Bioresource Technology 128 (2013) 745–750

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Bioresource Technology

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Review The contamination and control of biological pollutants in mass cultivation of microalgae ⇑ ⇑ Hui Wang, Wei Zhang , Lin Chen, Junfeng Wang, Tianzhong Liu

CAS Key Laboratory of , Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, PR China highlights

" Biological contamination in mass cultivation of microalgae is inevitable. " Transmission routes of biological pollutants are analyzed. " Different biological pollutants species have different contamination mechanisms. " Recent attempts to overcome the contamination are under active study. article info abstract

Article history: The potential of microalgae as a biomass feedstock for biofuels, bioproducts and as a technological solu- Received 28 August 2012 tion for CO2 fixation is subject to intense academic and industrial researches. However, current microal- Received in revised form 30 October 2012 gal mass culture technologies have failed to produce bulk volume of microalgal biomass at low cost, Accepted 30 October 2012 because the contaminations of biological pollutants become a big constraint in mass cultivation and Available online 7 November 2012 impede the industrial process. Here the transmission routes, contamination mechanisms of biological pollutants both in open ponds and are described and recent attempts to overcome Keywords: the barrier are reviewed. What worth noting, unlike conventional microbial fermentation which uses a Microalgal biomass pure monoculture, the cultivation of microalgae is a complicated symbiotic system of microalgae– Open ponds bacterial– where the target microalgae dominate, cross infection or contamination by Contamination biological pollutants is inevitable and it will require much further research. Further investigation and development of control methods are necessary, particularly microalgal strain selection. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction are mainly based on suspension culture. And raceway ponds (Chisti, 2007) and photobioreactors (Mata et al., 2010) are the most Microalgae are unicellular photosynthetic organisms with rela- common style of cultivations in large scales. However, sustained tively simple requirements for growth, are sunlight-driven facto- open pond production has been successful only for a limited num- ries which can convert water and carbon dioxide (CO2) into ber of cultures like Spirulina and Dunaliella with extreme condi- potential nutrients such as proteins, amino acids, lipids, polysac- tions such as very high salinity or high pH (Asha et al., 2011). charides, and other biologically-active molecules Sufficient supply of nutrients, efficient gas transfer and ex- (Asha et al., 2011; Mulbry et al., 2008). Microalgae can be promis- change, and delivery of photosynthetically-active radiation (PAR) ing biomass feedstock owing to their fast growth, high reproduc- (Logan and Roanld, 2011) are all major challenges during produc- tion and low emission. Priorly, microalgae have tions of microalgae, which have been the subject in academic potentially many broad applications in biotechnology (Walter and industrial studies. Besides these, it was also found by U.S.DOE et al., 2005), including (Chisti, 2007), pharmaceuticals in 2010, microalgal monocultures grown for biofuel and other bio- (Lorenz and Cysewski, 2003), (Mulbry et al., 2005). products were susceptible to biological pollutants. Infection or Bulk volume of microalgal biomass at low cost through large- Contamination by biological pollutants could cause sudden and scale cultivations should be satisfied to realize these industrial massive death of microalgal cells, but little attention was paid to potentials of microalgae. Presently, most methods of producing this. microalgal biomass for productions of biofuels and bioproducts This review gives an introduction of the transmission routes and contamination mechanisms of biological pollutants, follow which, possible typical measures for controlling biological pollu- ⇑ Corresponding authors. Tel.: +86 535 8066 2737; fax: +86 535 8066 2735. E-mail addresses: [email protected] (W. Zhang), [email protected] (T. Liu). tants are summarized and suggested.

0960-8524/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biortech.2012.10.158 746 H. Wang et al. / Bioresource Technology 128 (2013) 745–750

2. The transmission routes of biological pollutants 3.1. Zooplankton

Though the structures are different, whatever raceway ponds or Large scale cultivation is susceptible to grazing by zooplankton closed photobioreactor are relative open systems, besides the input (e.g., rotifers and cladocerans) which can reduce algal concentra- of water, gas transfer and exchange are also needed between the tion and production to low levels within just a few days culture system and external environment. (Benemann, 2008a). Zooplankton includes (<2 mm), There is a variation in the biomass productivity of microalgae, nanoplankton (2–20 mm), microplankton (20–200 mm), mesoplank- ranging from 0.01 g/L/d to 0.37 g/L/d depending on the type of mic- ton (0.2–20 mm), macroplankton (20–200 mm) and megaplankton roalgae species (Chen et al., 2011) under mass phototrophic culti- (>200 mm). Among these zooplankton, (Rosetta and vation, which proves the production of microalgae is likely McManus, 2003), rotifer (Lurling and Beekman, 2006), cladocera dependent upon large volumes of water. It is unrealistic to adopt and (Frederiksen et al., 2006) are the common predatory heat sterilization used in conventional microbial fermentation to species in the mass cultivation of microalgae. Li et al. (2006) incu- treat so large volumes of water. Although, water can be processed bated ciliate simultaneously with sufficient Dunaliella salina as with bleaching powder or filtration before mass cultivations of food and found that the cell densities of microalgae decreased from microalgae, it is possible that large amounts of pollutants remain 2.7 Â 104 cells/mL to 1.2 Â 104 cells/mL after 2 days incubations. due to insufficient disposals, which could be caused by low chlo- This has also been reported by Moreno-Garrido and Canavate rine content or short processing time. (2001), who observed that grazing can clarify dense out- In open ponds, the large interface between the air and liquid door mass cultures of Dunaliella salina within 2 days. culture is helpful for CO2 input and releasing of excess-dissolved Many research results showed that zooplankton had two types , but this would of course increase the chances of contam- of feeding mechanism: mechanical (negative) mechanism and ination from the air (Logan and Roanld, 2011). Despite the closed behavior (positive) mechanism (Vanderploeg and Paffenhofer, photobioreactors can reduce the exposure of the culture to the 1985) and they, particularly , could alternate between external environment and then give better protection against the two mechanisms due to different food supply. The copepods pollutants by closed type design, aeration has to be done contin- selected the negative feeding mechanism at a low concentration uously via bubbling from the bottom of photobioreactor with of food, whereas the positive feeding mechanism was adopted as

1–5% CO2 at a rate of 0.1–0.5 vvm (volume gas per volume broth the density of food exceeded a critical value (Kleppel et al., per minute) (Choi et al., 2012; Manoranjan et al., 2011). Hence, 1996). Grazing activities of zooplankton are also impacted by other for photobioreactors large volumes of air must be provided for factors, such as temperature (Huntley and Lopez, 1992) and illumi- dilution of CO2, which are helpful with mixing of the culture, nation. Wang and Conover (1986) reported that the feeding inten- efficient CO2 fixation and releasing of dissolved oxygen. Filtration sity of copepods at night was higher than that in day-time. with microporous membrane is generally adopted for air sterilization, whereas the shortcoming is that the in the 3.2. air couldn’t be eliminated. In addition, it’s very impractical to apply it to gas with low pressure (0.02–0.05 MPa), bulk volumes Some species of bacteria, called -lytic bacteria, and high velocity during the mass cultivation of microalgae. have potential of inhibiting the growth of microalgae. They were Complete sterility is very difficult even in closed photobioreac- initially found due to their involvement with termination and tors, because it’s totally different with anaerobic fermentation, decomposition of water blooms and red tides (Imai et al., 2001; during which sterile air is provided just for positive pressure Mu et al., 2007; Wang et al., 2010a,b). Subsequently it was proved environment. that some of them indeed had negative influences on microalgal In fact, whether open ponds or photobioreactors, biological pol- growth and could destruct mass cultivation of microalgae (Zhou lutants will inevitably go into the culture by water or gas, unless et al., 2011). In the present study, the bacterial strains mainly large volumes of them can be avoided during mass-cultivations including Alteromonas sp. (Imai et al., 1995), sp. of microalgae. (Fukami et al., 1992), Cytophaga sp., Myxobacter sp. (Junichi et al., 1998), Bacillus sp., and Pseudomonas sp. (Kim et al., 2007) were re- ported. Their lytic modes and activities of common phytoplankton- 3. The species of biological pollutants and their contamination lytic bacterial strains were listed in Table 2. mechanisms The phytoplankton-lytic bacteria can impact microalgae effec- tively through either direct attack depending on cell-to-cell contact This section outlines the species and their contamination mech- (Imai et al., 1995; Shi et al., 2006) or indirect attack mediated by anisms of biological pollutants (zooplankton, bacteria, other extracellular compounds (Imai et al., 1995; Kang et al., 2005). Xan- and virus) (Table 1) which can significantly constrain the growth thus sp. is the earliest and most widely reported one of the direct of microalgae. In addition, a better understanding of the contami- phytoplankton-lytic bacteria (Shilo, 1970). Bacteria Saprospira sp. nation mechanisms will be required. (SS98-5) and Pseudoalteromonas sp. (J18/M01) could respectively lyse the cells of Dinoflagellate and after their distinctive contacts (Anne et al., 2004). Compared with the direct attack, most

Table 1 phytoplankton-lytic bacteria prefer indirect attacks. An associated The contamination modes of biological pollutants. heterotrophic dominant single bacterium (ZQS01) was once se- lected for its inhibitive effect on through excret- Species Contamination Mode Reference ing chemic substance (Zhou et al., 2011). As well as Wang et al. Zooplankton Grazing Huo et al. (2010a,b), two strains of phytoplankton-lytic bacteria (DHQ25 (2008) and DHY3) had abilities of secreting algicidal proteins against axe- Bacteria Cell Secrete extracellular Shi et al. contact compounds (2006) nic Alexandrium tamarense. Harmful Cell Resource Competition Allelpathy Twiner et al. Recent studies have demonstrated that phytoplankton-lytic Algae contact (2005) bacteria could destroyed the double helix structure of DNA in mic- Virus Infection Wu et al. roalgae and caused the death of microalgae (Sakai et al., 2007). In (2011) addition, the maximal photochemical photochemical efficiency (Fv/ H. Wang et al. / Bioresource Technology 128 (2013) 745–750 747

Table 2 The lytic mode and lytic activity of some bacterial stains.

Bacterial Strains Algal strains Lytic mode Lytic activity Reference Alteromonas sp. Alexandrium tamarense Indirect attack 89.9% (5d) Su et al. (2011) Bacillus cereus Microcystis Indirect attack Nakamura et al. (2003) Bacillus fusiformis Chlorella Secreting metabolites 45.6% (1d) Mu et al. (2007) Micrococcus luteus Cochlodinium polykrikoides Over 90% Kim et al. (2008) Pseudoalteromona sp. Skeletonema costatum Secreting protein Lee et al. (2002) Pseudoalteromonas sp. Alexandrium tamarense Secreting Protein 58.3% Wang et al. (2012a,b) Pseudomonas aeruginosa Scrippsiella trochoidea 69.5% (5d) Pseudomonas putida Microcystis aeruginosa 89.3% (7d) Zhang et al. (2011) Pseudomonas putida Stephanodiscus hantzschii 80.4% (2d) Kang et al. (2005) Pseudomonas fluorescens Heterosigma akashiwo Secreting protein 88.9% Kim et al. (2007) Pseudomonas sp. ceratosporum Secreting 2,3-indolinedione Sakata et al. (2011) Saprospira sp. Chaetoceros ceratosporum Direct attack Furusawa et al. (2003) Sphingomonas sp. Microcystis viridis Secreting argimicin A Imamura et al. (2001) Vibrio sp. Alexandrium tamarense Indirect attack 71.1% (5d) Su et al. (2011) Vibrio sp. Oscillatoria amphibian Secreting b-Cyanoalanine Yoshikawa et al. (2000)

Fm) and the actual photochemical efficiency of PSII in microalgae rate of ammonium cause the difference during the simultaneous reduced sharply, what means the of certain micro- culture of Microcystis mpvacelii and Scenedesmus uadricauda. algae strains was restrained because of the phytoplankton-lytic bacteria (Banin et al., 2000). Furthermore, Nakashima et al. (2006) considered the phytoplankton-lytic bacteria inhibited the 3.3.3. Allelopathy growth of microalgae depending on breaking the integrity of Allelopathy is a biological phenomenon by which an organism microalgal cell wall and made the intracellular material leakage produces one or more biochemicals that can influence the growth, (Nakashima et al., 2006). survival and reproduction of other organisms (Suikkanen et al., 2004). These biochemicals are known as allelochemicals, which have beneficial (positive allelopathy) or detrimental (negative alle- 3.3. Other microalgae lopathy) effects on the target organisms. Most studies have been focused on negative allelopthy. Pridinium aciculiferum could inter- The cross contaminations by other microalgae are inevitable fere with the growth of Rhodomonas lacustris through secreting a and have been reported broadly (Piazzi and Ceccherelli, 2002). If certain substance (Rengefors and Legrand, 2001); Fischerella musci- the initial culture is not very pure and other microalgae are capable cola produced fischerellin A(C H N O ) to inhibit the growth of of growing more rapidly than the ‘‘production’’ strain (Vasudevan 23 36 2 2 some strains of microalgae (Papke et al., 1997); Peridinium gatun- and Briggs, 2008), the likelihood of over-growth by other microal- ense and Microcystis sp. inhibited each other through allelopathy gae is high in practice. Direct cell contact (Twirler et al., 2001), re- (Vardi et al., 2002). source competition and allelopathy (Twiner et al., 2005) are the three main contamination mechanisms between different microalgae. 3.4. Virus

3.3.1. Direct contact are ubiquitous in aquatic environment and their associ- As the density of microalgae cells reaches a certain concentra- ations with both eukaryotic algae and cyanobacteia are well tion after prolonged culturing, it is bound to cause the space com- known. Viral infection can also significantly reduce the pond algal petition and these contacts will result mutual collision between population within a few days and trigger changes in algal cell them, the dominant microalgae species would be substituted dur- structure, diversity and succession (Kagami et al., 2007). The short ing this process. Yasuhiro et al. (2007) concluded that cell-to-cell replication cycle and high specificity of infection on the host means contact should lead to the conformation change and inhibited that, the microalgal virus can rapidly reduce the amount of algae in growth of Akashiwo sanguinea cells when they were mix cultivated culture. Viruses can infect both prokaryotic (cyano- with Cochlodinium polykrikoides cells. Uchida et al. (1999) esti- phage) and eukaryotic algae. mated the cells of Gymnodinium mikimotoi could be killed after Safferman and Morris (1963) firstly reported a virus infecting 19 times of contacts with Heterocapas circularisquama cells. the cyanobacterium, the LPP virus, which could infect multiple hosts such as Lynbya sp., Phormidium sp. and Plectonema sp. Gibbs 3.3.2. Resource competition et al. (1976) identified the first eukaryotic algal virus named CCV, Competition occurs between different microalgae species when which specifically infected the Chara coralline. Nagasaki et al. the capability of the environment to supply resources (CO2 and (1999) designed a one-step growth experiment to estimate the nutrient) is smaller than the potential biological requirement. algicidal activity of HaVo1, the results was that almost all of the

The same CO2 supply may cause different biomass of different mic- cells lost motility within 24 h and the host cell density had de- 1 5 roalgae, because microalgae have different CO2 absorption abilities creased to less than 10 cells/ml from 1.27 Â 10 cells/ml, while depending on the activities of carbonic anhydrase and rubisco en- the density of virus HaVo1 increased to 9.8 Â 107 LCU/ml from zyme. Microalgae compete for nutrients such as phosphorus, nitro- 2.58 Â 105 LCU/ml. gen, potassium, calcium and magnesium. Microalgae species which In general, many biological pollutants were found to be able to have the larger absorbing capacities of nutrient, or make better use influence the microalgal cultivation. as the predator of the available resources will hold dominant positions in compe- of microalgae were thought to be the main cause leading to culti- titions. Litchman (2003) studied the competition between two cya- vation failure. While there is still a question what a concentration nobacteria and found different effects under different light of pollutions in the culture could lead to the outbreak of microalgal conditions. Kuwata and Miyazaki (2000) reported that the supply death. 748 H. Wang et al. / Bioresource Technology 128 (2013) 745–750

Table 3

Median lethal concentration (LC50, 24 h) of several pesticides to common harmful zooplankton in microalgae cultivation. Adapted from Snell and Hoff (1987), Wang and Yi (1997).

Variety Trichlorphon (mg/L) Buprofezin (mg/L) Decamethrin (mg/L) Tralocythrin (mg/L) Brachionus calyciflorus 318.5 263.5 4.2 0.4 Brachionus urceolaris 315.9 241.6 – 0.3 Brachionus plicatilis 274.9 – – – Daphnia pulex 3.6 Â 10À3 27.3 Â 10À3 – 59.8 Â 10À3 Daphnia carinata – – – 0.2 Â 10À3

4. The control measures of biological pollutants Additionally, adjusting the pH of microalgal liquid is the common method for killing or remaining the biological contaminants. Liu To overcome the challenges of biological pollutants, academic and Lu (1990) killed flagellate by reducing pH of microalgae cul- and industrial researchers have been searching for feasible ap- ture to 3.0, and Becher (1994) recommends employing a pH shift proaches to control them. Some researchers are attempted to filter to pH3.0 for 1–2 h to control rotifers. In Dunaliella ponds when the algae liquid or add drugs to annihilate the biological contami- the salinity drops above 20% (w/v) NaCl, and ciliates could nations, while others focused on changing the environmental con- not easily decimate the algal culture (Post et al., 1983). ditions to control them (John et al., 2012). Despite the use of selective culture environments employed for Spirulina sp. production, the alkaliphilic green alga Oocystis may 4.1. Filtration cause significant problems (Belay et al., 1997) and the contamina- tion of Dunaliella salina ponds by non- producing Dunal- Due to relatively small size of microalgal cells, filtration can be iella species has also been reported (Mitchell and Richmond, 1987). considered as an effective method to remove biological organisms Another point is that the application of this method needs the com- with large volumes, such as rotifers and copepods. There have been prehensive understanding of the adaptive range to ecological fac- reports on controlling by netting within the culture and during tors of both target algae and biological pollutants. harvesting (Borowitzka, 2005). However, despite rotifer adults As mentioned above, infection and contamination by biological can be removed using mesh silk screens because of their large pollutants could be managed by several approaches such as: filtra- sizes, the rotifer eggs and developing young individuals could not tion, chemical and biological drugs additives and growth condi- be completely removed. In order to clear the large biological con- tions changes. A greater understanding of how these biological taminations thoroughly, microalgae liquid should be continuously pollutants interact with host microalgae (Park et al., 2011) and rea- filtered over 3–4 days. sonable cultivation technology may lead to the development of effective control methods. However, it is a pity that these approaches also have deficiencies. It is most likely that strain 4.2. Chemicals additives selection will be the most practicable approach, with non- susceptibility/resistance to biological pollutants being an impor- There are a few publications suggesting how to use chemicals to tant factor in production strain selection. inhibit or kill biological pollutants (Gaiakowski et al., 1999). Among these chemicals, pesticides were firstly used to annihilate the zooplankton in the microalgae suspensions. Here outlines the 5. Conclusions toxicity analysis of several pesticides on common zooplankton (Table 3). Since biological pollutions during microalgae cultivations can- Moreno-Garrido and Canavate (2001) reported that quinine not be avoided, is there ways to control the pollutions in a certain (10 mg) could effectively kill ciliates and have a relative less dam- limits that target microalgal species can be continuously repro- age on the algae cells of Dunaliella salina (1 L). Besides formalde- duced and take the majorities in the symbiotic system? Stress hyde, ammonia and hydrogen peroxide are common substances resistance of species and its enhancement, specific inhibitor and used for disinfection in aquaculture (Rach et al., 1997; Schreier environmental conditions of biological contaminations, reasonable et al., 1996). cultivation technology and monitoring of pollution degree would Although, adding chemicals is one of the options for controlling probably promote industrialization of microalgae cultivation in biological pollutants, it may also damage the growth of target mic- the future. But prior to that, many relevant mechanism problems roalgae, the screening of biological drugs which inhibit biological especially focused on economic microalgae species must be pollutants without damaging the target microalgae is the preferred resolved by further researches. route. Li et al. (2006) studies an alcohol extract of Artemisia annua L. to inhibit the growth of ciliate. A further issue is that the separa- Acknowledgements tion and test of biological drugs still require further investigation.

This work was supported by the Key Technologies R&D Program 4.3. Changes of the environmental conditions from Ministry of Science and Technology of China (2011BAD14B01), Solar Energy Initiative Plan (Y21201110E), and Light and temperature are not only the important parameters of International Innovation Partnership Program from Chinese Acad- microalgal photosynthesis and growth, they also have certain roles emy of Sciences. on the breed of biological pollutants (Huntley and Lopez, 1992). For example, it has been reported that the feeding intensity of cope- pods increased in the night was proved by different analytic meth- References ods (Morales et al., 1993). Adjusting these parameters to an Anne, M.P., Flavia, E., Doralyn, D.S., Sacha, S., Suhelen, E., Sally, J., Jeremy, S., Staffan, optimum range at which the native microalgae could have the K., 2004. Biofilm development and cell death in the marine bacterium favorable growth status while the biological pollutants could not. Pseudoalteromonas tunicate. Appl. Environ. Microbiol. 7 (70), 3232–3238. H. Wang et al. / Bioresource Technology 128 (2013) 745–750 749

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