, 1990) and the United Kingdom (Dennis et al. 1983, 1991). grilled and barbecued food products in several regions of The concentrations ranged from <0.01 µg/kg for benzo(k) the world (Petrun and Rubenchik 1966; Lawrence and fluoranthene and dibenzo(a,h)antracene to 2.7 µg/kg for Weber 1984; Storelli et al. 2003; Rey-Salgueiro et al. 2008; pyrene. High concentrations of PAHs were also detected in Farhadian et al. 2010; Silva et al. 2011; Chung et al. 2011; the milk of reared cows and sheep in Kuwait (Husain et al. Viegas et al. 2012). Some specific examples are reported in 1997). PAH compounds have been detected in some other this review, such as a study of smoked food samples by food types such as fruits and confectionaries. However, the Gomaa et al. (1993) that measured PAHs in smoked meat details of sources and occurrence in such cases are not and fish. Total PAH concentrations in smoked meat ranged parsed in this review. Although PAHs are routinely mon- from 2.6 to 29.8 ppb, while in smoked fish the range was itored in many foodstuffs in several countries, particularly between 9.3 and 86.6 ppb. Concentrations of five potential advanced countries, concern about its occurrence and carcinogens [benzo(a)pyrene, benzo(a)anthracene, benzo(b) potential toxicity persists. However, in recent times, more fluoranthene, dibenzo(a,h)anthracene and indeno(1,2,3-cd) stringent regulations are being enacted. For instance, pyrene] reached levels of 16.0 ppb (in salmon). The same recently, a new law was passed in the European Union study measured PAHs in liquid smoke seasonings, with restricting the presence of PAHs in foodstuff (Vander- total PAH levels of up to 43.7 ppb detected, and the levels meersch et al. 2015). Some of the old regulations are also of the five selected compounds up to 10.2 ppb. Another being reviewed. In cases where only B(a)P was screened for study of smoked food commercially available in Canada in foodstuffs, other compounds such as benzo(a)anthracene, reported similar findings. PAHs were detected in 19/ benzo(a)fluoranthene and chrysene must now be analysed in 43 smoked meat samples at levels as high as 13 ppb total addition to B(a)P. Furthermore, the maximum residue levels PAH. The compounds were also detected in 18/25 smoked permitted in fish, crustaceans and molluscs have been fish samples, with levels as high as 141 ppb detected (in reduced in this region (Vandermeersch et al. 2015). smoked oysters) (Panalaks 1976). Roasting and drying have been reported to influence the presence and amount of PAHs in coffee, tea, certain cereals, Effects of PAHs vegetable oils and margarine (Dennis et al. 1991; Thomson et al. 1996; Srogi 2007). The process of roasting and drying PAHs are of great environmental and health concern as they the coffee beans, tea leaves and oil seeds, where they may are recalcitrant, bioaccumulative and toxic to living Environmental Management organisms and ecosystems (Shi et al. 2005; Kweon et al. following acute inhalation, with the likely complication of 2011; Hajisamoh 2013). Reactive metabolites (e.g. epoxides abdominal pain (IPCS 2000). and dihydrodiols) of some PAHs have great potential to bind Phenanthrene, a major constituent of urban air pollution, to cellular proteins and DNA, often generating toxic effects. has been shown to be mutagenic and impair immune The resulting biochemical disruption and cell damage can function (Liu et al. 2013). It is a weak inducer of sister lead to mutations, developmental malformations, tumors, and chromatid exchanges and a potent inhibitor of gap junc- cancer (Kim et al. 2013). The absorption, distribution and tional intercellular communication (Weis et al. 1998). It is toxicity of PAHs depend on a number of factors, including known to be a photosensitiser of skin and a mild allergen the species, route of exposure and physicochemical char- (Mastrangela et al. 1999; Sudip et al. 2002). Acenapthene acteristics (CCME 1999;Rameshetal.2004). The uptake of has been proven to have harmful effects on skin, body fluids high doses of persistent molecules can have hazardous effects and immune system of animals after both short- and long- on flora and, through the food chain, on fauna and human term exposure (ATSDR 1995; Kim et al. 2013). Some health (Langenbach 2013). Humans are exposed to PAHs studies suggest that fluorene induces skin and eye irritation through inhalation, ingestion of contaminated food and and is a potential carcinogen (New Jersey Department of water, and through dermal contact (Sowa 2011). Health and Senior Services 1999). Animal exposure to PAHs such as benzo(a)antracene, benzo(a)pyrene, benzo(b)fluoranthene, benzo(j)fluor- Human Health Effects anthene, benzo(k)fluoranthene, chrysene, dibenz(a,h) anthracene and indeno(1,2,3-c,d)pyrene have caused The effects of PAHs on human health depend mainly on the tumours, mortality, growth and reproductive impairment, duration and rate of exposure, as well as the concentration teratogenesis, endocrine disruption, liver and kidney and the innate toxicity of the individual PAH (Buha 2011; damage, neurobehavioral changes and altered thermo- Rengarajana et al. 2015). Factors such as pre-existing health regulatory ability (CCME 2008; ATSDR 1995; Kim et al. status, personal traits, habits, the presence of other pollu- 2013). The scientific consensus is that similar effects could tants and age can also influence the effects that human occur in people, but these effects have not been reported in exposure to PAHs induces [Agency for Toxic Substances humans (ATSDR 1995). and Disease Registry (ATSDR) 1995; Buha 2011]. It is The Department of Health and Human Services, US often difficult to ascribe exclusive health effects in epide- (DHHS), has determined that benzo(a)anthracene, benzo(b) miological studies to specific PAHs because most exposures fluoranthene, benzo(j)fluoranthene, benzo(k)fluoranthene, are to a combination of different PAHs (ATSDR 2011). benzo(a)pyrene, dibenz(a,h)anthracene and indeno(1,2,3-c,d) However, some studies have shown that exposure to certain pyrene are known animal carcinogens. The International individual PAHs over extended periods at elevated con- Agency for Research on Cancer (IARC) has determined that centrations can induce deleterious effects (ATSDR 2011). benzo(a)anthracene and benzo(a)pyrene, benzo(b)fluor- Naphthalene, a common micropollutant in potable water anthene, benzo(j)fluoranthene, benzo(k)fluoranthene and (Sudip et al. 2002), binds covalently to molecules in liver, indeno(1,2,3-c,d)pyrene are probable human carcinogens, and kidney and lung tissues, thereby enhancing its toxicity. It is anthracene, benzo(g,h,i)perylene, benzo(e)pyrene, chrysene, also known to cause haemolytic anaemia and eye defects fluoranthene, fluorene, phenanthrene and pyrene are not clas- [International Programme on Chemical Safety (IPCS) 2000; sifiable as to their carcinogenicity to humans (ATSDR 1995). Srogi 2007]. Reports suggest that it is capable of acting as US EPA has determined that benzo(a)anthracene, benzo an inhibitor of mitochondrial respiration (Falahatpisheh (a)pyrene, benzo(b)fluoranthene, benzo(k)fluoranthene, et al. 2001). In cases of acute exposure, especially in the chrysene, dibenz(a,h)anthracene and indeno(1,2,3- c,d)pyr- case of occupational exposure, signs and symptoms such as ene are probable human carcinogens and that acenaphthy- nausea, vomiting, abdominal pain, diarrhoea, headache, lene, anthracene, benzo(g,h,i)perylene, fluoranthene, confusion, profuse sweating, fever, tachycardia, tachypnoea fluorene, phenanthrene and pyrene are not classifiable as and agitation may be induced (IPCS 2000). Acute dermal regards human carcinogenicity. Acenaphthene has not been exposure to naphthalene has been associated with mild classified for carcinogenic effects by the DHHS, IARC or irritation and, in some sensitive individuals, may cause US EPA (ATSDR 1995; Sram et al. 1999). dermatitis [Centres for Disease Control and Prevention (CDC) 2009]. Naphthalene is not believed to cause cancer in humans, but has been shown to induce tumour in Effects of PAHs on Soil Microbiota laboratory mice and other animals (IPCS 2000). Ingestion of naphthalene is not a common route of exposure; how- The short- and long-term effects of PAH pollution on the ever, the effects observed are similar to those seen structure of soil microbial communities have been widely Environmental Management investigated (Johnsen and Karlson 2005; Liang et al. 2011; petrogenic source PAHs (Carls et al. 1999). Similarly, Ji et al. 2013). PAH pollution disrupts the biodiversity and classical cytogenetic techniques showed significant genetic evenness (even distribution) of species of soil microbes and toxicity in herring larvae, in association with the Exxon in certain cases may even lead to total loss of certain spe- Valdez oil spill in Alaska, the effects of which were cor- cies. If key populations are compromised (or threatened), related with levels of PAHs found in mussels in the area certain crucial soil functions may be completely lost (Hose and Brown 1998). Other sublethal effects caused by (Muckian et al. 2009; Valentı´n et al. 2013). The influence embryonic exposures include yolk sac and pericardial of PAHs on the enzymatic activity of soil microbiota oedema, haemorrhaging, disruption of cardiac function, depends to a significant level on soil properties such as total craniofacial and cardiac deformities, neuronal cell death and organic carbon content and pH (Baran et al. 2004). impaired swimming (White et al. 1999, Barron et al. 2003; PAH pollution usually triggers an increase in hydro- Brinkworth et al. 2003). carbonoclastic bacteria occurrence in soil. A study by Biochemical defects have been observed in fish in coastal Benedek et al. (2013) showed that PAH-polluted soil waters, lakes and rivers in a number of countries (Payne samples were mainly inhabited by the representatives of the et al. 2003). Alteration of phase I and to a lesser extent β, ϒ proteobacteria, overwhelming pre-contamination phase II enzymes, which play a major role in detoxification dominance of Pseudomonas and Actinobacteria. Another and other biochemical processes, has also been observed study by Ren et al. (2015) showed that the bacterial richness (Hose and Brown 1998). Changes in hormones, energy and diversity in the soil samples studied was affected by reserves and serum enzymes in fish exposed to PAHs have pyrene pollution. Organisms belonging to the phyla occasionally been reported. Results obtained from experi- Chlorflexi, Alphaproteobacteria, Actinobacteria, Deltapro- mental studies with fish chronically exposed to sediments teobacteria and Crenarchaeota were significantly decreased contaminated with PAHs of petrogenic or pyrolytic sources after pyrene pollution, while members of Phyla Acid- as well as industrial formulations such as creosote indicate obacteria, Betaproteobacteria and Gamaproteobacteria that PAHs are a likely cause of some of the pathological were significantly increased. Apart from the effects on soil defects found in fish in highly contaminated environments life, accumulation of PAHs in soils is a potential source of (Payne et al. 2003). An unusually high prevalence of oral, contamination of vegetables, other crop produce and food dermal and hepatic neoplasms have been observed in chains, which may cause direct or indirect exposure to bottom-dwelling fish from polluted sediments containing humans. Moreover, leaching, evaporation and migration are grossly elevated PAH levels (Couch and Harshbarger 1985; possible PAH sources of atmospheric or groundwater con- Eisler 2007). tamination (Srogi 2007). Continuous PAH contamination, Anthracene, which is known to produce highly cytotoxic therefore, has grave potential consequences not just for soil by-products in some organisms when they are simulta- life but, extensively, for life on earth. neously exposed to the chemical compound, and ultraviolet light damaged the gills of fish upon exposure to low levels of the compound (Oris and Giesy 1985; Choi and Oris Effects on Aquatic Ecosystem 2003). Kim et al. (2007) found that adult Pacific oysters Many studies have examined the effects of PAHs on aquatic (Crassostrea gigas) exhibited marked decreased pro- organisms (Varanasi et al. 1989; Harvey 1997; Hose and ductivity when exposed to even low concentrations of Brown 1998; Beasley and Kneale 2002; Grotte et al. 2005; PAHs. A study by Martineau et al. (2002) in St Lawrence Hellou et al. 2006; Hjorth et al. 2007; Petersen et al. 2008). Estuary, Quebec, Canada, on Beluga (Delphinapterus leu- PAH toxicity to a variety of aquatic organisms has been cas) suggests a correlation between the incidence of cancer reported, acting as carcinogens, DNA mutagens and endo- in these species and the presence of PAHs in their habitat crine disruptors (Pittinger et al. 1987; Hellou et al. 2006). introduced by local aluminium smelters. Adverse biological effects associated with PAHs in sedi- Stream biota, such as insect larvae and crustaceans, are ments include decreased benthic invertebrate abundance, also affected adversely, resulting in reduced species diver- distorted diversity and growth, as well as physiological and sity in affected areas (Beasley and Kneale 2002). A study behavioural changes, among others (Liu et al. 2013). by Ikenaka et al. (2013) demonstrated the effect of B(a)P on In aquatic mammals and fish, the immunotoxic effects of the zooplankton community; the study showed that B(a)P PAHs have been widely demonstrated (Weeks and Warimer notably induced a decrease in zooplankton abundance. 1984; Hellou et al. 2006). Exposure to PAHs has been Researchers have expressed concerns that PAHs and reported to affect egg production in fish and alter normal other toxic components in oil could wipe out generations of fish development. Cytogenetic toxicity was also observed in some species (Mascarelli 2010). Microorganisms live in fish larvae exposed as eggs to low concentrations of areas of delicate balance, which can be disrupted by Environmental Management episodes of pollution (Beazley et al. 2012), causing drastic the ingested materials are seemingly complex and not yet changes to microbial communities in ecosystems. Selective fully understood (Meador 2003; Cornelissen et al. 2005; pressure has been seen to be placed on communities of Heijden and Jonker 2009). There is ample research evidence organisms after major pollution incidents such as oil spills emphasising the importance of mode of feeding of inver- (Beazley et al. 2012). For instance, post-spill samples after tebrates to the overall degree of bioaccumulation (Morrison the Deep water Horizon oil spill in the Gulf of Mexico, near et al. 1996; Kaag et el. 1997; Baumard et al. 1998a; Meador Mississippi, USA, contained mostly oil-degrading organ- et al. 2006). isms resulting from a drastic decrease in diversity. Selective One of the most relevant considerations for bioaccumu- pressure placed upon communities of organisms by the lation of PAHs in aquatic species is the amount of accu- large increase of petroleum and other petroleum derivatives mulated PAH that is efficiently metabolised. For species selects for the survival of organisms that can use petroleum that have the capacity to efficiently metabolise PAHs, they and derivatives as energy, electron and/or carbon source may accumulate large amounts of PAH compounds, exhibit (Beazley et al. 2012). effects, but not contain measurable levels of the parent compounds. Mutagenic metabolites may however be formed, which may be more toxic than the parent com- Bioaccumulation Potential of PAHs in Aquatic pounds (Meador 2012). On the other hand, for species that Ecosystems have a weak or non-existent ability to metabolise PAHs, assessing tissue concentrations would be relatively simpler PAHs have the ability to bioaccumulate and biomagnify in for different biological responses (Meador 2003). Inverte- organisms in aquatic food chains, with potential negative brates which are a very diverse and ecologically important effects not only on the growth and reproduction of indi- group, exhibit considerable variability in their capability to genous wildlife such as fish, but also for human health, metabolise PAHs. Certain crustacean species possess some particularly because of consumption of contaminated sea- of the highest rates of biotransformation for PAHs, while food (Sun et al. 2016). Seafood is one of the most important mollusks usually have weak or even non-existent activation food commodities globally, recognised for their high-pro- of detoxifying enzymes. Even within taxa, there is high tein, low-saturated-fat content, as well as for omega fatty variability. Certain studies have reported that annelids and acids, which are famous for the health benefits they confer crustacean species display highly differential rates of bio- on consumers (Vandermeersch et al. 2015; Ke et al. 2017). transformation for PAHs. For instance, McElroy et al The uptake and accumulation of PAHs into aquatic organ- (2000) studied four annelid species and reported wide dis- isms may be via water, food or sediment (Yakan et al. parities in the percentage of BaP metabolism, one species 2017), although PAHs typically partition preferentially to successfully metabolised 7% of BaP, two species metabo- sediments in aquatic ecosystems because of their hydro- lised about 40%, and another species was able to convert phobicity, where they persist for protracted periods and 96% of the total BaP. Furthermore, the study found high continually affect bottom-dwelling organisms and high- variability for two crustacean species, with metabolites trophic-level animals via food webs (Wan et al. 2007). accounting for 20 and 60% of the BaP accumulated after Numerous other factors influence the rate and progression 7 days. Certain members such as Mussels accumulate and of bioaccumulation in aquatic organisms. Some of these transfer PAHs to higher food chain levels because they are include physico-chemical properties, organic carbon, con- filter feeding bivalves and their enzyme activities related to tact time (aging), desorption rate, PAH source (petrogenic pollutant (PAH) metabolism are low (Baumard et al. 1998b, vs pyrogenic), toxicokinetics, feeding mode, metabolism, 1999; Zhou et al. 2008). PAHs are hydrophobic and lipo- biota-sediment accumulation factors (BSAFs), organism philic, allowing them to be stored in adipose tissues of physiology, size and behaviour, lipid levels, organ-specific predator species at the top of the web, such as polar bears bioaccumulation, as well as the occurrence of bound resi- and beluga whales, where metabolism is significantly dues among others (Meador 2003, 2012). slower (Mackay and Fraser 2000; Kelly et al. 2007). Typically, aquatic species exhibit various feeding modes, Invariably, organisms located at the top of the food chain, including (selective and nonselective) sediment ingestion, such as humans, build up the highest concentrations of detritus feeding, predation, filter feeding and suspension PAHs within their bodies. feeding (Meador 2012). Each of these feeding modes can There are tools available for the determination of expo- dramatically influence the exposure degree and final sure routes, accumulation patterns and concentrations of bioaccumulation values in organisms. Ingestion of prey pollutants in different aquatic organisms. These are known organisms, detritus as well as sediment is an important route as toxicokinetic models and several of these exist for marine for PAH accumulation; however, the factors that determine and freshwater food webs, such as equilibrium partitioning the bioavailable fraction that will be bioaccumulated from models, mechanistic mass balance models, fugacity models, Environmental Management compartment-based kinetic models, physiological and available, however, suggest a high degree of contamination. bioenergetics models. Bioaccumulation modelling studies Layshock et al. (2010) showed oxy PAH levels in mussel for fresh water food webs are however more abundant in tissue higher than PAH compounds. Another study by literature compared to marine food webs, particularly for the Bandowe et al. (2014) showed higher concentrations of oxy upper trophic level organisms such as fish species, which PAHs in fish muscle than the evaluated 16 US-EPA PAHs. play ecologically important roles due to their high mobility There is also a paucity of data for alkylated PAHs. Certain and energy transfer responsibilities between lower and researchers have however demonstrated that alkyl-PAHs upper trophic levels in the food web (Beyer et al. 1996; Van may have greater toxicity profiles than their parent com- der Oost et al. 2003). Apart from fish species, mussels are pounds (Sun et al. 2016). Another important problem is the also highly relevant players in the food chain. In many difficulty associated with the accurate quantification of cultures, worldwide, they are part of the human diet and alkyl-PAHs because of the unavailability of commercial they have been confirmed as a biomonitor for hydrocarbons standards for many of the individual isomers (Yang et al. in the environment because of their ability to bioaccumu- 2014). Alkyl-PAHs have been detected in fish and shellfish late. Modelling studies using mussels have highlighted at sites contaminated by crude oil. The studies showed concentration levels, transfer routes and depuration dura- general higher concentrations of alkyl PAHs in the tissues tions of PAHs in the food chain. Although there is a relative than the parent non-alkylated PAHs (Baird et al. 2007). scarcity of marine modelling studies, there are some studies on bioaccumulation of PAHs through marine food webs (Broman et al. 1990; Kayal and Connell 1990; Wan et al Persistence of PAHs in the Environment 2007; Nfon et al. 2008; Takeuchi et al 2009) and these studies have documented that PAH compounds did not PAHs in the environment are usually subjected to processes appear to biomagnify. Due to the conflicting results such as volatilisation, photo-oxidation, chemical oxidation, obtained for freshwater and seawater food chains, in addi- emulsification, adsorption onto organic matter and leaching, tion to the limited information on the subject, further as well as microbial degradation responsible for PAH losses investigation into the biomagnification of PAHs in fresh- (Wild and Jones 1995;Pantsyrnayaaetal.2011). In the water and marine food webs is highly desirable. aquatic environment, dissolution, adsorption onto suspended There are some simulation models that use chemical, solids and subsequent sedimentation, biotic and abiotic environmental and organism-specific properties such as rate degradation, uptake by aquatic organisms and accumulation of elimination to predict the occurrence of individual PAH are all major pathways of PAHs (Pantsyrnayaa et al. 2011). compounds in the different aquatic ecosystem compart- PAHs escape degradation and persist in environmental ments. Some others such as fugacity models take PAH matrices for long periods because of a variety of factors, physico-chemical properties into consideration (Meador including chemical structure, environmental conditions, the 2012). These models and experimental evidence suggest concentration and dispersion of the PAH, and the bioavail- that LMW PAHs are taken up predominantly in the aqueous ability of the contaminant (Bamforth and Singleton 2005). phase. The uptake generally occurs when water passes over Generally, the higher the molecular weight of a PAH the gills. HMW compounds will be mostly accumulated molecule, the higher the hydrophobicity and toxicity, and from dietary sources. This concept is generally profound the longer the environmental persistence of such a molecule because the concentration of the compound is orders of (Cerniglia 1992; Bamforth and Singleton 2005). The age of magnitude higher in food and sediment that is ingested the contaminant in the sediment or soil also has an effect on relative to the amount found in the water phase (Meador the biodegradability of the PAH molecule (Hatzinger and 2012). Alexander 1995). A study using phenanthrene as a model There is a scarcity of information regarding the occur- PAH showed that phenanthrene mineralisation and there- rence and toxicity of PAH derivatives like oxygenated and fore biodegradability were significantly reduced with time alkylated PAHs in aquatic life. Studies have demonstrated of ageing of the contaminant (Rhodes et al. 2008). that a number of oxy PAHs are acutely toxic to a variety of The occurrence of PAHs with co-contaminants such as organisms (Hatch and Burton 1999; Bamforth and Single- other hydrocarbon compounds (alkanes, alkenes, BTEX, ton 2005; Lampi et al. 2006; Lundstedt et al. 2007). They among others), phenols and heavy metals is another factor have been shown to induce oxidative stress, endocrine that can prolong their residence time in the environment system disruptions, cytotoxic effects, as well as mutagenic (Bamforth and Singleton 2005). Aliphatic hydrocarbons and effects. Also, it is believed that oxy-PAHs are potentially BTEX compounds are readily biodegradable by the indi- more toxic than their parent compounds (Lundstedt et al. genous microbial community relative to the more complex 2007). However, knowledge of the levels of these com- chemical structures of the PAHs. This results in the deple- pounds in seafood is still relatively limited. The scarce data tion of available oxygen in the surrounding environment Environmental Management and the onset of anaerobicity (Bamforth and Singleton microbial metabolism (Maier et al. 2000;Wicketal.2011). 2005). Though it has recently been concluded that there is a This is usually achieved using various methods such as real potential for the biodegradation of PAHs in the absence biostimulation, bioaugmentation, composting, land farming, of molecular oxygen, details regarding the efficiency and use of surfactants, solvents and other solubility enhancers scale of PAH degradation in anaerobic environments is still (Wick et al. 2011). In experimental conditions, the addition of comparatively limited, with rates of anaerobic organic detergents and non-ionic surfactants such as Tween-20 and matter oxidation being up to an order of magnitude less than Tween-80 increases the solubility and substrate availability to those under aerobic conditions. In addition, there is the ligninolytic enzymes and cells (Pozdnyakova 2012). Various possibility that the presence of heavy metals in con- surfactants could increase the rate of anthracene, pyrene and taminated matrices could inhibit microbial growth and limit B(a)P oxidation by Bjerkandera sp. BOS55 by two-to-five the metabolism of PAH contaminants under anaerobic fold (Kotterman et al. 1998). The stimulating effect of sur- conditions (Bamforth and Singleton 2005). factants was found to be solely due to the increased bioa- vailability of PAHs, indicating that the oxidation of PAHs by the extracellular ligninolytic enzymes is limited by low Bioavailability of PAHs compound bioavailability (Kotterman et al. 1998). However, some studies have shown that the use of syn- One of the most important factors that directly influence the thetic surfactants to clean up contaminated sites may result in efficiency of biological treatment is the availability of the introduction of more pollutants (Wang and Brusseau contaminants for the degrading microorganisms (bioavail- 1993; Makkar and Rockne 2003; Pacwa-Plociniczak et al. ability) (Ławniczak 2013; Olaniran et al. 2013). Bioavail- 2011), which suggests they might be unsafe for the envir- ability can be defined as the effect of physico-chemical and onment after extensive use. The application of some surfac- microbiological factors on the rate and degree of biode- tants might improve the solubility and desorption rate of the gradation (Mueller et al. 1996). It is the percentage of PAH compounds to the aqueous phase, but not necessarily contaminant that can be readily accessed and degraded by improve the degradation rate and efficiency (Makkar and microorganisms (Bosma et al. 1997; Maier et al. 2000). Rockne 2003). A study conducted by Mulder et al. (1998a, b) Generally, contaminants ‘escape’ degradation due to showed that the introduction of hydropropyl-ß-cyclodextrin reasons that include (i) contaminant toxicity to the micro- (HPCD), a well-known PAH solubility enhancer, sig- organisms; (ii) preferential feeding of microorganisms on nificantly increased the solubilisation of PAHs although it did other substrates; (iii) unfavourable environmental condi- not improve the biodegradation rate of PAHs (Mulder et al. tions in the matrix for propagation of appropriate micro- 1998a, b). This asserts that factors other than solubility affect organisms; and (iv) poor contaminant bioavailability to the degradation rate of PAHs. microorganisms (Castaldini 2008). PAHs are stable due to The dissolution rate of PAH particles can also be their structure, which consists of several double bonds (Web improved by the hydrodynamic conditions of the system in 2011). They have low water solubility and studies have a bioreactor. Riess et al. (2005) demonstrated that the revealed that PAHs in the solid state are consumed by volumetric mass transfer coefficient of PAH particles was microorganisms only after they are transferred to the aqu- significantly enhanced in a bioreactor. The use of glass eous phase through the dissolution process (Volkering et al. beads in the reactor significantly increased the turbulence at 1993; Sowa 2011; Olaniran et al. 2013). Studies have also the interfacial surface of solid particles, thus reducing the shown that the strong adsorption capacity that PAHs have film thickness and enhancing the mass transfer coefficient. for particulate matter contributes largely to the recalcitrance On the other hand, the grinding force acting on the PAH of PAHs, which in turn significantly reduces their bioa- particles by the beads broke up the PAH particles, vailability (Castaldini 2008). increasing the surface area of particles and improving the In contaminated sediments, availability depends on mass transfer coefficient. Many other researchers have also physical factors such as grain size of the sediment, organic reported the effect of hydrodynamics on the mass transfer matter content, suspended particulate materials and biolo- rate of PAH particles (Mulder et al. 1998b; Viñas et al. gical factors, including wildlife diversity of the aquatic 2005) among others. ecosystem (benthic or pelagic organisms) and mode of exposure to the contaminants. One of the best methods proposed for assessing the bioavailability of sediment- Bioremediation associated contaminants is to observe their accumulation in organisms (Geffard et al. 2003; Lu et al. 2006). Bioremediation, also known as bioreclamation or bior- Several studies have demonstrated that PAHs can be estoration, involves the use of living organisms, primarily biologically degraded by increasing their availability to microorganisms, to degrade or detoxify hazardous waste Environmental Management into harmless substances such as carbon dioxide, water and proceed only when molecular oxygen is available for ring cell biomass (Barret et al. 2010; Langenbach 2013). In this cleavage. It may thus appear that aromatic metabolism is technique, the biodegradative abilities of microorganisms restricted to aerobes possessing oxygenase enzymes. are harnessed to remove or detoxify environmental pollu- Microbial transformation of aromatic compounds under tants (Labana et al. 2007). The technology can adopt a denitrifying, sulphate-reducing, and methanogenic condi- natural degradation pathway or utilise recombinant organ- tions, however, is fundamentally different from degradation isms to use certain toxic compounds as carbon or energy under aerobic conditions (Karthikeyan and Bhandari 2001). source (Lu et al. 2011). Bioremediation can occur on its own through natural attenuation (intrinsic bioremediation), but in many cases could take several years; hence, various Aerobic Biodegradation of PAHs bioremediation strategies have been developed to enhance the microbial metabolism of contaminants by adjusting The aerobic biodegradation process, also known as aerobic several variables (Langenbach 2013). This can be achieved respiration, is the breakdown of contaminants by micro- by biostimulation (stimulating viable native microbial organisms in the presence of oxygen (Bamforth and Sin- population), bioaugmentation (artificial introduction of gleton 2005; Gan et al. 2009). Aerobic bacteria use oxygen viable populations), biosorption (dead microbial biomass), as an electron acceptor to break down both the organic and bioaccumulation (live cells), phytoremediation (plants) and inorganic matter into smaller compounds, often producing rhizoremediation (plant and microbe interaction) (Sharma carbon dioxide and water as the final products (Gan et al. 2012). Other examples of bioremediation technologies are 2009). The principal mechanism for the aerobic bacterial land farming, bioventing, bioleaching, composting and the metabolism of PAHs is the initial oxidation of the benzene use of bioreactors, among others (Vidali 2001; Mohan et al. ring by the action of dioxygenase enzymes to form cis- 2006). Bioremediation technologies can be applied in situ or dihydrodiols. These dihydrodiols are dehydrogenated to ex situ, are relatively cost-effective, and use low-technology form dihydroxylated intermediates that may be further methods that are non-invasive and that generally have a metabolised via dihydroxy compounds (catechols) to car- high public acceptance (Sharma 2012; Castaldini 2008). bon dioxide and water (Habe and Omori 2003; Bamforth The success of bioremediation is governed by three and Singleton 2005; Wick et al. 2011). Fungal species, important factors—availability of efficient degraders, particularly members of the White Rot Fungi group, such as accessibility of contaminants and a conducive environment Phanerochaete chrysosporium, Bjerkandera adusta and (Chadrankant and Shwetha 2011). Several life forms are Pleurotus ostreatus, have been documented to efficiently known to efficiently degrade various kinds of hazardous biodegrade PAHs under aerobic conditions (Haritash and wastes; however, microorganisms are more successfully Kaushik 2009; Pozdnyakova 2012). They produce extra- used for the process of bioremediation because of their cellular lignin-degrading enzymes with low substrate spe- ubiquitous distribution in normal and extreme environ- cificity, which makes them ideal degraders of PAHs under ments, fast biomass growth, easy manipulation and high aerobic conditions (Haritash and Kaushik 2009; Gan et al. diversity of catabolic enzymes (Sharma 2012; Langenbach 2009). 2013). Bioremediation of PAH waste has been extensively studied at both the laboratory and commercial levels (Prince Anaerobic Biodegradation of PAHs 2010), and has also been implemented at a number of contaminated sites, such as the cleanup of the Exxon Valdez PAHs commonly contaminate anaerobic environments such oil spill in Prince William Sound, Alaska, in 1989, the as aquifers (Bakermans et al. 2002) and marine sediments Mega Borg spill off the Texas coast in 1990 and the Burgan (Coates et al. 1997). Aerobic environments such as con- oil field, Kuwait, in 1994 (Purwaningsih et al. 2002). The taminated soils, sediments and groundwater may also mechanisms through which microorganisms degrade PAHs develop anaerobic zones (Anderson and Lovely 1997; include metabolism or cometabolism, where cometabolism Bamforth and Singleton 2005). This is due to the organic has been shown to be especially relevant for the degradation contaminant stimulating the in situ microbial community, of mixtures of PAHs (Prince 2010). PAH degradation can resulting in the depletion of molecular oxygen during be either aerobic or anaerobic in nature, but the aerobic aerobic respiration. This oxygen is not replenished at the pathways, their kinetics, enzymatic and genetic regulation same rate as it is depleted, resulting in the formation of thereof is more extensively documented (Arun et al. 2010; anaerobic zones proximal to the contaminant source Wick et al. 2011). (Bamforth and Singleton 2005). Most biological transformations of aromatic ring struc- In such cases when oxygen is absent or limited, biode- tures are catalysed by mono or dioxygenases, and therefore gradation can occur anaerobically. Unlike aerobic Environmental Management biodegradation, anaerobic microorganisms use other avail- Micrococcus lylae-SBS661 are able to mineralise able substances such as nitrate, sulphate, iron, manganese acenaphthene. Species of Arthrobacter, Brevibacterium, and carbon dioxide as their electron acceptors to break Burkholderia, Mycobacterium, Pseudomonas and Sphin- down organic compounds into smaller constituents, often gomonas have been reported to degrade fluorene (Seo et al. producing carbon dioxide and methane as the final products 2009), while Mycobacterium has been extensively studied (Gan et al. 2009). Alternatively, some anaerobic micro- and is well known to mineralise HMW PAHs such as organisms can break down organic contaminants by fer- fluoranthene, pyrene and benzo(a)pyrene (Seo et al. 2009). mentation, whereby the organic contaminants act as the Strains in the genera Burkholderia, Pasteurella, Rhodo- electron acceptors (Gan et al. 2009; Ukiwe et al. 2013). coccus, Sphingomonas and Stenotrophomonas have been Primarily, anaerobic biodegradation is enforced when the isolated to degrade fluoranthene, using it as a sole carbon degree of contamination is very high, limiting oxygen flow and energy source (Mrozik et al. 2009; Seo et al. 2009). due to organic matter pore saturation or clogging of Rhodococcus sp., Bacillus cereus, Burkholderia cepacia, aggregates. As such, this technology is a promising reme- Cycloclasticus sp. P1, Pseudomonas fluorescens, Pseudo- diation process for accidental oil spills as well as remedia- monas stutzeri, Sphingomonas sp. VKM B-2434, Sphin- tion of water-submerged soil, such as paddy fields and gomonas paucimobilis and Stenotrophomonas maltophilia swamps. Furthermore, anaerobic biodegradation is antici- are all efficient pyrene degraders (Seo et al. 2009). pated to replace aerobic biodegradation since a large aera- Rehmann et al. (1998) isolated a Mycobacterium sp. strain tion area is not necessary to reduce total remediation cost. KR2 from a gaswork site, which was able to utilise pyrene Anaerobic bioremediation may also be applied for the as a sole carbon and energy source. The isolate metabolised treatment of deep underground soil and groundwater since up to 60% of the pyrene within 8 days at 20 °C. Pseudo- the process is not oxygen dependent (Bamforth and Sin- monas, Agrobacterium, Bacillus, Burkholderia, Sphingo- gleton 2005; Prince 2010; Karigar and Rao 2011). monas Rhodococcus, Mycobacterium, as well as a mixed culture of Pseudomonas and Flavobacterium species have all been reported to efficiently degrade B(a)P (Bhatnagar Bacterial Degradation of PAHs and Kumari 2013). Bacillus firmus has been reported to completely degrade benzo(b)fluoranthene, dibenzo(a,h) Organisms belonging to genera Pseudomonas, Alcanivorax, anthracene and indeno (1,2,3-c,d) pyrene (Bayoumi 2009). Microbulbifer, Sphingomonas, Micrococcus, Cellulomonas, The detailed pathways and mechanisms through which Dietzia, Gordonia, Marinobacter, Mycobacterium, Hae- bacterial species sequester PAH compounds have been mophilus, Rhodococcus, Paenibacillus, Bacillus, Aero- explored by numerous studies (Kanaly and Harayama 2000; monas, Burkholderia, Xanthomonas, Micrococcus, Peng et al. 2008; Seo et al. 2009) among others. Arthrobacter, Acinetobacter, Corynebacterium and Enter- obacter (Bayoumi 2009; Wu et al. 2013) have been docu- mented to effectively degrade PAH compounds. Fungal Degradation of PAHs Many studies have revealed that several bacterial species can utilise naphthalene as a sole source of carbon and Fungal species are very proficient PAH degraders because energy. These belong to the genera Alcaligenes, Bur- they are tolerant of high concentrations of recalcitrant kholderia, Mycobacterium, Polaromonas, Pseudomonas, compounds and are able to flourish in extreme conditions Ralstonia, Rhodococcus, Sphingomonas, Streptomyces (Seo such as at high temperature and under low pH conditions et al. 2009), as well as Bacillus firmus-APIS272, Pseudo- (Anastasi et al. 2013; Ding et al. 2013). Furthermore, the monas alcaligenes-DAFS311 and Bacillus subtilis-SBS526 fact that fungi form large, branching mycelia makes it (Bayoumi 2009). Anthracene has been reported to be possible for them to grow and distribute through a solid completely mineralised by Bacillus firmus-APIS272, matrix to degrade PAHs within contaminated areas (in situ) Bacillus subtilis-SBS526, Bacillus licheniformis, Bur- by virtue of secreting extracellular enzymes (Silva et al. kholderia cepacia-DAFS11 Pseudomonas alcaligenes- 2009; Bhattacharya et al. 2012). They possess enzyme DAFS311, Sphingomonas sp., Nocardia sp., Beijerinckia groups/systems such as lignin peroxidase, versatile perox- sp., Rhodococcus sp. and Mycobacterium sp. (Bayoumi idases, manganese dependent peroxidases, phenoloxidases

2009; Mrozik et al. 2009). Various Mycobacterium, Brevi- (lacases, tyrosinases), H2O2-producing enzymes, cyto- bacterium, Sphingomonas, Rhodotorula, Aeromonas, chrome P450 monooxygenase and epoxide hydrolase that Acidovorax, Arthrobacter and Comamonas species have efficiently oxidise PAHs, further enhancing their profi- been reported to metabolise phenanthrene (Romero et al. ciency (Pozdnyakova 2012; Ding et al. 2013). Due to the 1998; Mrozik et al. 2009; Seo et al. 2009). A study by irregular structure of lignin, lignolytic fungi produce Bayoumi (2009) showed that Bacillus subtilis-SBS526 and extracellular enzymes with very low substrate specificity, Environmental Management making them capable of degrading a wide array of pollu- did not identify the metabolites formed. B(a)P is known to tants (Juckpecha et al. 2012). White rot basidiomycetes be transformed to diols and quinones by marine algae in a fungi such as Phanerochaete chrysosporium, Trametes period of 5–6 days. Warshawsky et al. (1995) concluded versicolor, Cirnipellis stipitaria, Bjerkandera adusta and that only green algae almost completely metabolised B(a)P Pleurotus ostreatus have the ability to efficiently degrade to dihydrodiols, whereas yellow algae and blue-green algae lignin, a natural aromatic polymer that is structurally similar failed to metabolise the PAH compound. to most PAHs by the synthesis of lignin-modifying The green freshwater microalgae Selenastrum capri- enzymes. cornutum has been widely reported to be capable of Silva et al. (2009) reported that LMW PAHs were found degrading PAH compounds (Warshawsky et al. 1988, 1995; to be degraded most extensively by Aspergillus sp., Tri- Mueller et al. 1996; Tam et al. 2010). Warshawsky et al. chocladium canadense and Fusarium oxysporum. For (1995) reported the degradation of B(a)P by S. capri- HMW PAHs, maximum degradation was observed by Tri- cornutum and the production of 11,12-dihydrodiol and chocladium canadense, Aspergillus sp., Verticillium sp., 9,10-dihydrodiol under gold and white light, respectively. and Achremonium sp. The study also proved that fungi had An increase in light energy from gold to white to UV-A in a great capability to degrade a broad range of PAHs under the PAH-absorbing region led to a concomitant increase in low-oxygen conditions. In addition to biodegradation and B(a)P quinone production. A study by Chan et al. (2006) mineralisation of PAHs, fungal species are capable of reported the biodegradation of a mixture of PAHs, phe- adsorbing PAHs onto their hydrophobic cell wall (Tekere nanthrene, fluoranthene and pyrene, by S. capricornutum. et al. 2005). A study by Bhattacharya et al. (2012) showed The study identified metabolites monohydroxy- that Pleurotus ostreatus was able to degrade B(a)P and that phenanthrene, dihydroxyphenanthrene, as well as hydro- Phanerocheate chrysosporium showed significant biosorp- xylated fluoranthene and pyrene. Another study by Ke et al. tion and biodegradation of phenanthrene. The potential to (2010) showed that a consortium of five PAH compounds, biodegrade under micro-aerobic conditions can be explored fluorene, phenanthrene, fluoranthene, pyrene and B(a)P, to replenish saturated aquifers, waterlogged soils, paddy was efficiently biodegraded by S. capricornutum. Similarly, rice swamps and other anaerobic zones contaminated by Luo et al. (2014) reported the removal and transformation of PAHs. seven HMW PAH compounds, benz(a)anthracene, benzo(b) fluoranthene, benzo(k)fluoranthene, B(a)P, dibenzo(a,h) anthracene, indeno(1,2,3-c,d)pyrene and benzo(g,h,i) Algal Degradation of PAHs perylene, by S. capricornutum under white and gold light. Conversely, certain reports suggest that PAHs Prokaryotic and eukaryotic algal strains have great potential such as B(a)P, anthracene and benzo(a)anthracene are to degrade PAH compounds because they are ubiquitous in phototoxic to Selenastrum capricornutum (Cody et al. aquatic environments, which are common reservoirs of 1984). Similar studies with 3–4 ring PAH compounds have PAH contaminants (Labana et al. 2007). Prokaryotic and induced toxic responses in Anabaena flos-aquae, a blue- eukaryotic photoautotrophic marine algae [members of green alga. Other alga strains, including Scenedesmus cyanobacteria (blue-green), green algae and diatoms (red obliquus, Dunaliella sp. and Chlamydomonas sp., have and brown)] oxidise PAHs under photoautotrophic condi- also been reported to efficiently degrade PAHs (Semple tions to form hydroxylated intermediates (Mueller et al. et al. 1999). 1996). Naphthalene and phenanthrene have been reported to The potential for the adoption of algal–bacterial micro- be oxidised by cyanobacteria to metabolites similar to those cosms for the biodegradation of PAH pollutants has been produced by mammals and fungi (Narro et al. 1992a, b; explored (Warshawsky et al. 2007; Haritash and Kaushik Labana et al. 2007; Haritash and Kaushik 2009; Dwivedi 2009). When occurring in a consortium (particularly with 2012). The marine cyanobacterium Oscillatoria sp. strain bacteria), certain algae have been reported to enhance the JCM was shown to oxidise naphthalene via an arene oxide removal of fluoranthene and pyrene (Haritash and Kaushik intermediate that isomerised with concomitant non- 2009). A study by Borde et al. 2003 demonstrated the effect enzymatic rearrangement shift (Narro et al. 1992a). of bacterial–algal synergistic relationship on the biode- Another study by Narro et al. (1992b) demonstrated the gradation of phenanthrene. The green alga Chlorella sor- metabolism of phenanthrene by another marine cyano- okiniana was used in conjunction with bacterial species bacterium Agmenellum quadruplicatum PR6 to trans- Ralstonia basilensis and Acinetobacter haemolyticus and 9,10-dihydroxy, 9,10-dihydrophenanthrene and 1- was found to improve the biodegradation of the con- methocyphenanthrene. Freshwater microalgae, Chlorella taminant. The biodegradative potential of algal species have vulgaris, was reported by Patel and Tiwari (2015)to been extensively researched; however, there is still very degrade acenaphthene and fluoranthene; however, the study limited literature on the enzymes and the detailed Environmental Management degradation pathways for the degradation of individual potential or survival of an otherwise efficient PAH degrader PAH compounds by individual algal strains. (Samanta et al. 2002; Bustamante et al. 2011). It is possible to improve the bioremediation potential of such microorganisms prior to their field scale use by manipulating their genetic properties through genetic Phytoremediation engineering. There are available molecular tools and techniques that can efficiently modify remediation Phytoremediation is the use of green plant-based systems to genes (Paul et al. 2005; Fernández-Luqueño et al. 2011). degrade, assimilate, metabolise or detoxify pollutants in There is a proven relationship between the relative abun- contaminated soils, sediments and water. Phytoremediation dance of the genes involved in bioremediation and the is a fledgling technology that appears to have great potential potential for contaminant degradation (Schneegurt and to combat PAH pollution (Du et al. 2011). Kulpa 1998). However, sometimes, a microbial strain This technology makes use of naturally occurring pro- might possess the required gene for PAH remediation cesses by which plants and their microbial rhizosphere flora but the genes might not be fully expressed (Lovely degrade and/or sequester PAH pollutants (Pradhan et al. 2003). There are two options available for genetically sti- 1998). Research has shown that various grasses and legu- mulating microorganisms to achieve optimal bioremedia- minous plants are potential candidates for phytoremediation tion results: gene introduction or gene manipulation (Gentry of PAHs (Ukiwe et al. 2013). Some tropical plants have also et al. 2004). been reported to show effective degradation potential due to In the case of gene introduction, specific desired reme- inherent properties such as deep fibrous root system and diation genes are incorporated into plasmids or the chro- tolerance to high hydrocarbon concentration (Ukiwe et al. mosome of the target microorganism (Fernández-Luqueño 2013). Chen et al. (2003) reported that the tall fescue grass et al. 2011). This could be done with naturally occurring (Festuca arundinacea) and switch grass (Pannicum virga- plasmids, if they are transmissible, or by mating of a donor tum) are capable of sequestering about 38% of pyrene in with a target microorganism. This process involves no 190 days. Industrial hemp (Cannabis sativa) was reported recombinant DNA techniques and occurs commonly in to degrade B(a)P and chrysene, while rye grass (Lolium nature (Fernández-Luqueño et al. 2011). When an appro- multiflorum), bermuda grass (Cynodon dactylon) and water priate naturally occurring plasmid is not available, it hyacinth (Eichhornia crassipes) were reported to reduce may be necessary to clone the desired gene into a broad- about 45% of naphthalene in waste water in 7 days (Ukiwe host-range plasmid, which is then added to the donor et al. 2013). Although using plants for remediation of per- microorganism either through conjugation or through sistent contaminants may have advantages over other transformation. It might be important to incorporate the methods, many limitations exist for large-scale application, gene into the host chromosome to mitigate the potential for including that contaminant sensitivity may retard the gene transfer to other microorganisms (Fernández-Luqueño establishment of sufficient biomass to facilitate degradation et al. 2011). (Mohan et al. 2006). In the case of gene manipulation, selected genes are altered, so that they express optimal activity under varying environmental conditions. Conventionally, the gene of Genetically Engineered Microorganisms interest is first cloned into a laboratory microorganism such as Escherichia coli, which is easily manipulated and culti- There are microorganisms that exhibit physiological and vated in the laboratory. Factors such as the transcriptional metabolic versatility and have been established as proficient promoter and terminator sequences, the number of copies of PAH degraders. There are some others, which have no the gene in the host organism, as well as the stability of the proven capacity to degrade PAHs in contaminated envir- cloned gene protein may be manipulated to improve gene onmental matrices, but possess other desirable character- expression. After the genes have been altered, they are re- istics such as ability to withstand extreme conditions and introduced into the desired microorganisms. Although the produce certain desirable compounds like enzymes, sur- prospect of using exotic, designer microbes seems very factants and emulsifiers, which might enhance desorption appealing, the practical realisation is still constrained by (Alexander 1999; Mohan et al. 2006; Pazos et al. 2010). factors such as the interaction of modified organisms with Also, many times, microorganisms exhibit optimal profi- the local microbial population, the possibility of horizontal ciency in PAH degradation at the laboratory scale, but show transfer of genes to the indigenous microorganisms, their less efficiency at the field scale. This might be due to factors ability to retain activity, as well as environmental and such as adverse environmental conditions or other unfa- ecological safety concerns and regulatory constraints, in vourable conditions capable of inhibiting the biodegradative many countries. Environmental Management

Factors Affecting Bioremediation of PAHs diversity of the microbial flora in the contaminated matrix (Venosa and Zhu 2003; Das and Chandran 2011). Each The success of bioremediation depends on the microbial microorganism has peculiar temperature requirements out- population involved, degree of acclimation, accessibility of side which it cannot survive. At elevated temperature, contaminants, chemical structure of the compound, cellular protein denaturation results in enzyme dysfunction, dete- transport properties, chemical partitioning in growth media, rioration of the cell membrane and ultimate thermal death as well as a conducive environment for remediation (Brock and Madigan 1988; Pollard et al. 1994). At tem- (Swaranjit and Randhir 2010). Efficiency related to the peratures below the optimum for growth, microorganisms above factors is further dependent on pH, temperature, become unable to sequester substrates from their environ- oxygen, salinity, nature and pollution history of the con- ments because of lowered affinity. According to Nedwell taminated site, accessibility of nutrients, the occurrence of (1999), affinity for substrates generally decreases as tem- other toxic compounds (co-contamination) among others perature drops below the optimum for growth. This effect (Margesin and Schinner 2001a, b). Some environmental could be attributed to the stiffening of the lipids of the factors are capable of altering the rate of microbial uptake membrane below the temperature optimum, leading to and metabolism (the intrinsic activity of the cell), while decreased efficiency of transport proteins embedded in the some others can change the rate of contaminant transport to membrane (Nedwell 1999). Temperature also affects the the microorganisms (Bosma et al. 1997; Tang et al 2005). solubility of PAHs; solubility of PAHs increases with an increase in temperature, which in turn increases the bioa- vailability and mass transfer of the PAH molecules to pH microbial cells (Mohan et al. 2006). Temperature typically influences oxygen solubility, which decreases with Most important PAH-degrading microorganisms perform increasing temperature, and reduces the metabolic activities best when pH is neutral. However, fungi are known to be of aerobic microorganisms. Moreover, widely fluctuating more tolerant of acidic conditions (Al-Daher et al. 1998). seasonal and diurnal temperatures are generally unfavour- Many sites contaminated with PAHs are not at the optimal able to the sustenance of a stable, active PAH-degrading pH for bioremediation (Prince 2010). Many retired gaswork microbial population (Pollard et al. 1994). It is reported that, sites have been used as case studies; they often contain in soil, optimal temperature requirements range between significant quantities of demolition waste such as concrete 30–40 °C, in some freshwater environments 20–30 °C, and and brick. Leaching of this material increases the pH of the in marine environments 15–20 °C (Das and Chandran soil, resulting in less favourable conditions for microbial 2011). metabolism (Bamforth and Singleton 2005). In addition, the In spite of this, biodegradation of PAHs may occur over oxidation and leaching of coal spoil creates an acidic a versatile temperature range, since there are microbial environment through the release and oxidation of sulphides. species that can thrive at too low or too high temperatures, As the pH of contaminated sites can often be linked to the some of which have been documented to be active PAH pollutant, the indigenous microorganisms at the sites might degraders (Siron et al. 1995; Margesin and Schinner 2001a, not have the capacity to transform PAHs under acidic or b; Lau et al. 2003; Dash et al. 2013). Most studies, however, alkaline conditions. Therefore, it is common practice to tend to focus on mesophilic temperatures rather than the adjust the pH at these sites, by the addition of lime, nutrients efficiency of biodegradation under extreme temperature or fertilisers (Wilson and Jones 1993; Bamforth and Sin- conditions. Certain reports have shown that microorganisms gleton 2005). are capable of metabolising PAHs at extreme temperatures (Bamforth and Singleton 2005). For instance, naphthalene and phenanthrene degradation was reported from crude oil Temperature in seawater at temperatures as low as 0 °C (Siron et al. 1995). In contrast, the laccase and manganese peroxidase Temperature plays a significant role in determining the enzymes of ligninolytic fungi were reported to have a extent and rate of microbial PAH metabolism in the natural temperature optimum of ~50 and >75 °C, respectively, in environment (Pollard et al. 1994; Mohan et al. 2006). spent-mushroom compost during the degradation of PAHs, Temperature has a marked influence on equilibrium (parti- with over 90% degradation of the contaminating PAHs tion) and kinetic (rate) constraints, as illustrated by Van’t occurring at these temperatures (Lau et al. 2003). Another Hoff Isochore and Arrhenius equations, respectively (Pol- study by Müller et al. (1998) isolated microorganisms lard et al. 1994). PAH biodegradation is temperature capable of biodegrading naphthalene, phenanthrene and dependent because temperature directly affects the chem- anthracene under thermophilic conditions. The study indi- istry of the PAH compound, as well as the physiology and cated that metabolites produced differ significantly from Environmental Management those formed under mesophilic conditions. Also, naphtha- lipoproteins or complex mixtures of lipopeptides, glycolipids, lene degradation by a thermophilic Bacillus thermo- neutral lipids, and fatty acids) (Cameotra and Bollaga 2003; leovorans at 60 °C differs from the pathways known for Pacwa-Plociniczak et al. 2011). mesophilic bacteria (Annweiler et al. 2000). Several new Biosurfactants facilitate the transport of hydrophobic metabolites (2,3-dihydroxynaphthalene, 2-carboxycinnamic contaminants into the aqueous phase through specific acid, phthalic acid, benzoic acid) were found apart from interactions resulting in solubilisation, thereby increasing typical metabolites well known from naphthalene degrada- their bioavailability, which potentially makes them more tion by mesophiles. Other hydrocarbon-utilising bacteria susceptible to biodegradation (Maier and Soberón-Chávez such as Geobacillus, Alcanivorax and Pseudomonas sp. can 2000). They enhance hydrocarbon biodegradation by two also adapt to extreme temperature to maintain metabolic mechanisms (Pacwa-Plociniczak et al. 2011). The first activity (Kostka et al. 2011; Zhang et al. 2012). involves the increase of substrate availability for micro- organisms, while the other involves interaction with the cell surface, which increases the hydrophobicity of the surface, Salinity allowing hydrophobic substrates to associate more easily with bacterial cells (Mulligan and Gibbs 2004). By reducing High salinity levels can disrupt the tertiary protein structure surface and interfacial tensions, biosurfactants increase the of microbes, denature enzymes and dehydrate cells (Atlas surface areas of insoluble compounds, leading to increased and Bartha 1987; Pollard et al. 1994), thereby resulting in mobility and bioavailability of hydrocarbons. The capability reduced microbial metabolic rates (Dupraz and Visscher of biosurfactants and biosurfactant-producing bacterial 2005). Ward and Brock (1978) reported that the rates of strains to enhance the availability of organic contaminants hydrocarbon metabolism decreased with increasing levels of and biodegradation rates have been reported by many salinity (3.3–28.4%) for a series of hypersaline evaporation authors (Rahman et al. 2003; Inakollu et al. 2004). Obayori ponds of the great Salt Lake, Utah, United States. Another et al. (2009) investigated the biodegradative properties of study by Minai et al. (2012) showed that PAH degradation biosurfactant produced by Pseudomonas sp. LP1 strain on was more efficient in a medium containing 0% NaCl than in crude oil and diesel. The results obtained confirmed the 5% NaCl medium. To counter high salt conditions, dilution ability of strain LP1 to metabolise the hydrocarbon com- to lower salinity, removal of salt by reverse osmosis, ion ponents of crude and diesel oil. It was reported that 92.34% exchange or electrodialysis before biological treatment are degradation of crude oil and 95.29% removal of diesel oil common techniques used. However, this has significant cost was achieved during the investigation. The biodegradative implications (Margesin and Schinner 2001b). properties of biosurfactant-producing Brevibacterium sp. PDM-3 strain were tested by Reddy et al. (2010). The study showed that this strain could degrade 93.92% of phenan- Biosurfactants threne and is capable of degrading other PAHs such as anthracene and fluorene. Other microorganisms such as Biosurfactants are a structurally diverse group of surface- Bacillus subtilis, Pseudomonas aeruginosa and Torulopsis active compounds synthesised by a variety of microorgan- bombicola have been reported to produce surfactants such isms. They are amphiphilic molecules that have both as surfactin, rhamnolipid and sophorolipid, which are cap- hydrophobic and hydrophilic domains and are capable of able of improving PAH bioremediation (Kuyukina et al. lowering the surface and interfacial tension of a growth 2005; Cottin and Merlin 2007). medium (Pacwa-Plociniczak et al. 2011). They are usually Biosurfactants are applied in a variety of ways; the used as additives to counter the low aqueous solubility of molecules may either be added externally (influent, spray- PAHs and enhance the efficiency of bioremediation (Gan ing or injection) or produced on site, which seems espe- et al. 2009). They are environmentally friendly, biodegrad- cially promising in case of in situ treatment. In the latter able, less toxic and non-hazardous, highly reactive, and case, the production of biosurfactants may be obtained by active at extreme temperatures, pH and salinity (Das et al. bioaugmentation with appropriate microorganisms since 2008; Pacwa-Plociniczak et al. 2011). Biosurfactants are autochthonous microorganisms do not usually exhibit categorised by their chemical composition, molecular weight, satisfactory efficiency (Ławniczak et al. 2013). physicochemical properties, mode of action and microbial origin (Nguyen et al. 2008;Nievasetal.2008). Based on molecular weight they are divided into low-molecular mass Bioreactor biosurfactants (including glycolipids, phospholipids and lipopeptides) and HMW biosurfactants/bioemulsifiers A bioreactor is a manufactured or engineered vessel in (amphipathic polysaccharides, proteins, lipopolysaccharides, which a chemical process is carried out that involves Environmental Management organisms or biochemically active substances derived from Biofilm systems are especially suitable for the treatment such organisms (Atanu et al. 2011). This process can be of PAHs because of their high microbial biomass and ability either aerobic or anaerobic (Decker and Reski 2008), may to immobilise compounds (Singh et al. 2006). PAH bior- be in batch or continuous mode, and the type could be fixed emediation is also facilitated by enhanced gene transfer film or stirred tank (Wilson and Jones 1993). These bior- among biofilm organisms and by the increased bioavail- eactors are commonly cylindrical, ranging in size from litres ability of PAH compounds for degradation as a result of to cubic metres, and are often made of stainless steel or bacterial chemotaxis. Strategies for improving bioremedia- glass (Decker and Reski 2008). A bioreactor may also refer tion efficiency include genetic engineering to improve to a device or system meant to grow cells or tissues in the strains and chemotactic ability, as well as the use of mixed context of cell culture (Calabrò and Basile 2011). Bior- population biofilms and optimisation of physicochemical eactors have proven to be effective in remediating soil, and conditions (Singh et al. 2006). in some cases water, polluted with fuel hydrocarbons (oil, Biofilm-mediated PAH degradation presents a proficient gasoline, diesel) and organics (Das and Chandran 2011). and safer alternative to conventional remediation techniques Bioreactor design is dependent on the contaminant to be because cells in a biofilm have a better chance of adaptation remediated, the media that is contaminated, as well as cost and survival (especially during periods of stress) as they are constraints [International Union of Pure and Applied protected within the matrix (Decho 2000). Due to the close, Chemistry (IUPAC) 2014]. The microorganisms respon- mutually beneficial physical and physiological interactions sible for pollutant degradation are usually bacteria, but can among organisms in biofilms, the ability to utilise these also be fungi. Usually, bioreactor operation relies on the use PAH pollutants as carbon source by microorganisms is of native microflora already existing in the polluted media. improved and this improves the efficiency of biodegrada- However, whenever desirable indigenous microflora is tion (Singh et al. 2006). scarce or weak, or with no apparent capability of degrading the target compounds, researchers inoculate the reactors with enriched or acclimated consortia or strains (more Conclusions and Future Work commonly consortia) in the form of bioaugmentation (Lu et al. 2011). The introduction of specialised biomass may PAHs are ubiquitous pollutants that are introduced into the permit increased biodegradation of target pollutants as well environment majorly via anthropogenic activities such as as a more effective detoxification of the solid matrix, which refuse incineration and gasification of fossil fuels. This also significantly saves time (Robles-González et al. 2008). group of pollutants are of particular interest because they One of the distinct advantages of bioreactors is the ability possess characteristics such as hydrophobicity which makes to manipulate, monitor and control environmental and them highly stable and therefore, recalcitrant. Their toxicity operational variables to maximise biodegradation potential. to the environment, human health as well as other life forms Variables such as pH, temperature, nutrient levels, micro- has been thoroughly investigated and established. Levels of bial activity and dissolved oxygen (in the case of aerobic PAHs in the environment vary widely, depending on the reactors) are usually manipulated, thus optimising con- extent of industrial development, proximity of the con- taminant degradation (Fulekar and Geetha 2008; Robles- taminated sites to the pollution source and the mode of PAH González et al. 2008). transport. Compared to other remediation schemes avail- able, bioremediation has proven to be effective, eco-friendly and is publicly accepted. Bioremediation strategies and Biofilms protocols have been designed, optimised and adopted overtime to replenish PAH contaminated terrestrial and Biofilms are microbial colonies that form when single aquatic environments, yielding considerable success. Bac- microorganisms attach and aggregate on a hydrated surface terial, fungal and algal species capable of degrading PAH and undergo a “lifestyle switch”, giving up life as a single compounds have been isolated and utilised at both labora- cell to live on a surface in an adhesive cell matrix with other tory and field scale with significant strides achieved. Many microorganisms (Lemon et al. 2007). They are usually autochthonous microorganisms capable of competently resistant to antimicrobial agents, and studies have revealed transforming, degrading and utilising PAHs as sources of that cells within a particular biofilm are usually of diverse Carbon and energy have been isolated, identified and community properties (Lemon et al. 2007). Biofilms are characterised by numerous studies. The molecular tools capable of attaching to living and non-living surfaces, capable of manipulating the genetic component of microbial generating medical problems and altering industrial pro- species to suit bioremediation purposes have been resear- cesses, but more importantly play an important role in ched and some key aspects have been examined in this environmental clean-up. review. Some important environmental factors such as Environmental Management temperature, salinity and pH which influence microbial and terrestrial ecosystems is currently quite sparse, an biodegradation capabilities have been monitored and opti- important knowledge gap that may be useful in the selection mum requirements have been determined by several studies. of indigenous species for bioremediation studies. Also, Other relevant factors such as PAH bioavailability and there is a need to further characterise single-cell PAH persistence have also been investigated. The influence of metabolic pathways in pure cultures and properly under- biosurfactants and biofilms as well as the use of bioreactors stand the implications of co-metabolic reactions in coop- to biodegrade PAHs have also been widely researched. erative metabolic networks. Further identification and Although several workers have studied the levels, effects development of strategies to optimise functions and para- and remediation of PAH pollution in the environment, more meters that are pertinent for microbial mineralisation of research into this class of ubiquitous chemicals is desirable. PAHs in environmental matrices is required. Investigations USEPA has 16 PAHs listed as priority pollutants in water into microbial interactions with PAH-containing matrices and wastewaters and 24 as soil contaminants. Existing data and co-existent microbial communities are highly desirable. on the few that have been studied are quite scanty; more Finally, the review of literature suggests that further studies should be initiated for a more robust database that research is needed for in-depth investigation of PAH bior- will be useful for policy decisions. There is a need for emediation in microaerobic, anoxic, anaerobic, hypersaline continuous monitoring of all the priority PAHs in envir- and other extreme habitats. onmental samples since they have continued to be used in domestic activities and industrial applications. Considering Acknowledgements The authors wish to acknowledge the financial that PAHs are a common and abundant class of pollutants, support of the National Research Foundation (NRF), South Africa, there is a paucity of toxicity data for species that are con- through the Thuthuka Research Grant No. 84185 awarded to Prof B.O. Opeolu. tinuously exposed to PAHs. The fact that very low con- centrations of PAH exposure can ellicit serious adverse Compliance with Ethical Standards effects is particularly bothersome, because many popula- tions are simply unprotected. Up till now, there are still too Conflict of Interest The authors declare that they have no compet- few environmental statutes that contain regulatory restric- ing interests. tions designed to protect ecosystems from PAH pollution. The development of methods for the qualitative and quan- titative analyses of the non-extractable bound fractions of PAHs in soils is a research area that is not yet fully References explored. The ecological and human health implications of each compound singly and in mixtures are also not yet fully Agency for Toxic Substances and Disease Registry (ATSDR) (1995) Toxic Substances Portal-Polycyclic Aromatic Hydrocarbons understood. Efforts should be made to understand to what (PAHs) Public Health Statement for Polycyclic Aromatic extent PAHs occur in the environment as the solid crystals Hydrocarbons (PAHs). www.atsdr.cdc.gov/phs/phs.asp?id= that most studies regard. Future research efforts may con- 120&tid=25 sider investigating the toxicities of individual PAHs, mix- Agency for Toxic Substances and Disease Registry (ATSDR). (2011). Toxic Substances-Polycyclic Aromatic Hydrocarbons (PAH- tures of PAHs and mixtures of PAHs with other classes of s).”ATSDR home web http://www.atsdr.cdc.gov/substances/ pollutants in the environment. toxsubstance.asp?toxid=25. Accessed 6 Oct 2014 Indeed, bioremediation has proven to be an efficient and Al-Daher R, Al-Awadhi N, El-Nawawy A (1998) Bioremediation of safe technology that can be further exploited to ameliorate damaged desert environment using the windrow soil pile system in Kuwait. Environ Int 24:175–180 the consequences of PAH contamination. However, the Alexander M (1999) Biodegradation and bioremediation. Gulf successful application of bioremediation technologies is still Professional Publishing. 2nd Edition. CA, USA. ISBN: constrained by several factors, including but not limited to 9780120498611, p 141–176 inadequate monitoring tools to ensure the occurrence of Anastasi A, Tigini V, Varese GC (2013) The bioremediation potential of different ecophysiological groups of fungi. In: Goltapeh EM, active biodegradation processes as well as inaccurate risk Danesh YR, Varma A (eds) Fungi as bioremediators. Springer, assessment policies, in many systems and cases. It is Berlin, p 29–49 necessary to further explore the guild of (autochthonous) Anderson RT, Lovley DR (1997) Ecology and biogeochemistry of – microorganisms capable of ameliorating PAH pollution in situ groundwater remediation. Adv Microbial Ecol 15:289 350 Annweiler E, Richnow HH, Antranikian G, Hebenbrock S, Garms C, particularly in sites prone to direct PAH contamination. The Franke S, Francke W, Michaelis W (2000) Naphthalene degra- use of advanced, contemporary molecular methods to dation and incorporation of naphthalene-derived carbon into comprehend the microbiomes of PAH polluted sites is biomass by the thermophilic Bacillus thermoleovorans. Appl – revealing an increasing number of yet uncultured micro- Environ Microbiol 66:518 523 Arun K, Ashok M, Rajesh S (2010) Crude oil PAH constitution, organisms whose biodegradative potential remains unex- degradation pathway and associated bioremediation microflora: plored. Information on the microbial diversity of aquatic an overview. Int J Environ Sci 1(7):11–22 Environmental Management

Arey J, Atkinson R (2003) Photochemical reactions of PAHs in the term hydrocarbon pollution. World J Microbiol Biotechnol 29 atmosphere. In: Douben PET (ed) PAHs: an ecotoxicological (11):1989–2002 perspective. Wiley: West Sussex, UK, p 47–63 Beyer J, Sandvik M, Hylland K, Fjeld E, Egaas E, Aas E, Skare JU, Atanu KJ, Mahalakshmi DK, Sridhari G (2011) Integrated application Goksøyr A (1996) Contaminant accumulation and biomarker of bioprocess engineering and biotechniques for quality & bulk responses in flounder (Platichthys flesus L) and Atlantic cod drug manufacturing. J Bioequiv Availab 11:3–11 (Gadus morhua L) exposed by caging to polluted sediments in Atlas RM, Bartha R (1987) Microbial ecology: fundamentals and Sørfjorden, Norway. Aquat Toxicol 36(1–2):75–98 applications, 2nd edn. Benjamin/Cummings Publ.Co. Inc, Menlo Bhattacharya S, Angayarkanni J, Das A, Palaniswamy M (2012) park, CA, p 412–416 Mycoremediation of benzo(a)pyrene by Pleurotus ostreatus iso- Baek SO, Field RA, Goldstone ME, Kirk PW, Lester JN, Perry R lated from Wayanad district in Kerala, India. IOSR J Pharm Biol (1991) A review of atmospheric polycyclic aromatic hydro- Sci 2(2):84–93 carbons: sources, fate and behavior. Water Air Soil Pollut Bhatnagar S, Kumari R (2013) Bioremediation: A sustainable tool for 60:79–300 environmental management; a review. Annu Rev Res Bio 3 Baird SJ, Bailey EA, Vorhees DJ (2007) Evaluating human risk from (4):974–993 exposure to alkylated PAHs in an aquatic system. Hum Ecol Risk Boonchan S, Britz ML, Stanley GA (2000) Degradation and miner- Asses 13(2):322–338 alization of High-Molecular-Weight polycyclic aromatic hydro- Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aro- carbons by defined fungal-bacterial cocultures. Appl Environ matic hydrocarbons: current knowledge and future directions. J Microbiol 66(3):1007–1019 Chem Technol Biotechnol 80:723–736 Bosma TNP, Middeldorp PJM, Schraa G, Zehnder AJB (1997) Mass Bandowe BAM, Meusel H, Huang RJ, Ho K, Cao J, Hoffmann T, transfer limitation of biotransformation: quantifying bioavail- Wilcke W (2014) PM 2.5-bound oxygenated PAHs, nitro-PAHs ability. Environ Sci Technol 31(1):248–252 and parent-PAHs from the atmosphere of a Chinese megacity: Borde X, Guieysse B, Delgado O, Munnoz R, Hatti-Kaul R, Nugier- seasonal variation, sources and cancer risk assessment. Sci Total Chauvin C, Patin H, Mattiasson B (2003) Synergistic relation- Environment 473:77–87 ships in algal–bacterial microcosms for the treatment of aromatic Bakermans C, Hohnstock-Ashe AM, Padmanabhan S, Padmanabhan pollutants. Bioresour Technol 86:293–300 P, Madsen EL (2002) Geochemical and physiological evidence Brinkworth LC, Hodson PV, Tabash S, Lee P (2003) CYP1A induc- for mixed aerobic and anaerobic field biodegradation of coal tar tion and blue sac disease in early developmental stages of rain- waste by subsurface microbial communities. Microb Ecol bow trout (Oncorhynchus mykiss) exposed toretene. J Toxicol 44:107–117 Environ Health 66A:627–646 Baran S, Bielinska JE, Oleszcuzuka P (2004) Enzymatic activity in an Brock TD, Madigan MT (1988) Biology of microorganisms, 5th edn. airfield soil polluted with polycyclic aromatic hydrocarbons. Prentice Hall, Englewood cliffs, NJ Geoderma 118:221–232 Broman D, Näuf C, Lundbergh I, Zebühr Y (1990) An in situ study on Barron MG, Carls MG, Short JW, Rice SD (2003) Photoenhanced the distribution, biotransformation and flux of polycyclic aro- toxicity of aqueous phase and chemically dispersed, weathered matic hydrocarbons (pahs) in an aquatic food chain (seston‐ Alaska North Slope crude oil to Pacific herring eggs and larvae. Mytilus edulis L.‐Somateria mollissima L.) from the baltic: Environ Toxicol Chem 22:650–660 An ecotoxicological perspective. Environ Toxicol Chemi 9 Barret M, Carrère H, Delgadillo L, Patureau D (2010) PAH fate during (4):429–442 the anaerobic digestion of contaminated sludge: Do bioavail- Buha A (2011) Polycyclic aromatic hydrocarbons. Toxipedia, 1:12–16. ability and/or co-metabolism limit their biodegradation? Water Bustamante MA, Mier MV, Estrada JA, Domiguez CD (2011) Res 44(13):3797–3806 Nitrogen and potassium variation on contaminant removal for a Baumard P, Budzinski H, Garrigues P (1998a) Polycyclic aromatic vertical subsurface flow lab scale constructed wetland. Bioresour hydrocarbons in sediments and mussels of the western Medi- Technol 102(17):7745–7754 terranean Sea. Environ Toxicol Chem 17(5):765–776 Byeong-Kyu Lee (2010) Sources, distribution and toxicity of poly- Baumard P, Budzinski H, Garrigues P, Sorbe JC, Burgeot T, Bellocq J aromatic hydrocarbons (PAHs) in particulate matter, air pollution. (1998b) Concentrations of PAHs (polycyclic aromatic hydro- Vanda Villanyi (ed), InTech, doi:10.5772/10045. carbons) in various marine organisms in relation to those in Calabrò V, Basile A (2011) Fundamental membrane processes science sediments and to trophic level. Mar Poll Bull 36(12):951–960 and engineering. In advanced membrane science and technology Baumard P, Budzinski H, Garrigues P, Dizer H, Hansen PD (1999) for sustainable energy and environmental applications. Basile A Polycyclic aromatic hydrocarbons in recent sediments and mus- and Nunes SP (eds), Woodhead Publishing: Cambridge, UK and sels (Mytilus edulis) from the Western Baltic Sea: occurrence, Italy, p 3–18 bioavailability and seasonal variations. Mar Environ Res 47 Cameotra SS, Bollaga J (2003) Biosurfactant-enhanced bioremediation (1):17–47 of polycyclic aromatic hydrocarbons. Crit Rev Environ Sci Bayoumi RA (2009) Bacterial bioremediation of polycyclic aromatic Technol 33(2):111–126 hydrocarbons in heavy oil contaminated soil. J Appl Sci Res 5 Carls MG, Rice SD, Hose JE (1999) Sensitivity of fish embryos to (2):197–211 weathered crude oil: Low level exposure during incubation Beasley G, Kneale P (2002) Reviewing the impact of metals and PAHs causes malformations, genetic damage, and mortality in larval on macro-invertebrates in urban watercourses. Prog Phys Geogr Pacific herring (Clupea pallasi). Environ Toxicol Chem 26(2):236–270 18:481–493 Beazley M, Martinez R, Rajan S, Powell J, Piceno Y, Tom L, Castaldini F (2008) Bioremediation of PAHs- limitations and solu- Anderson G, Hazen T, Nostrand J, Zhou J, Mortazavi B, Sobecky tions. Universita Di Bologna Alma Mater Digital Library. Doc- P (2012) Microbial community analysis of a coastal salt marsh toral dissertation. Accessed 26 Jun 2013 affected by the Deepwater horizon oil spill. PloS ONE 7(7): Canadian Council of Ministers of the Environment (CCME) (1999). A e41305. doi:10.1371/journal.pone.0041305 protocol for the derivation of ecological effects-based and human Benedek T, Vajna B, Tancsics A, Mariaaligeti K, Lanyi S, Mathe I health-based soil quality criteria for contaminated sites, Ottawa. (2013) Remarkable impact of PAHs and TPHs on the richness CCME subcommittee on Environmental quality criteria for con- and diversity of bacterial species in surface soils exposed to long taminated sites, Environment Canada Environmental Management

Canadian Council of Ministers of the Environment (CCME). 2008. Dennis MJ, Massey RC, Cripps G, Venn N, Howarth N, Lee G (1991) Canadian Soil Quality Guidelines: Carcinogenic and Other Factors affecting the polycyclic aromatic hydrocarbons content of Polycyclic Aromatic Hydrocarbons (PAHs) (Environmental and cereals, fats and other food products. Food Addit Contam Human Health Effects). Canadian Council of Ministers of the 8:517–530 Environment, Ottawa, Canada de Vos RH, van Dokkum W, Schouten A, de Jong-Berkhout P (1990) Centers for Disease Control and Prevention (CDC) (2009) Fourth Polycyclic aromatic hydrocarbons in Dutch total diet samples National Report on Human Exposure to Environmental Chemi- (1984–1986). Food Chem Toxicol 28(4):263–268 cals. Accessed 22 Aug 2014 Ding J, Chen B, Zhu L (2013) Biosorption and biodegradation of Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydro- polycyclic aromatic hydrocarbons by Phanerochaete chrysos- carbons. Biodegradation 3:351–368 porium in aqueous solution. Envir Chem 58(6):613–621 Chadrankant SK, Shwetha SR (2011) Role of microbial enzymes in Duedahl-Olesen L, White S, Binderup ML (2006) Polycyclic aromatic the bioremediation of pollutants: A Review. Enzyme Res 11:1–11 hydrocarbons (PAHs) in Danish smoked fish and meat products. Chan SMN, Luan T, Wong MH (2006) Removal and biodegradation Polycyclic Aromat Compd 26:163–164 of polycyclic aromatic hydrocarbons by Selenastrum capri- Du W, Sun Y, Cao L, Huang J, Ji R, Wang X, Wu J, Zhu J, Guo H cornutum. Environ Toxicol Chem 25(7):1772–1779 (2011) Environmental fate of phenanthrene in lysimeter planted Chen YC, Banks MK, Schwab AP (2003) Pyrene degradation in the with wheat and rice in rotation. J Hazard Mater 188:408–413 rhizosphere of tall fescue (Festuca arundinacea) and switchgrass Dupraz C, Visscher PT (2005) Microbial lithification in marine stro- (Panicum Virgatum). Environ Sci Technol 37:5778–5782 matolites and hypersaline mats. Trends Microbiol 13(9):429–438 Choi J, Oris JT (2003) Assessment of the toxicity of anthracene photo- Dwivedi S (2012) Bioremediation of heavy metal by algae: current and modification products using the topminnow (Poeciliopsis lucida) future perspective. J Adv Lab Res Biol 3(3):195–199 hepatoma cell line (PLHC-1). Aquat Toxicol 65(3):243–251 Environment Ontario (1992) Polycyclic Aromatic Hydrocarbons: Choi H, Harrison R, Komulainen H, Delgado Saborit JM (2010) sources, fate and levels in air, water, soil, sediments, sludge and Polycyclic aromatic hydrocarbons. WHO Guidelines for Indoor food in Ontario. Report Number 0772992819, p 25–56. doi:10. Air Quality: Selected Pollutants. World Health Organization, 5962/bhl.title.20226 Geneva, p 289–345 Eisler R (2007) Polycyclic aromatic hydrocarbons In Eisler’s Ency- Chung SY, Yettella RR, Kim JS, Kwon K, Kim MC, Min DB (2011) clopedia of Environmentally Hazardous Priority Chemicals. Effects of grilling and roasting on the levels of polycyclic aromatic Elsevier, The Netherlands, p 645–676 hydrocarbons in beef and pork. Food Chem 129(4):1420–1426 Falahatpisheh MH, Donnelly KC, Ramos KS (2001) Antagonistic Coates JD, Woodard J, Allen J, Philip P, Lovely DR (1997) Anaerobic interactions among nephrotoxic polycyclic aromatic hydro- degradation of polycyclic aromatic hydrocarbons and alkanes in carbons. J Toxicol Environ Health 62(7):543–60 petroleum-contaminated marine harbour sediments. Appl Environ Farhadian A, Jinap S, Abas F, Sakar ZI (2010) Determination of Microbiol 63:3589–3593 polycyclic aromatic hydrocarbons in grilled meat. Food Control Cody TE, Radike MJ, Warshawsky D (1984) The phototoxicity of 21(5):606–610 benzo(a)pyrene in the green alga Selenastrum capricornutum. Fernández-Luqueño F, Valenzuela-Encinas C, Marsch R, Martínez- Environ Res 35(1):122–132 Suárez C, Vázquez-Núñez E, Dendooven L (2011) Microbial Coover MP, Simms RC (1987) Haz WastePlease provide article title in communities to mitigate contamination of PAHs in soil—possi- the reference Coover and Simms (1987). Haz Mat 4:69–82 bilities and challenges: a review. Environ Sci Pollut Res Cornelissen G, Gustafsson Ö, Bucheli TD, Jonker MT, Koelmans AA, 18:12–30 van Noort PC (2005) Extensive sorption of organic compounds to Fismes J, Perrin-Ganier C, Empereur-Bissonnet P, Morel JL (2002) black carbon, coal, and kerogen in sediments and soils: Soil-to-root transfer and translocation of polycyclic aromatic mechanisms and consequences for distribution, bioaccumulation, hydrocarbons by vegetables grown on industrial contaminated and biodegradation. Environ Sci Technol 39(18):6881–6895 soil. J Environ Qual 31(5):1649–1656 Cottin NC, Merlin G (2007) Study of pyrene biodegradation capacity Fulekar MH, Geetha M (2008) Bioremediation of chlorpyrifos in in two types of solid media. Sci Total Environ 380:116–123 surface soil treatment unit using microbial consortium. Can J Pure Couch JA, Harshbarger JC (1985) Effects of carcinogenic agents on Appl Sci 2(2):267–273 aquatic animals: An environmental and experimental overview. J Gan S, Lau EV, Ng HK (2009) Remediation of soils contaminated Environ Sci Health C Environ Carcinog Ecotoxicol Rev 3 with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater (1):63–105 172(2–3):532–549 Das P, Mukherjee S, Sen R (2008) Improved bioavailability and Garcia-Londoño VA, Garcia LP, Scussel VM (2013) Polycyclic aro- biodegradation of a model poly aromatic hydrocarbon by a bio- matic hydrocarbons in milk powders marketed in Argentina and surfactant producing bacterium of marine origin. Chemosphere Brazil. Food Addit Contam 30(9):1573–1580 72:1229–1234 Geffard O, Geffard A, His E, Budzinski H (2003) Assessment of the Das N, Chandran P (2011) Microbial degradation of petroleum bioavailability and toxicity of sediment-associated polycyclic hydrocarbon contaminants: An overview. Biotechnol Res Int aromatic hydrocarbons and heavy metals applied to Crassostrea 941810:1–13 gigas embryos and larvae. Mar Pollut Bull 46(4):481–490 Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S (2013) Gentry TJ, Rensing C, Pepper IL (2004) New approaches for Marine bacteria: potential candidates for enhanced bioremedia- bioaugmentation as a remediation technology. Crit Rev Environ tion. Appl Microbiol Biotechnol 97:561–571 Sci Technol 34:447–494 Decho AW (2000) Microbial biofilms in intertidal systems: An over- Girellia AM, Speratia D, Tarolab AM (2014) Determination of poly- view. Cont Shelf Res 20:1257–1273 cyclic aromatic hydrocarbons in Italian milk by HPLC with Decker EL, Reski R (2008) Current achievements in the production of fluorescence detection. Food Addit Contam Part A 31 complex biopharmaceuticals with moss bioreactors. Bioprocess (4):703–710 Biosyst Eng 31:3–9 Gomaa EA, Gray JI, Rabie S, Lopez-Bote C, Booren AM (1993) Dennis MJ, Massey RC, McWeeny DJ, Knowles ME (1983) Analysis Polycyclic aromatic hydrocarbons in smoked food products and of polycyclic aromatic hydrocarbons in UK total diets. Fd Chem commercial liquid smoke flavourings. Food Addit Contam Toxic 21:569–574 10:503–521 Environmental Management

Gomes A, Santos C, Almeida J, Elias M, Roseiro LC (2013) Effect of Ji X, Ripp SA, Layton AC, Sayler GS, De Bruyn JM (2013) Assessing fat content, casing type and smoking procedures on PAHs con- long term effects of bioremediation: soil bacterial communities 14 tents of Portuguese traditional dry fermented sausages. Food years after polycyclic aromatic hydrocarbon contamination and Chem Toxicol 58:369–374 introduction of a genetically engineered microorganism. J Bior- Grotte M, Schuurmann G, Altenburger R (2005) Modeling photo emed Biodeg doi:10.4172/2155-6199.1000209 induced algae toxicity of polycyclic aromatic hydrocarbons. Johnsen A, Karlson U (2005) PAH degradation capacity of soil Environ Sci Technol 39:4141–4149 microbial communities: Does it depend on PAH exposure? Guillen F, Gómez-Toribio V, Martıneź MJ, Martıneź AT (2000) Microb Ecol 50:488–495 Production of hydroxyl radical by the synergistic action of fungal Jones KC, Alcock RE, Johnson DL, Semple KT, Woolgar PJ laccase and aryl alcohol oxidase. Arch Biochem Biophys (1996) Organic chemicals in contaminated land: analysis, 383:142–147 significance and research priorities. Land Contam Reclamat Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon 4(3):189–198 metabolism in diverse aerobic bacteria. Biosci Biotechnol Bio- Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight chem 67(2):225–243 polycyclic aromatic hydrocarbons: a review of the microbial Hajisamoh A (2013) Pollution Levels of 16 Priority PAHs in the major degradation of benzo(a)pyrene. Int Biodeterior Biodegradation 45 Rivers of Southern Thailand. J Chem 2(1):7–11 (1–2):57–88 Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic Juckpecha K, Pinyakonga O, Rerngsamrana P (2012) Degradation of aromatic hydrocarbons (PAHs): A review. J Hazard Mater 169 polycyclic aromatic hydrocarbons by newly isolated Curvularia (1):1–15 sp. F18, Lentinus sp. S5 and Phanerochaete sp. T20. Sci Asia Harvey RG (1997) Polycyclic aromatic hydrocarbons: Chemistry and 38:147–156 Carcinogenicity. In: Neilson AH (ed) Cambridge Monographs on Kaag NHBM, Foekema EM, Scholten MCTh, van Straalen NM (1997) Cancer Research. Wiley, New York, NY, pp 667–670 Comparison of contaminant accumulation in three species of Harvey RG (1998) Environmental chemistry of PAHs. In: Neilson AH marine invertebrates with different feeding habits. Environ Tox- (ed) The handbook of environmental chemistry: PAHs and rela- icol Chem 16:837–842 ted compounds. Springer, New York, NY, p 1–54 Kamaljit B, Gurpal ST, Tait C, Lena M (2010) Polycyclic aromatic Hatch AC, Burton GA (1999) Photo-induced toxicity of PAHs to hydrocarbons in urban soils of different land uses in Miami, Hyalella azteca and Chironomus tentans: effects of mixtures and Florida. Soil Sediment Contam 19:231–243 behavior. Environ Pollut 106(2):157–167 Kanaly RA, Harayama S (2000) Biodegradation of High-Molecular- Hatzinger PB, Alexander M (1995) Effect of aging on chemicals in Weight Polycyclic Aromatic Hydrocarbons by Bacteria. J Bac- soil on their biodegradability and extractability. Environ Sci teriol 182(8):2059–2067 Technol 29:537–545 Karigar CS, Rao SS (2011) Role of microbial enzymes in the bior- Heijden SAVD, Jonker MT (2009) PAH bioavailability in field sedi- emediation of pollutants: a Review. Enzyme Res 1:1–11 ments: comparing different methods for predicting in situ Karthikeyan R, Bhandari A (2001) Anaerobic biotransformation of bioaccumulation. Environ Sci Technol 43(10):3757–3763 aromatic and polycyclic aromatic hydrocarbons in soil micro- Hellou J, Leonard J, Collier TK, Ariese F (2006) Assessing PAH cosms: A review. J Hazard Subst Res 3:3–19 exposure in feral finfish from the Northwest Atlantic. Mar Pollut Karyab H, Yunesian M, Nasseri S, Mahvi AH, Ahmadkhaniha R, Bull 52(4):433–441 Rastkari N, Nabizadeh R (2013) Polycyclic aromatic hydro- Hjorth M, Vester J, Henriksen P, Forbes V, Dahllof I (2007) Func- carbons in drinking water of Tehran, Iran. J Environ Health Sci tional and structural responses of marine planktonic food web to Eng 11:25. doi: 10.1186/2052-336X-11-25 pyrene contamination. Mar Ecol Prog Ser 338:21–31 Kayal SI, Connell DW (1990) Partitioning of unsubstituted polycyclic Hose JE, Brown ED (1998) Field applications of the piscine anaphase aromatic hydrocarbons between surface sediments and the water aberration test: lessons from the Exxon Valdez oil spill. Mutat column in the Brisbane river estuary. Mar Freshwater Res 41 Res 399:167–178 (4):443–456 Howard PH, Meylan WM (1997) Handbbok of Physical Properties of Ke L, Luo L, Wang P, Luan T, Tam NF (2010) Effects of metals on Organic Chemicals. CRC Press, Inc, Boca Raton, FL, p 288 biosorption and biodegradation of mixed polycyclic aromatic Husain A, Naeemi E, Dahsti B, Al-Omirah H, Al-Zenki S (1997) hydrocarbons by a freshwater green alga Selenastrum capri- Polycyclic aromatic hydrocarbons in food products originating cornutum. Bioresour Technol 101(18):6950–6961 from locally reared animals in Kuwait. Food Addit Contam Ke CL, Gu YG, Liu Q, Li LD, Huang HH, Cai N, Sun ZW (2017) 14:295–299 Polycyclic aromatic hydrocarbons (PAHs) in wild marine Ikenaka Y, Sakamoto M, Nagata T, Takahashi H, Miyabara Y, organisms from South China Sea: Occurrence, sources, and Hanazato T, Ishizuka M, Isobe T, Kim JW, Chang KH (2013) human health implications. Mar Poll Bull doi:10.1016/j.ma Effects of polycyclic aromatic hydrocarbons (PAHs) on an rpolbul.2017.02.018 aquatic ecosystem: acute toxicity and community level toxic Kelly BC, Ikonomou MG, Blair JD, Morin AE, Gobas FA (2007) impact tests of benzo(a)pyrene using lake zooplankton commu- Food web–specific biomagnification of persistent organic pollu- nity. J Toxicol Sci 38(1):131–136 tants. Science 317(5835):236–239 Inakollu S, Hung H, Shreve GS (2004) Biosurfactant enhancement Kim SJ, Kweon O, Jones RC, Freeman JP, Edmondson RD, Cerniglia of microbial degradation of various structural classes of CE (2007) Complete and integrated pyrene degradation pathway hydrocarbon in mixed waste systems. Environ Eng Sci in Mycobacterium vanbaalenii PYR-1 based on systems biology. 21:463–469 J Bacteriol 189:464–472 International Programme on Chemical Safety (IPCS) (2000) Human Kim KH, Jahan SA, Kabir E, Brown RJC (2013) A review of airborne exposure assessment; Environmental Health Criteria, 214. www. polycyclic aromatic hydrocarbons (PAHs) and their human health inchem.org/documents/ehc/214. Accessed 14 Feb 2014 effects. Environ Int 60:71–80 International Union of Pure and Applied Chemistry (IUPAC) (2014) Kishikawa N, Wada M, Kuroda N, Akiyama S, Nakashima N (2003) Compendium of Chemical Terminology, Gold book ‘Bioreactor’. Determination of polycyclic aromatic hydrocarbons in milk 2nd edition, Version 2.33 p 166. sample by high-performance liquid chromatography with fluor- escence detection. J Chromatogr Part B 789:257–264 Environmental Management

Kostka JE, Prakash O, Overholt WA, Green SJ, Freyer G, Canion A Lundestedt S (2003) Analysis of PAHs and their transformation pro- et al. (2011) Hydrocarbon-degrading bacteria and the bacterial ducts in contaminated soil and remedial processes. Dissertation, community response in gulf of Mexico beach sands impacted by Umea University the Deepwater Horizon oil spill. Appl Environ Microbiol Lundstedt S, White PA, Lemieux CL, Lynes KD, Lambert IB, Öberg 77:7962–7974 L, Haglund P, Tysklind M (2007) Sources, fate, and toxic hazards Kotterman MJJ, Rietberg HJ, Hage A, Field JA (1998) Polycyclic of oxygenated polycyclic aromatic hydrocarbons (PAHs) at PAH- aromatic hydrocarbon oxidation by the white-rot fungus Bjer- contaminated sites. AMBIO: A. J Human Environ 36(6):475–485 kandera sp. strain BOS55 in the presence of nonionic surfactants. Luo L, Wang P, Lin L, Luan T, Ke L, Tam NF (2014) Removal and Biotechnol Bioeng 57(2):220–227 transformation of high molecular weight polycyclic aromatic Kuyukina MS, Ivshina IB, Makarov SO, Litvinenko LV, Cunningham hydrocarbons in water by live and dead microalgae. Process CJ, Philip CJ (2005) Effect of biosurfactants on crude oil deso- Biochem 49(10):1723–1732 rption and mobilization in a soil system. Environ Int 31:155–161 Lu X, Reible DD, Fleeger JW (2006) Bioavailability of polycyclic Kweon O, Kim SJ, Holland RD, Chen H, Kim DW, Gao Y, Yu LR, aromatic hydrocarbons in field-contaminated Anacostia River Baek S, Baek DH, Ahn H (2011) Polycyclic aromatic hydro- (Washington, DC) sediment. Environ Toxicol Chem 25 carbon metabolic network in Mycobacterium vanbaalenii PYR-1. (11):2869–2874 J Bacteriol 193:4326–4337 Lu JC, Li ZT, Hussain K, Yang GK (2011) Bioremediation: The new Labana S, Kapur M, Malik DK, Prakash D, Jain RK (2007) Diversity, directions of oil spill cleanup. Middle-East J Sci Res 7 biodegradation and bioremediation of polycyclic aromatic hydro- (5):738–740 carbons. In: Sing SN, Tripathi RD (eds) Environmental bior- Mackay D, Fraser A (2000) Bioaccumulation of persistent organic emediation technologies, Springer, Berlin, Heidelberg, p 409–443 chemicals: Mechanisms and models. Environ Pollut 110:375–391 Lampi MA, Gurska J, McDonald KI, Xie F, Huang XD, Dixon DG, Maier RM, Pepper IL, Gerba CP (2000) Environmental Microbiology. Greenberg BM (2006) Photoinduced toxicity of polycyclic aro- Academic Press, New York, NY, p 112–132 matic hydrocarbons to Daphnia magna: Ultraviolet‐mediated Maier RM, Soberón-Chávez G (2000) Pseudomonas aeruginosa effects and the toxicity of polycyclic aromatic hydrocarbon rhamnolipids: biosynthesis and potential applications. Appl photoproducts. Environ Toxicol Chem 25(4):1079–1087 Microbiol Biotechnol 54:625–633 Langenbach T (2013) Persistence and bioaccumulation of persistent Maisto G, De Nicola F, Iovieno P, Prati MV, Alfani A (2006) PAHs organic pollutants (POPs). In: Yogesh B, Patil, Prakash R (eds) and trace elements in volcanic urban and natural soils. Geoderma Agricultural and biological sciences; Applied bioremediation- 136:20–27 active and passive approaches. Rijeka, Croatia, p 223–229 Makkar RS, Rockne KJ (2003) Comparison of synthetic surfactants Latimer JS, Zheng J (2003) The sources, transport and fate of PAHs in and biosurfactants in enhancing biodegradation of polycyclic the marine environment. In: Douben PE (ed) PAHs: An ecotox- aromatic hydrocarbons. Environ Toxicol Chem 22 icology perspective. Wiley, West Sussex, UK, p 9–33 (10):2280–2292 Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost Maliszewska-Kordybach B (1999) Sources, concentrations, fate and to bioremediate PAH-contaminated samples. Chemosphere effects of polycyclic aromatic hydrocarbons (PAHs) in the 52:1539–1546 environment. Part A: PAHs in Air. Pol J Environ Stud 8 Ławniczak Ł, Marecik R, Chrzanowski Ł (2013) Contributions of (3):131–136 biosurfactants to natural or induced bioremediation. Appl Manoli E, Samara C (1999) Polycyclic aromatic hydrocarbons in Microbiol Biotechnol 97(6):2327–2339 natural waters: sources, occurrence and analysis. Trends Analyt Lawrence JF, Weber DF (1984) Determination of polycyclic aromatic Chem 18(6):417–428 hydrocarbons in some Canadian commercial fish, shellfish, and Margesin R, Schinner F (2001a) Bioremediation (natural attenuation meat products by liquid chromatography with confirmation by and biostimulation) of diesel-oil-contaminated soil in alpine gla- capillary gas chromatography-mass spectrometry. J Agric Food cier skiing area. Appl Environ Microbiol 67(7):3127–3133 Chem 32:789–794 Margesin R, Schinner F (2001b) Biodegradation and bioremediation of Layshock JA, Wilson G, Anderson KA (2010) Ketone and quinone‐ hydrocarbons in extreme environments. Appl Environ Microbiol substituted polycyclic aromatic hydrocarbons in mussel tissue, 56:650–663 sediment, urban dust, and diesel particulate matrices. Environ Martineau D, Lemberger K, Dallaire A, Labelle P, Lipscomb T, Toxicol Chem 29(11):2450–2460 Michel P, Mikaelian I (2002) Cancer in wildlife, a case study: Lemon KP, Higgins DE, Kolter R (2007) Flagella-mediated motility is Beluga from the St. Lawrence Estuary, Québec, Canada. Environ critical for Listeria monocytogenes biofilm formation. J Bacteriol Health Perspect 110:285–292 189:4418–4424 Mascarelli A (2010) Deepwater horizon: After the oil. Nat News Lenicek J, Sekyra M, Pandey P, Citkova M, Be-Nes I, Novotna J, 467:22–24. doi:10.1038/467022a Kociano S, Helaskova J, Simonova A (1997) Polycyclic aromatic Mastrangela G, Fadda E, Marzia V (1999) Polycyclic aromatic hydrocarbon at “program teplice” sites in the Czech Republic. hydrocarbons and cancer in man. Environ Health Perspect Toxicol Environ Chem 58:25–35 104:1166–1170 Liang Y, Van Nostrand JD, Deng Y, He Z, Wu L, Zhang X, Li G, McElroy AE, Leitch K, Fay A (2000) A survey of in vivo benzo[a] Zhou J (2011) Functional gene diversity of soil microbial com- pyrene metabolism in small benthic marine invertebrates. Mar munities from five oil-contaminated fields in China. ISME J Environ Res 50:33–38 5:403–413 McGrath TE, Chan WG, Hajaligol MR (2003) Low temperature Liu J, Zhang L, Winteroth L, Garcia M, Weiman S, Wong J, Sunwoo mechanism for the formation of polycyclic aromatic hydro- J, Nadeou K (2013) Epigenetically mediated pathogenic effects of carbons from the pyrolysis of cellulose. J Anal Appl Pyrol 66 phenanthrene on regulatory T cells. J Toxicol 12:104–116 (1–2):51–70 Lovley DR (2003) Cleaning up with genomics: applying molecular Meador JP, Stein JE, Reichert WL, Varanasi U (1995) Bioaccumula- biology to bioremediation. Nat Rev Microbiol 1:35–44 tion of polycyclic aromatic hydrocarbons by marine organisms. Luch A (2005) The carcinogenic effects of polycyclic aromatic Rev Environ ContamToxicol 143:79–165 hydrocarbons. Imperial College Press, London, p 223–300. ISBN Meador JP (2003) in Marine Invertebrates. PAHs: An ecotoxicological 1-86094-417-5 perspective, 147–171 Environmental Management

Meador JP, Sommers FC, Ylitalo GM, Sloan CA (2006) Altered Nfon E, Cousins IT, Broman D (2008) Biomagnification of organic growth and related physiological responses in juvenile Chinook pollutants in benthic and pelagic marine food chains from the salmon (Oncorhynchus tshawytscha) from dietary exposure to Baltic Sea. Sci Total Environ 397(1):190–204 polycyclic aromatic hydrocarbons (PAHs). Can J Fish Aquat Sci Nguyen TT, Youssef NH, McInerney MJ, Sabatini DA (2008) 63(10):2364–2376 Rhamnolipid biosurfactant mixtures for environmental remedia- Meador JP (2012) Polycyclic Aromatic Hydrocarbons. Reference tion. Water Res 42:1735–1743 module in earth systems and environmental sciences. Encyclo- Nievas ML, Commendatore MG, Estevas JL, Bucalá V (2008) Bio- pedia Ecol 2008:2881–2891 degradation pattern of hydrocarbons from a fuel oil-type complex Menichini E, Bocca B (2003) Em Encyclopedia of Food Sciences and residue by an emulsifier-producing microbial consortium. J Nutrition. In: Caballero B, Trugo LC, Finglas PM (eds) Ency- Hazard Mater 154:96–104 clopaedia of food sciences and nutrition. Academic Press, Nigam PS, Singh A (2011) Production of liquid biofuels from Amsterdam, The Netherlands, p 4616 renewable resources. Prog Energy Combust Sci 37(1):52–68 Minai TD, Minoui S, Hefatmanesh A (2012) Effect of salinity on Nkansah MA (2012) Environmental remediation: removal of poly- biodegradation of polycyclic aromatic hydrocarbons (PAHs) of cyclic aromatic hydrocarbons. Dissertation, University of Bergen heavy crude oil in soil. Bull Environ Contam Toxicol 82: Obayori OS, Ilori MO, Adebusoye SA, Oyetibo GO, Omotayo AE, 179–184 Amund OO (2009) Degradation of hydrocarbons and biosurfac- Motelay-Masseia A, Garban B, Tiphagne-larcher K, Chevreuil M, tant production by Pseudomonas sp. strain LP1. World J Ollivon D (2006) Mass balance for polycyclic aromatic hydro- Microbiol Biotechnol 25:1615–1623 carbons in the urban watershed of Le Havre (France): Transport Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘pristine’ and fate of PAHs from the atmosphere to the outlet. Water Res 40 soils from different climatic regions. J Biorem Biodegrad 1 (10):3–11 (6):1–11 Mohan SV, Kisa T, Ohkuma T, Kanaly RA, Shimizu Y (2006) Okoli CG, Ogbuagu DH, Madu GS, Njoku-Tony RF (2011) Proximal Bioremediation technologies for treatment of PAH-contaminated input of polynuclear aromatic hydrocarbons (PAHs) in ground- soil and strategies to enhance process efficiency. Rev Environ Sci water sources of Okrika Mainland, Nigeria. Sci Res 2(6):848–854 Biotechnol 5:347–374 Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy Morrison HA, Gobas FA, Lazar R, Haffner GD (1996) Development metals in soil: Impact on microbial biodegradation of organic and verification of a bioaccumulation model for organic con- compounds and possible improvement strategies. Int J Mol Sci 14 taminants in benthic invertebrates. Environ Sci Technol 30 (5):197–228 (11):3377–3384 Olatunji OS, Fatoki OS, Opeolu BO, Xhimba BJ (2014) Determination Mrozik A, Piotrowska-Seget Z, Labuzek S (2009) Bacterial degrada- of polycyclic aromatic hydrocarbons (PAHs) in processed meat tion and bioremediation of polycyclic aromatic hydrocarbons. Pol products using gas chromatography – Flame ionization detector. J Environ Stud 12(1):15–25 Food Chem 156:296–300 Muckian L, Grant R, Clipson N, Doyle E (2009) Bacterial community Oris JT, Giesy JP (1985) The photoenhanced toxicity of anthracene to dynamics during bioremediation of phenanthrene and fluor- juvenile sunfish (Lepomis spp). Aquat Toxicol 6:133–146 anthene amended soil. Int Biodeterior Biodegradation 63:52–56 Pacwa-Plociniczak M, Plaza GA, Piotrowska-Seget Z, Cameotra SS Mueller JG, Cerniglia CE, Pritchard PH (1996) Bioremediation of (2011) Environmental applications of biosurfactants: Recent environments contaminated by polycyclic aromatic hydro- advances. Int J Mol Sci 12(1):633–654 carbons. Biotechnology Research Series 6:125–194 Pan E, Sun H, Xu Q,Zhang Q, Liu LF, Chen XD, Xu Y (2015) Mulder H, Breure AM, Van-Honschooten D, Grotenhuis JTC, Van- Polycyclic aromatic hydrocarbons concentrations in drinking Andel JG, Rulkens WH (1998a) Effect of biofilm formation by water in villages along the Huai River in China and their asso- Pseudomonas 8909N on the bioavailability of solid naphthalene. ciation with high cancer incidence in local population. BioMed Appl Microbol Biotechnol 50:277–283 Res Int Article ID 762832, doi:10.1155/2015/762832 Mulder H, Breure AM, Van Andel JG, Grotenhuis JTC, Rulkens WH Panalaks T (1976) Determination and identification of polycyclic (1998b) Influence of hydrodynamic conditions on naphthalene aromatic hydrocarbons in smoked and charcoal-broiled food dissolution and subsequent biodegradation. Biotechnol Bioeng products by high pressure liquid chromatography and gas chro- 57:145–154 matography. J Environ Sci Health B 11:299–315 Müller R, Antranikian G, Maloney S, Sharp R (1998) Thermophilic Pantsyrnayaa T, Blancharda F, Delaunaya S, Goergena JL, Guédona degradation of environmental pollutants. In: Antranikian G (ed) E, Gusevab E, Boudrant J (2011) Effect of surfactants, dispersion Biotechnology of Extremophiles, (Advances in Biochemical and temperature on solubility and biodegradation of phenanthrene Engineering/Biotechnology). Vol. 61, Springer, Berlin, Heidel- in aqueous media. Chemosphere 83(1):29–33 berg, New York, p 155–169 Patel MS, Tiwari KK (2015) Remediation of Acenaphthene and Mulligan CN, Gibbs BF (2004) Types, production and applications of Fluoranthene by Chlorella vulgaris Beijerinck: FTIR based biosurfactant Products. Proc Indian Natn Sci Acad B70(1):31–55 study. Int J Biosci Technol 8(2):5–9 Narro ML, Cemiglia CE, Van Baalen C, Gibson DT (1992a) Evidence Paul D, Pandey G, Pandey J, Jain RK (2005) Accessing microbial of NIH shift in naphthalene oxidation by the marine cyano- diversity for bioremediation and environmental restoration. bacterium, Osciiiatoria species strain JCM. Appl Environ Trends Biotechnol 23:135–142 Microbiol 58:1360–1363 Payne JF, Mathieu A, Collier TK (2003) Ecotoxicological studies Narro ML, Cemiglia CE, Van Baalen C, Gibson DT (1992b) Meta- focusing on marine and freshwater fish. In: Dauben PET (ed) bolism of phenanthrene by the marine cyanobacterium Agme- PAHs-an ecotoxicological perspective. Wiley: West Sussex, UK, nellum quadruplicatum, strain PR-6. Appl Environ Microbiol p 191–224 58:1351–1359 Pazos M, Rosales E, Alcántara T, Gómez J, Sanromán MA (2010) Nedwell DB (1999) Effect of low temperature on microbial growth: Decontamination of soils containing PAHs by electroremediation: lowered affinity for substrates limits growth at low temperature. a review. J Hazard Mater 177(1):1–11 FEMS Microbiol Ecol 30(2):101–111 Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao New Jersey Department of Health and Senior Services (1999) QH (2008) Microbial biodegradation of polyaromatic hydro- Hazardous Substance Fact Sheet. CAS number 86-73-7 carbons. FEMS Microbiol Rev 32:927–955 Environmental Management

Perelo LW (2010) Review: In situ and bioremediation of organic hydrocarbons and their hydroxylated metabolites in infant foods. pollutants in aquatic sediments. J Hazard Mater 177(1–3): Food Chem 115:814–819 81–89 Rhodes A, Carlin A, Semple T (2008) Impact of black carbon in the Perugini M, Visciano P, Giammarino A, Manera M, Di Nardo W, extraction and mineralisation of phenanthrene in soil. Environ Sci Amorena M (2007) Polycyclic aromatic hydrocarbons in marine Technol 42(3):740–745 organisms from the Adriatic Sea, Italy. Chemosphere Rice JW, Suuberg EM (2010) Thermodynamic study of (anthracene + 66:1904–1910 benzo[a]pyrene) solid mixtures. J Chem Thermodyn 42 Petersen DG, Reichenberg F, Dahllof I (2008) Phototoxicity of pyrene (11):1356–1360 affects benthic algae and bacteria from the Arctic. Environ Sci Riess R, Nemati M, Headley J, Hill G (2005) Improved mass transfer Technol 42:1371–1376 and biodegradation rates of naphthalene particles using a novel Petrun AC, Rubenchik BL (1966) On the possibility of appearance of bead mill bioreactor. J Chem Technol Biotechnol 80(6):662–668 the carcinogenous agent 3,4 benzpyrene in electrically smoked Robles-González IV, Fava F, Poggi-Varaldo HM (2008) A review on fish. Vrazhednoe Delo 2:93–95 slurry bioreactors for bioremediation of soils and sediments. Pittinger CA, Buikema AL, Falkinham JO (1987) In-situ variations in Microb Cell Fact 7:5–15 oyster mutagenicity and tissue concentrations of polycyclic aro- Roseiro LC, Gomes A, Santos C (2011) Influence of processing in the matic hydrocarbons. Environ Toxicol Chem 6:51–60 prevalence of polycyclic aromatic hydrocarbons in a Portuguese Pollard SJT, Hrudey SE, Fedorak PM (1994) Bioremediation of pet- traditional meat products. Food Chem Toxicol 49:1340–1345 roleum and creosote-contaminated soils: A review of constraints. Romero MC, Cazau MC, Giorgieri S, Arambari AM (1998) Phenan- Waste Manag Res 12:173–194 threne degradation by microorganisms isolated from a con- Pozdnyakova NN (2012) Involvement of the ligninolytic system of taminated stream. Environ Pollut 101:335–359 white-rot and litter-decomposing fungi in the degradation of Ruby MV, Lowney YW, Bunge AL, Roberts SM, Gomez-Eyles JL, polycyclic aromatic hydrocarbons. Biotechnol Res Int 243217. Ghosh U, Kissel JC, Tomlinson P, Menzie C (2016) Oral Bioa- doi:10.1155/2012/243217 vailability, Bioaccessibility, and Dermal Absorption of PAHs Prabhu Y, Phale PS (2003) Biodegradation of Phenanthrene by from Soil—State of the Science. Environ Sci Technol 50 Pseudomonas sp. Strain PP2: novel metabolic pathway role of (5):2151–2164 biosurfactant and cell surface hydrophobicity in Hydrocarbon Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydro- assimilation. Appl Microbiol Biotechnol 61:342–351 carbons: environmental pollution and bioremediation. Trends Pradhan SP, Conrad JR, Paterek JR, Srivastava VJ (1998) Potential of Biotechnol 20(6):243–248 phytoremediation for treatment of PAHs in soil at MGP sites. J Sanagi MM, Loh SH, Wan-Ibrahim WA, Hasan MH, Aboul-Enein HY Soil Contam 7:467–480 (2013) Determination of polycyclic aromatic hydrocarbons in Prince RC (2010) Bioremediation of marine oil spills. Handbook fresh milk by hollow fiber liquid-phase microextraction-gas Hydrocarbon Lipid Microbiol 6:2617–2630 chromatography mass spectrometry. J Chromatogr Sci Purwaningsih IS, Hill GA, Headley JV (2002) Air stripping and 51:112–116 dissolution rates of aromatic hydrocarbon particles in a bior- Schneegurt MA, Kulpa CF (1998) The application of molecular eactor. Chem Eng Commun 189(2):268–283 techniques in environmental biotechnology for monitoring Quinn L, Pieters R, Nieuwoudt C, Borgen A, Kylin H, Bouwman H microbial systems. Biotechnol Appl Biochem 27(2):73–79 (2009) Distribution profiles of selected organic pollutants in soils Scientific Committee on Food, European Commission (2002) Opinion and sediments of industrial, residential and agricultural areas of of the Scientific Committee on Food on the risks to human health South Africa. J Environ Monit 9(11):1647–1657 of polycyclic aromatic hydrocarbons in food. http://ec.europa.eu/ Rahman KSM, Rahman TJ, Lakshmanaperumalsamy P, Marchant R, food/fs/sc/scf/out153_en.pdf. Accessed 15 May 2013 Banat IM (2003) The potential of bacterial isolates for Semple KT, Cain RB, Schimdt S (1999) Biodegradation of aromatic emulsification with range of hydrocarbons. Acta Biotechnol compounds by microalgae. FEMS Microbiol Lett 170:291–300 4:335–345 Seo J, Young SK, Qing XL (2009) Bacterial degradation of aromatic Ramesh A, Walker SA, Hood DB, Guillien MD, Schneider K, Wey- compounds. Int J Environ Res Public Health 6(1):278–309 hand EH (2004) Bioavailability and risk assessment of orally Sharma S (2012) Bioremediation: Features, Strategies and applica- ingested polycyclic aromatic hydrocarbons. Int J Toxicol 23 tions. Asian J Pharm Life Sci 2(2):202–213 (5):301–333 Shi W, Krella A, Orth A, Yu Y, Fundele R (2005) Widespread dis- Reddy MS, Naresh B, Leela T, Prashanthi M, Madhusudhan NC, ruption of genomic imprinting in adult interspecies mouse (Mus) Dhanasri G, Devi P (2010) Biodegradation of phenanthrene with hybrids. Genesis 43(3):100–8 biosurfactant production by a new strain of Brevibacillus species. Shiraishi N, Pilkington NH, Otsuki A, Fuwa K (1985) Occurrence of Bioresour Technol 101:7980–7983 chlorinated polynuclear aromatic hydrocarbons in tap water. Rehmann K, Noll HP, Steiberg CEW (1998) Pyrene degradation by Environ Sci Technol 19:585–590 Mycobacterium sp. Strain KR2. Chemosphere 6(14):2977–2992 Silva IS, Grossman M, Durranta LR (2009) Degradation of polycyclic Ren G, Ren W, Teng Y, Li Z (2015) Evident bacterial community aromatic hydrocarbons (2-7 rings) under microaerobic and very- changes but only slight degradation when polluted with pyrene in low-oxygen conditions by soil fungi. Int Biodeter Biodegr 63 a red soil. Front Microbiol 6:22–33 (2):224–229 Rengarajana T, Rajendran P, Nandakumar N, Lokeshkumar B, Silva BO, Adetunde OT, Oluseyi TO, Olayinka KO, Alo BI (2011) Rajendran P, Nishigaki I (2015) Exposure to polycyclic aromatic Effects of the methods of smoking on the levels of polycyclic hydrocarbons with special focus on cancer. Asian Pac J Trop aromatic hydrocarbons (PAHs) in some locally consumed fishes Biomed 5(3):182–189 in Nigeria. African. J Food Sci 5(7):384–391 Rey-Salgueiro L, García-Falcón MS, Martínez-Carballo E, Simal- Simon R, Gomez-Ruiz JA, Wenzi T (2010) Results of an European Gándara J (2008) Effects of toasting procedures on the levels of inter-laboratory comparison study on the determination of the 15 polycyclic aromatic hydrocarbons in toasted bread. Food Chem +1 EU priority polycyclic aromatic hydrocarbons (PAHs) in 108(2):607–615 liquid smoke condesates. Food Chem 123:819–826 Rey-Salgueiro L, Martínez-Carballo E, García-Falcón MS, Simal- Singh R, Paul D, Jain RK (2006) Biofilms: implications in bior- Gándara J (2009) Occurrence of polycyclic aromatic emediation. Trends Microbiol 14(9):389–397 Environmental Management

Siron R, Pelletier E, Brochu H (1995) Environmental factors influ- Allegaert W, Bekaert K (2015) Environmental contaminants of encing the biodegradation of petroleum hydrocarbons in cold emerging concern in seafood–European database on contaminant seawater. Arch Environ Contam Toxicol 28:406–416 levels. Environ Res 143:29–45 Skupinska K, Mislewicz I, Kasprzycka-Guttman T (2004) Polycyclic Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation aromatic hydrocarbons: environmental appearance and impact on and biomarkers in environmental risk assessment: a review. living organisms. Acta Pol Pharm 61(3):233–240 Environ Toxicol Pharmacol 13(2):57–149 Sojinu OS, Sonibare OO, Zeng EY (2011) Concentrations of poly- Varanasi U, Reichert WL, Stein JE (1989) 32P-Postlabeling analysis of cyclic aromatic hydrocarbons in soils of a mangrove forest DNA adducts in liver of wild English sole (Parophrys vetulus) affected by a forest fire. Toxicol Environ Chem 93(3):450–461 and winter flounder (Pseudopleuronectes americanus). Cancer Sowa D (2011) Sphingomonas spp: Agents of Bioremediation and Res 49:11–71 Pathogenesis. From Microbe wiki, the student-edited micro- Vega S, Gutierrez R, Ortiz R, Schettino B, Ramirez M, Perez J biology resource. https://microbewiki.kenyon.edu. Accessed 27 (2011) Hydrocarbons derived from petroleum in bottled drinking July 2014 water from Mexico city. Bull Environ Contam Toxicol Sram RJ, Binková B, Rössner P, Rubeš J, Topinka J, Dejmeka J 86:632–636 (1999) Adverse reproductive outcomes from exposure to envir- Venosa AD, Zhu X (2003) Biodegradation of crude oil contaminating onmental mutagens. Mutat Res 428:203–215 marine shorelines and freshwater wetlands. Spill Sci Technol Bull Srogi K (2007) Monitoring of environmental exposure to polycyclic 8(2):163–178 aromatic hydrocarbons: a review. Environ Chem Lett 5 Vidali M (2001) Bioremediation: An overview. Pure Appl Chem 73 (4):169–195 (7):1163–1172 Storelli MM, Stuffler RG, Marcotrigiano GO (2003) Polycyclic aro- Viegas O, Novo P, Pinto E, Pinho O, Ferreira IMPLVO (2012) Effect matic hydrocarbons, polychlorinated biphenyls, chlorinated pes- of charcoal types and grilling conditions on formation of het- ticides (DDTs), hexachlorocyclohexane, and hexachlorobenzene erocyclic aromatic amines (HAs) and polycyclic aromatic residues in smoked seafood. J Food Prot 66(6):1095–1099 hydrocarbons (PAHs) in grilled muscle foods. Food Chem Tox- Stumpe-Vīksna I, Bartkevičs V, Kukāre A, Morozovsa A (2008) icol 50(6):2128–2134 Polycyclic aromatic hydrocarbons in meat smoked with different Viñas M, Sabate J, Espuny M, Solanas A (2005) Bacterial community types of wood. Food Chem 110(3):794–797 dynamics and polycyclic aromatic hydrocarbon degradation Sudip KS, Om VS, Rakesh KJ (2002) Polycyclic aromatic hydro- during bioremediation of heavily creosote contaminated soil. carbons: environmental pollution and bioremediation. Trends Appl Environ Microbiol 71(11):7008–7018 Biotechnol 20:243–248 Volkering F, Breure AM, Van Andel JG (1993) Effect of micro- Sun RX, Lin Q, Ke CL, Du FY, Gu YG, Cao K, Xiao JL, Mai BX organisms on the bioavailability and biodegradation of crystalline (2016) Polycyclic aromatic hydrocarbons in surface sediments naphthalene. Appl Microbiol Biotechnol 40:535–540 and marine organisms from the Daya Bay, South China. Mar Poll Wan Y, Jin X, Hu J, Jin F (2007) Trophic dilution of polycyclic Bull 103(1):325–332 aromatic hydrocarbons (PAHs) in a marine food web from Bohai Swaranjit SC, Randhir SM (2010) Biosurfactant-enhanced bior- Bay, North China. Environ Sci Technol 41(9):3109–3114 emediation of hydrophobic pollutants. Pure Appl Chem 82 Wang X, Brusseau ML (1993) Solubilisation of some low polarity (1):97–116 organic compounds by hydroxypropyl-β-cyclodextrin. Environ Takeuchi I, Miyoshi N, Mizukawa K, Takada H, Ikemoto T, Omori K, Sci Technol 27:2821–2825 Tsuchiya K (2009) Biomagnification profiles of polycyclic Wang G, Zhang Q, Ma P, Rowden J (2008) Sources and distribution of aromatic hydrocarbons, alkylphenols and polychlorinated polycyclic aromatic hydrocarbons in urban soils. Case studies of biphenyls in Tokyo Bay elucidated by δ 13 C and δ 15 N isotope Detroit and New Orleans. Soil Sediment Contam 17(6): ratios as guides to trophic web structure. Mar Poll Bull 58 547–563 (5):663–671 Ward DM, Brock TD (1978) Hydrocarbon biodegradation in hyper- Tam NFY, Chan MN, Wong YS (2010) Removal and biodegradation saline environments. Appl Environ Microbiol 35:353–359 of polycyclic aromatic hydrocarbons by immobilized microalgal Warshawsky D, Radike M, Jayasimhulu K, Cody T (1988) Metabo- beads. Trans Ecol Environ, Waste Manag Environ 140:391–402. lism of benzo(a)pyrene by a dioxygenase enzyme system of the doi:10.2495/WM100351 freshwater alga Selenastrum capricornutum. Biochem Biophys Tang Y, Qi JL, Krieger-Brockett B (2005) Evaluating factors that Res Commun 152:540–544 influence microbial phenanthrene biodegradation rates by Warshawsky D, Cody T, Radike M, Reilman R, Schumann B, LaDow regression with categorical variables. Chemosphere 59:729–741 K, Schneider J (1995) Biotransformation of benzo(a)pyrene and Tekere M, Read J, Mattiasson B (2005) Polycyclic aromatic hydro- other polycyclic aromatic hydrocarbons and heterocyclic analogs carbon biodegradation in extracellular fluids and static batch by several green algae and other algal species under gold and cultures of selected sub-tropical white rot fungi. J Biotechnol white light. Chem Biol Interact 97:131–148 115:367–77 Warshawsky D, LaDow K, Schneider J (2007) Enhanced degradation Thomson B, Lake R, Lill R (1996) The contribution of margarine to of benzo[a]pyrene by Mycobacterium sp. in conjunction with cancer risk from polycyclic aromatic hydrocarbons in the New green alga. Chemosphere 69(3):500–506 Zealand diet. Polycycl Aromat Compd 11:177–184 Web (2011) About coal tar and polycyclic aromatic hydrocarbons Ukiwe LN, Egereonu UU, Njoku PC, Nwoko CIA, Jude I, Allinor JI (PAHs). The truth about refined coal tar based pavement sealers (2013) Polycyclic aromatic hydrocarbons degradation techniques: and PAHs. http://www.truthaboutcoaltar.com/aboutcoaltar.html. A review. Int J Chem 5(4):43–55 Accessed 15 Oct 2014 Valentı´n L, Nousiainen A, Mikkonen A (2013) Introduction to Weeks BA, Warimer JE (1984) Effects of toxic chemicals on mac- organic contaminants in soil: concepts and risks. In: Vincent T, rophage phagocytosis in two estuarine fishes. Mar Environ Res Caminal G, Eljarrat E, Barceló D (eds) Emerging organic con- 14:327–335 taminants in sludges: analysis, fate and biological treatment. Weis LM, Rummel AM, Masten SJ, Trosko JE, Upham BL (1998) Springer-Verlag Berlin, Heidelberg 24: 1–30 Bay or bay like regions of polycyclic aromatic hydrocarbons were Vandermeersch G, Lourenço HM, Alvarez-Muñoz D, Cunha S, Dio- potent inhibitors of gap junctional intercellular communication. gène J, Cano-Sancho G, Sloth JJ, Kwadijk C, Barcelo D, Environ Health Perspect 106(1):17–22 Environmental Management

White PA, Robitaille S, Rasmussen JB (1999) Heritable reproductive Yang C, Zhang G, Wang Z, Yang Z, Hollebone B, Landriault M, Shah effects of benzo(a)pyrene on the fathead minnow (Pimephales K, Brown CE (2014) Development of a methodology for accurate promelas). Environ Toxicol Chem 18:1843–1847 quantitation of alkylated polycyclic aromatic hydrocarbons in Wick AF, Haus NW, Sukkariyah BF, Haering KC, Daniels WL (2011) petroleum and oil contaminated environmental samples. Anal Remediation of PAH-contaminated soils and sediments: A lit- Methods 6(19):7760–7771 erature review. CSES Department, Internal Research Document. Yalkowsky SH, Dannenfelser RM (1992) The aquasol database of aqu- p1–102 eous solubility, 5th edn. Univ Az, College of Pharmacy, Tucson, AZ Wilcke W (2000) Polycyclic aromatic hydrocarbons (PAHs) in soil. J Yanyangwu D (2012) Anaerobic biodegradation of PAHs in river Plant Nutr Soil Sci 163:229–248 sediments under denitrifying conditions-Another choice? Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the Yanyangwu.wordpress.com. Accessed 4 Oct 2013 United Kingdom environment: a preliminary source inventory Zanieri L, Galvan P, Checchini L, Cincinelli A, Lepri L, Donzelli GP, and budget. Environ Pollut 88(1):91–108 Del Bubba M (2007) Polycyclic aromatic hydrocarbons (PAHs) Wilson SC, Jones KC (1993) Bioremediation of soil contaminated in human milk from Italian women: Influence of cigarette smoke with polynuclear aromatic hydrocarbons (PAHs): A review. and residential area. Chemosphere 67:1265–1274 Environ Pollut 81(3):229–249 Zhang Y, Tao S (2009) Global atmospheric emission inventory of World Health Organisation (WHO) (2003). Polynuclear aromatic polycyclic aromatic hydrocarbons (PAHs) for 2004. Atmos hydrocarbons in Drinking-water Background document for Environ 43:812–819 development of WHO Guidelines for Drinking-water Quality. p 4 Zhang J, Zhang X, Liu J, Li R, Shen B (2012) Isolation of a ther- Wu M, Chen L, Tian Y, Dinga Y, Dick WA (2013) Degradation of mophilic bacterium, Geobacillus sp. SH-1, capable of degrading polycyclic aromatic hydrocarbons by microbial consortia enri- aliphatic hydrocarbons and naphthalene simultaneously, and ched from three soils using two different culture media. Environ identification of its naphthalene degrading pathway. Bioresour Pollut 178:152–158 Technol 124:83–89 Yakan SD, Focks A, Klasmeier J, Okay OS (2017) Numerical eva- Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an luation of bioaccumulation and depuration kinetics of PAHs in appealing tool for assessment of metal pollution in the aquatic Mytilus galloprovincialis. Environ Pollut 220:1244–1250 ecosystem. Anal Chim Acta 606:135e150