Journal of Advances in Microbiology
5(2): 1-21, 2017; Article no.JAMB.35591 ISSN: 2456-7116
Archaea Domain as Biocatalyst in Environmental Biotechnology and Industrial Applications: A Review
Mohd Asyraf Kassim1*, Noor Haza Fazlin Hashim2,3 and Nur Athirah Yusof4
1Bioprocess Technology Division, School of Industrial Technology, Universiti Sains Malaysia (USM), Malaysia. 2School of Biosciences and Biotechnology, Faculty of Sciences, Universiti Kebangsaan Malaysia (UKM), Malaysia. 3Water Quality Laboratory, National Hydraulic Research Institute Malaysia (NAHRIM), Seri Kembangan, Malaysia. 4Biotechnology Research Institute, Universiti Malaysia Sabah (UMS), Malaysia.
Authors’ contributions
This work was carried out in collaboration between all authors. Author MAK manage the outline and literature search and wrote the first draft of the manuscript. Authors NHFH and NAY helped in the writing certain part of the manuscript such as introduction and revised the manuscript. All authors read and approved the final manuscript.
Article Information
DOI: 10.9734/JAMB/2017/35591 Editor(s): (1) P. Rama Bhat, PG Biotechnology, Alva’s College, Karnataka, India. Reviewers: (1) Eliton da Silva Vasconcelos, Federal University of São Carlos – UFSCar, Brazil. (2) Selma Gomes Ferreira Leite, Universidade Federal do Rio de Janeiro, Brasil. Complete Peer review History: http://www.sciencedomain.org/review-history/20731
Received 20th July 2017 Accepted 21st August 2017 Review Article Published 30th August 2017
ABSTRACT
Achaea constitute a considerable fraction of the prokaryotes which colonize marine and terrestrial ecosystem especially in the extreme environments. These microorganisms play crucial roles and contribute significant impacts on global energy cycles. In fact, the extremophilic characteristics acquired by many archaeans display unusual properties of adaptations to extreme conditions which make them a potentially valuable resource in exploring new biotechnological processes and a wide range of industrial applications. In this review, the role of archaea domain as biocatalysts in environmental biotechnology and industrial applications were summarized and discussed. This review has been categories into three main sections, (a) archaeal characteristics and their extremozymes (b) environmental biotechnology that covers on bioremediation, hydrocarbon biodegradation and biomining (c) industrial applications, which discusses on the production of polyhydroxyalkanoates (PHA), biosurfactant, and antibiotic produced by archaea domain.
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*Corresponding author: E-mail: [email protected], [email protected];
Kassim et al.; JAMB, 5(2): 1-21, 2017; Article no.JAMB.35591
Keywords: Archaea; aromatic; bioleaching; extremozyme; halocin; polyhydroxylalkanoate (PHA).
1. INTRODUCTION shapes, ranging from spherical, spiral, oblong, rectangular to rod. One of the distinguishing Archaea are prokaryotic microorganisms that can features of archaea is the structure of their be found in the extreme environments. Due to membrane glycolipids; where archaea do not their capability to live under extreme conditions, contain murein at their cell wall. Archaea exhibit the exploration on the potential of archaea as unique features of cell surface organelles that biocatalysts for industrial applications has are not present in bacteria such as flagella, hami, become the subject of intensive research, aiming cannulaeand pili [1]. on the cell structures, enzyme characterizations and its adaptability under extreme conditions. Year 1977 marked a history when Carl Woese, a These exclusive properties make them as a microbiologist discovered two distinct groups of valuable resource with great potential organisms that were not related to one another applications in a wide range of new technologies. than they were to eukaryotes [2]. Later, a new classification was proposed based on Moreover, the study on archaeal enzymes that comparisons of gene sequences of the small are able to maintain their activity under extreme ribosomal subunit (SSU), which was accepted conditions such as high temperature, salinity, pH until now; three domains of life consist of and pressure has also gain great interest among Eukarya, Bacteria and Archaea [3]. After the researchers. The discovery of extremophilic discovery by Woese, molecular biology archaea and their enzymes has lead to techniques have been the preferred choice to significant effects conspicuously on biocatalysis distinguish between archaea and bacteria. activities. In addition, extremozymes produced by Indeed, the organization and information archaea are widely used in the synthesis of processing system in archaea point to a closer pharmaceutical products, antibodies, cosmetics, relationship to eukaryotes rather than bacteria. dietary supplements, enzymatic preparations, Apart from that, the structures of ribosomes and bioremediation, renewable energy, as well as all chromatin, presence of histones and sequence kinds of chemical compounds production. The similarity contribute to the classification of application of extremozymes from archaeal cells archaea [4,5]. In contrast, the metabolic has allow great improvements in multiple industry pathways of archaea show similarity to sectors and help to reduce the quantity of waste prokaryotic rather than eukaryotic counterparts production, energy usage and material [6]. Table 1 shows the comparison of consumption. Thus, archaeal applications harbor characteristics between bacteria and archaea. promise for creating cheaper technology, cost- effective sustainable energy sources and 3. BIOCATALYST environmentally friendly. The trend to an increasing number of researches The main hallmarks of this review are to discuss on genome data of extremophilic microorganisms and provide a comprehensive review on the worldwide has able to discover hundreds of future prospects of achaea as biocatalysts in enzymes with great potential in white environmental biotechnology and other industrial biotechnology. Currently, extremozymes are applications. In this review, the emphasis highly in demand in industries as they are able to encompasses on the type of extremozymes that withstand harsh processes for a long period of are produced by different group of achaea, time. Overall at present, microbial enzymes are enzymes and metabolites production and their currently on demand in various industries as they potential industrial applications. This review contribute immense advantages such as would be beneficial to scientists and researchers reducing the risk of contamination, improving the in understanding the potential of achaea as tools transfer rates, lowering viscosity and increasing for various value-added products and the solubility of substrates. Majority of the revolutionize the current industrial applications. industrial enzymes have been derived from bacteria and fungi. Nowadays, archaeal enzymes 2. ARCHAEA are in the limelight of intensive investigations due to their nature that grow optimally at extreme In general, Archaea have similar characteristics conditions. In terms of definition, extremozymes as bacteria in terms of shape, size and are enzymes that are able to withstand appearance. Archaeal cells can take all types of harsh and extreme conditions in industrial
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Table 1. Comparison of the distinctive characteristics of Archaea and Bacteria
Archaea Bacteria Ribosome Present Present Cell wall Pseudopeptidoglycan Peptidoglycan/Lipoposacchari de Habitat Extreme environment: hot spring, Soil, water, animal, plant and salt lake, ruminant etc. Growth Asexually by the process of binary Asexually by the fission, budding and fragmentation binary fission, budding and fragmentation Ability to form spore Genomic organization Topoisomerase I I/III Recombinase RadA RecA DNA ligase NAD dependant ATP dependant Replicative HelicaseA DnaB helicase DNA polymerase Family B polymerase DNA E polymerase (PolIII) Histones Yes No Introns Some present Rare/none Protein synthesis Methionine as start codon Formylmethionine as start codon Example Family Family Enterobactericeae Euryarchaeota (Aciduliprofundum (Escherichia coli) and boonei) and Crenarchaeota Streptococaceae (Sulfolobus solfataricus) (Streptococcus pneumoniae) processes [7]. Perhaps, the high demands of the temperature such as increased hydrophobicity biotech industries for tailor-made novel and surface charge, higher hydrogen bonds, biocatalysts, and the rapid development of new shorter loops structure, reduction in thermolabile techniques such as genomics, proteomics and amino acid, and lowered in surface area to metabolomics are the main factors contributing volume ratio [9]. Owing to that, thermophilic the enhancement of the development of novel enzymes are currently on demand in vast extremozymes. Here, this review will focus on industries which require superior biocatalysts that enzymes that are derived from extremophilic are capable to work at high temperatures. archaea and their relevance for industrial Moreover, reactions at high temperatures reduce applications. the probability of undesired by-products and microbial contamination. In addition, thermophilic 3.1 Thermophilic Extremozymes archaea also show high resistance under high pressure and presence of chemical denaturants Thermophiles can be further categorized either such as solvent and detergents [10]. as thermophiles or hyperthermophiles. Hyperthermophiles can grow optimally up to Glycoside hydrolases are large group of 115°C, whereas thermophiles grow best between enzymes involve in carbohydrate hydrolysis. 50 and 70°C. Majority of thermophiles/ Enzymes in this group are greatly in demand hyperthermophiles are identified to date belong especially those that are able to perform at high to the archaeal domain mainly from temperatures. Glucose production from starch for Crenarchaeota, Euryarchaeota, Korarchaeota instance, involves two-step processes where and Nanoarchaeota [8]. Most common habitats both are carried out at high temperature of (60- where archaea are naturally found are in the 105°C) and acidic pH of (4.5–6.0) [11]. The volcanic areas, geothermal systems and hot usage of thermostable amylolytic enzymes springs. To date, protein structural studies on (α-amylases, α-glucosidases, α-pullulanases) thermophilic enzymes show several factors provides advantages as novel energy which contribute to the enzymes stability at high alternatives, cost saving, as well as
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environmentally friendly process. Currently, was isolated from thermophilic bacteria, hydrolytic enzymes from Bacillus Thermusaquaticus [19]. Recently, polymerases stearothermophilus and B. licheniformis are from archaeal have been developed since these currently being used in the industry. Interestingly, polymerases show prominent advantages such several studies have reported higher activities of as stringent proofreading ability and five to thermostable hydrolases enzymes from archaea tenfold lower of error rates compared to compared to bacterial enzymes. On the other Taqpolymerase. Several DNA polymerases from hand, hyperthermophilic amylases are also archaea are already isolated and exhibited high reported from archaea of the genera Sulfolobus, commercial values such as from Thermococcus Thermophilum, Desulfurococcus and celericrescens (TceI) [20], Thermococcus Staphylothermus, which are recorded to be fumicolans (Tfu) [21], Thermococcus zilligii (Tzi) active at a broad range of temperatures ranging [22], Pyrococcusabyssi (IsisTM) [23]. from 40–100°C [12]. In addition, another study on thermostable α-amylase from Pyrococcus 3.2 Psychrophilic Extremozymes furiosus reported that the enzyme has a half life activity at 120°C after autoclaving for 2 hours Psychrophiles are defined as microorganisms and fascinatingly still exhibit residual activity at that are able to proliferate at 0–10°C, 140°C [13]. In another study, thermophilic metabolically active at subzero temperatures and pullulanases which usually belong to the type II also able to survive as low as −45°C [24]. class acquired enzymes that are able to Psychrophiles can be found either in hydrolyze both α-1,4- and α -1,6-glycosidic permanently cold environments such as bonds in branched polymers [11]. A heat-active permafrost, sea ice, polar, glacier or artificially pullulanase with an optimum temperature of cold environment such as the refrigerator. In 100°C has been discovered in Thermococcus order to adapt, psychrophiles produce enzymes kodakarensis KOD1 [14]. α-glucosidases are that are able to work optimally at cold involved in the final step of starch degradation, temperatures. Generally, cold adapted enzymes hydrolyzing terminal glucose residues. have higher structural flexibility and catalytically Thermophilic archaeal P. furiosus α-glucosidase effective at cold. Several features of cold has been characterized extensively where it adapted proteins have been reported to show works optimally at the range of temperatures unique characteristics compared to their between 105–115°C [15]. mesophilic and thermophilic counterparts. These include fewer disulfide bonds and salt bridges, Similarly, xylanases have been widely studied more solvent interactions, lower number of due to their ability to degrade hemicelluloses; the hydrogen bonds at domain interfaces, lower core most abundant natural resources. This type of hydrophobicity, and longer loops structure [25]. enzymes advocates attractive value to the paper bleaching industry; as an alternative to current Studies on psychrophilic archaea mainly focus chemical treatment; thus promoting an on methanogens as they play important roles in environmentally friendly industry [16]. However anoxic permanently cold environment like lake bleaching process performs optimally only at sediments, deep sea and permafrost. Genome high temperature therefore, the need of and proteome analysis on Methanococcoides thermostable xylanase is crucial. Recently, a burtonii have disclosed mechanisms for its thermostable xylanase was reported from survivability at cold environment [26,27]. The Thermotogathermarum, Xyn10A with a maximal usages of cold adapted enzymes are currently activity exhibited at 95°C, pH 7.0 [17]. In the center of attention of many researchers due addition, it has demonstrated high thermostability to their natural properties that able to grow/work over broad range of pH 4.0–8.5 and temperature optimally at cold temperatures. However, studies 55-90°C upon the addition of 5 mM Ca2+. On the of archaea and cold adapted enzymes from other hand, a xylanase from Thermococcus archaea are still in infancy level compared to zilligii is reported active at 100°C and has bacteria. To date, several applications have been preferences to different substrates [18]. reported of using archaea in wastewater treatment and methane production [28,29]. DNA polymerase; the key enzyme that is Similarly, archaeal enzymes/cofactors are also responsible in molecular biology especially for reported to involve in metabolic, light-harvesting DNA amplification in polymerase chain reaction, complexes and ether-linked lipids, which show has drawn high interest in biotechnology impressive values in biotechnology applications industries. The first DNA polymerase used, Taq [30,31].
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3.3 Haloarchaeal Extremozymes candidates in the industrial applications especially in food processing. Halophiles are organism that is able to thrive optimally at high salt concentration (> 0.6M NaCl; 4. BIOREMEDIATION seawater salt concentration). In this context, archaea have been discovered in several Bioremediation is a process of utilizing natural or ecological niches like Dead Sea and Great Salt genetically engineered living organisms such as Lake, where most of the isolated archaea are fungi, bacteria and archaea to transform pollutant able to adapt with the osmotic changes in their and contaminants from the environment into less environments [32,33]. Enzymes from halophiles toxic compound. Accordingly, bioremediation has remain active and stable although being exposed been proven to degrade hydrocarbon and other to high salt concentration due to the presence of aromatic compounds in soil and water. The unique properties in their proteins like high acidic success of this technology depends on the ability amino acids content, less hydrophobic surface to establish and maintain the favor of microbe to contact and presence of specific ion binding site grow and enhance the biodegradation rates in [34,9]. the contaminated environment. Hence, it is unsurprising that the suitable conditions such as Due to the ability to withstand extreme salt pH, temperature and salinity have been reported concentrations, halophiles have been first to influence the microbe growth and chosen to be applied in various industries. Many biodegradation metabolic activity [40,41]. enzymatic activities of halophilic archaea have Moreover, the physical and chemical been characterized, however no commercial characteristics of oil and oil surface also play applications have yet been developed for such crucial role to ensure the bioremediation enzymes [35]. Still, some archaeal enzymes success. Though this technology has been have triggered some potential interests, such as proven to be able to remediate contamination, the amylase of Haloarcula sp. that functions however there is a limitation for the optimally at 4.3 M salt at 50°C and known to be bioremediation process in extreme condition stable in the presence of benzene, toluene and such as high salinity and temperature. This is chloroform [36]. In addition, halophilic due to the fact that not many microorganisms galactosidases from Haloferax alicante that are have the capability to grow in these harsh active at 4M NaCl with the ability to cleave broad conditions. Archaea are one of the microbes that galactosidases excluding lactose have been long have gained much attention to remediate identified [37]. Besides, the archaeon Haloferax hydrocarbon contamination especially in the mediterranei has been reported to be able to extreme conditions. Analysis of microbial produce up to 38% Poly-β-hydroxyalkanoate community on soil sample contaminated with (PHA) compound from its dry weight grown at petroleum hydrocarbon in the European Alps, 150 g/L salt under phosphate limitation [38]. using fish-in-situ hybridization (FISH) and identification via 16S rRNA, revealed that a 3.4 Piezophilic Extremozymes number of archaea related to the orders of Methanomicrobiales, Methanosarcinales, Organisms that are able to thrive at high Methanobacteriales and Thermoplasmatales pressure are generally called as piezophilic. have been detected in that area [42]. In another Often they colonize in habitats like deep sea and study, a range of archaeal community that has extreme heat of hydrothermal vents. Piezophilic functions in hydrocarbon-degradation, production archaea are usually characterized as of surfactant and methanogenesis during the thermophilic as they are mainly being isolated displacement of oil such as Thermus, from thermophilic habitats [39]. The general Thermincola, Thermanaeromonas have been properties of piezophilic enzymes usually similar found in high-temperature oil reservoir [43]. to their temperature adaptation but with additional features; exist as multimers, smaller On a large scale, many researchers have hydrogen bonding amino acids and packed reported on the potential of archaea as hydrophobic core [9]. Paradoxically, research on biocatalyst in bioremediation [44-46]. Mainly, as piezophiles archaea are limited due to the archaea can grow in hypersaline condition and difficulties in culturing the strain at high pressure. encapsulate great catabolic activity compared to Albeit, the piezophiles are usually coupled with bacteria and fungi hence, archaea probably either high or low temperature adaptations comprise excellent selections as best possible mechanisms that making them as a great biocatalyst candidates [47]. On top of that,
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archaea can growth in either high or low of incubation. Based on previous studies, these temperatures and extreme pH conditions, findings suggested that halophilic archaea have contrariwise to bacteria which are commonly the capability to degrade crude oil at high used for bioremediation but are unable to survive temperatures and are probably the most suitable in these harsh conditions [43,48]. This unique candidates to be applied in bioremediation ability clearly provides advantages for archaea process at extreme environment conditions. especially to remediate contaminations that occur in extreme environments. Fascinatingly, it 4.2 Aromatic Compound Degradation has also been reported that some archaea show high resistant towards variety of antibiotics Apart from degrading aliphatic hydrocarbon, including cycloheximide, streptomycin and archaea have also been reported to acquire the penicillin, which turn archaea as a great potential ability to degrade aromatic hydrocarbon. Several to be applied in bioremediation in the presence of studies have been conducted to isolate and antibiotic [49]. determine the archaea that could degrade aromatic hydrocarbon. It has been reported that 4.1 Hydrocarbon Biodegradation Haloarchaea Haloferax sp. has the capability to degrade phenanthrene [46,49]. Study by Studies on bioremediation using archaea Emerson et al. [53] reported that Haloferax strain have been reported previously by other D1227 isolated from soil contaminated with oil researchers [49,50]. Table 2 shows the isolated brine was able to use aromatic hydrocarbon such halophilic archaea that have been reported to as benzoate, cinnamate and phenylpropanoate demonstrate capability to degrade hydrocarbon. as carbon source with 70% degradation. Archaebacterium strain EH4 which was isolated Similarly, Bonfa et al. [44] who investigated the from sail-mash was found to be able to grow in potential of Haloferax sp. to degrade aromatic medium supplemented with 20% NaCl [50,51]. reported that this archaea was able to degrade This study reported that this archaea could grow the mixture of aromatic compound. For this and degrade eicosane up to 62% of particular study, Haloferax sp. was cultured in a biodegradation in 10 hours of generation time. In medium with aromatic compound mixture of another study, three extreme halophilic benzoic acid, p-hydroxybenzoic acid, salicylic Haloferax, Halobacterium and Halococcus have acid and mixture of polycyclic aromatic been isolated from hypersaline coastal area of hydrocarbon. It was found that this archaea was Arabian Gulf. All of these archaea are able to use able to grow and degrade these compounds. crude oil as sole carbon source for energy. This In another study, other archaea members study also demonstrates that these strains are such as Halobacterium piscisalsi, Halorubrum able to use and degrade n-alkanes and mono- ezzemoulense, Halobacterium salinarium, and polyaromatic compounds as carbon and Haloarcula hispanica, Haloferax sp., Halorubrum energy source [49]. Interestingly, these archaea sp., Haloarcula sp. isolated from Camalti Saltern, could degrade crude oil up to 47% after 3 weeks Turkey have also exhibited capability to degrade of incubation at 40-45°C. Similar observation has aromatic hydrocarbon compound [45]. It was also been reported by Tapillatu et al. [46], who reported that Halorubrum sp. and Halorubrum isolated Haloarcula and Haloferax sp. that could ezzemoulense could grow in medium degrade 95% heptadecane at 40°C after 30 days supplemented with 20% NaCl.
Table 2. Halophilic archaea that are able to grow and use hydrocarbon as carbon and energy source
Archaea Hydrocarbon References Haloferax sp. n-alkane C10-C30 [46] Haloferax sp. Heptadecane [46] Haloarcula sp. Heptadecane [46] Halobacterium sp. n-alkane C10-C34 [49] Halococcus sp. n-alkane C10-C34 [49] Strain EH4 Tetradecane [51] Hexadecane Eicosane Heneicosane Halobacterium sp. n-alkane C10-C30 [52]
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4.3 Biomining There are several recent reviews on the biomining mechanisms that can be carried out by Metals and mining sector is considered as one of microbes. The bioleaching process of metal the major industries that is dedicated for could also contributed by the type of metals, its extraction of metal and valuable minerals from properties and mineral species [54]. There are lode, orebody, seams, and reef reserves in the two different reaction mechanisms that control world. These minerals are gold mine for profit the dissolution of metal sulfides: the thiosulfate and widely used in a vast range of industrial pathway and the polysulfate pathway. The applications, for instance, jewelry making, oxidation of acid-insoluble metals sulfide (pyrite, construction, ceramics, automobiles, electronics, molybdenite, tungstenite) and acid-soluble metal plastics and paper. Current mineral extraction sulfide (chalcopyrite and pyrrhotite) can be involved high temperature and chemicals which categories into the thiosulphate intermediate potentially lead to environmental pollution. pathway and polysulphide intermediate pathway Therefore, biomining using microbial has been (Fig. 1) [55]. The thiosulphate pathway is a considered to be an alternative approach to process where the metal is solubilized by ferric overcome the problem. In this process, microbes ion that generated by microbial process. In this are utilized to recover mineral resources such as pathway, the acid-insoluble metals sulfide such copper and other metals or minerals from low- as pyrite (FeS2), molybdenite (MoS2) or grade ores, waste, slag and sludge. This tungstenite (WS2) are exclusively oxidized via technique experimentally showed that it could electron extractions by ferric (Fe(III)) ions and improve recovery rate, reduce operational cost, thiosulphate is generated as main intermediate require less energy and reduce pollution product. On the other hand, the polysulphate problems. Biomining of minerals is carried out on pathway is a mechanism that the acid soluble different scale with different type of microbes metal sulfide such as sphalerite (ZnS) and including bacteria and archaea. The biomining chalcopyrite (CuS) are solubilized by process artificially can be divided into two modes combination attacked of ferric ion and proton. In namely bioleaching and bioxidation. this process, an element such as stable sulfide + Bioleaching- can be related to solubilization of cation (H2S ) is generated as main intermediate. metals such as copper, nickel, and zinc from However, this sulphate can spontaneously ores by microorganisms. While, biooxidation is dimerize to free disulfide (H2S2) and further used for bioleached solubilized metals which oxidized by sulphur-oxidizing microbes such as wrapped/locked in sulfide minerals such as gold archaea and bacteria via higher polysulfides and and silver. polysulfide radical to generate sulfur element.
Fe2+ (a)
Oxidizing-microbe, O2
Metal sulfide 2+ 2- 2- SO 2- + H Cu + S2O3 SnO6 , S8 4 2 Fe3+ Oxidizing-microbe Oxidizing-microbe
Fe2+ (b)
Oxidizing-microbe, O2
Metal sulfide 2+ SO 2- + H Cu + H2S+(H2S2) H2Sn, S8 4 2 Fe3+ Oxidizing-microbe Oxidizing-microbe H+
Fig. 1. The schematic diagram of the bioleaching mechanisms (a) The thiosulfate pathway (b) The polysulfate mechanisms
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3+ H+ Non-contact mechanisms Fe
2+ 2- Fe SO4 Fe 3+ or Fe 2+ - proton attack HS-
0 2+ S S2O3
EPS
2+ cell SO4
S0 cell
Contact mechanisms Fe 2+
Fe 3+
Fe 2+, sulfur intermediate and minerals fragment for iron and sulfur oxidizer microbes Cooperative leaching
Metal sulfide Leachate solution
Fig. 2. Contact and non-contact leaching mechanisms by microbes (Archaea and bacteria)