Diversity and Niche of Archaea in Bioremediation

Krzmarzick, Mark James; Taylor, David Kyle; Fu, Xiang; McCutchan, Aubrey Lynn

doi:https://doi.org/10.1155/2018/3194108

Archaea

On this page

Abstract Introduction Conflicts of Interest Acknowledgments References Copyright Related Articles

Special Issue

Archaea in Wastewater Treatment: Current Research and Emerging Technology

View this Special Issue

Review Article | Open Access

Volume 2018 | Article ID 3194108 | https://doi.org/10.1155/2018/3194108

Diversity and Niche of Archaea in Bioremediation

Mark James Krzmarzick,¹David Kyle Taylor,¹Xiang Fu,¹and Aubrey Lynn McCutchan¹

Academic Editor: Yu Tao

Received05 May 2018

Accepted01 Aug 2018

Published03 Sept 2018

Abstract

Bioremediation is the use of microorganisms for the degradation or removal of contaminants. Most bioremediation research has focused on processes performed by the domain Bacteria; however, Archaea are known to play important roles in many situations. In extreme conditions, such as halophilic or acidophilic environments, Archaea are well suited for bioremediation. In other conditions, Archaea collaboratively work alongside Bacteria during biodegradation. In this review, the various roles that Archaea have in bioremediation is covered, including halophilic hydrocarbon degradation, acidophilic hydrocarbon degradation, hydrocarbon degradation in nonextreme environments such as soils and oceans, metal remediation, acid mine drainage, and dehalogenation. Research needs are addressed in these areas. Beyond bioremediation, these processes are important for wastewater treatment (particularly industrial wastewater treatment) and help in the understanding of the natural microbial ecology of several Archaea genera.

1. Introduction

The contamination of soil, sediment, and water from industrial and other human inputs is widespread and poses a threat to human and ecological health. Bioremediation is the use of microbes for the beneficial removal of contaminants of concern [1]. The microbial processes involved in bioremediation are normally natural components of respiration or adaptation, often a component of carbon cycling or metal redox cycling. Thus, bioremediation often occurs without direct intervention; however, biostimulation (the addition of nutrients or adjustment of conditions) and bioaugmentation (the addition of microbes capable of bioremediation) are often important for the complete removal of contaminants within an economical timeframe. The field of bioremediation research has traditionally focused heavily on processes from the domain Bacteria, which has a large diversity of bioremediation applications. In many applications where Bacteria are the key players in bioremediation, however, Archaea are often involved as well. In “extreme” environments, archaeal processes are of particular interest for bioremediation. Many Archaea are extremophiles, capable of living in environments considered uninhabitable by most other organisms, and many extreme environments become contaminated and are in need of remediation. Furthermore, many industrial wastewaters have hypersaline, hyperthermal, metallic, and/or an acidic or alkaline pH, where extremophilic Archaea have the potential to play key functions for contaminant removal.

This manuscript aims at providing an overview of the various roles that Archaea have in bioremediation. This review is meant to be comprehensive but with a particular focus on recent contributions. Both pure culture and mixed community studies are included in the review. The review does not cover nutrient cycling. Nor does it explicitly cover wastewater treatment or provide any explicit review of the environmental microbiology of Archaea; however, bioremediation is heavily interconnected to these areas. The review summarizes major findings and suggests future areas of research needed to strengthen our understanding of the contributions of Archaea in bioremediation. Though many chapters and reviews exist that encompasses pieces of the topics below, as of the submission of this article, the authors have not uncovered any other comprehensive review that focuses purely on Archaea in the bioremediation area.

2. Archaea in the Degradation of Organics in Hypersaline Environments

Perhaps, the most developed research area that connects Archaea to bioremediation lies within the degradation of organics in hypersaline environments. Natural hypersaline environments include salterns, salt lakes, salt marshes, salt flats (sabkhas), and oil and gas production wastewaters. The contamination of these environments with crude oil is common, and about 5% of the chemical, pharmaceutical, and oil industries have highly saline wastewater effluents in need of treatment [2]. Members of both Bacteria and Archaea are known to inhabit such environments and these are often referred to as “halobacteria” and “haloarchaea,” respectively. Recent reviews have focused on hydrocarbon degradation by halobacteria and haloarchaea [3–5], the biotechnological potential of the hydrolytic enzyme [6], the biodiversity of microbial communities in halophilic environments [7, 8], the potential of haloarchaea in bioremediation processes [9], and the growing rate of research of haloarchaea in bioremediation [10]. Recently, a new database—called HaloDom—has compiled all isolated halophilic species into a single online resource [11]. Many Bacteria can degrade at salinities of up to 15% such as strains of the genera Ralstonia, Halomonas, Dietzia, and Alcanivorax [12, 13]. Here, an overview of the haloarchaeal strains isolated on the ability to degrade hydrocarbons, such as crude oil, is provided.

The haloarchaea cluster into a single class (the class Halobacteria) within the phylum Euryarchaeota. They are typically cultured at neutral pH and temperatures of 30-45°C, and they require high salinities of 1.8–5.0 M NaCl [14–17]. Many strains have been traditionally isolated on a standard nutrient media that contains heterotrophic carbon and energy sources [15]. Table 1 lists the strains associated with hydrocarbon degradation and their degradative abilities. Additionally, a phylogenetic tree of many of these strains (where nearly full-length 16S rRNA gene sequences were available), as well as other strains and phylogenetic groups discussed in this manuscript, is shown in Figure 1. The metabolic capabilities of haloarchaea for hydrocarbon degradation appear vast, and these Archaea all inhabit a close phylogenetic association.

The connection between the haloarchaea and the degradation of crude oil and xenobiotic pollutants extends past three decades. A haloarchaea strain named EH4, later determined to be closely related to Haloarcula vallismortis [18], was isolated in 1990 from a salt marsh in France and found able to degrade various aliphatic and aromatic hydrocarbons [14]. The discovery of hydrocarbon-degrading haloarchaea was independently confirmed with a manuscript published in 1991 reporting the isolation of a Halobacterium strain from a hypersaline wastewater in Russia that degrades alkanes [19]. Haloferax volcanii strain D1227 was then isolated from a saline oil brine from Michigan (USA) on monoaromatic carboxylic acids as sole carbon and energy sources [20] and later found to degrade 3-phenylpropionate [21]. Haloferax mediterranei st. M-11 was isolated from the brine of the Kalamkass oil field (Mangyshlak, Kazakhstan) [22]. Haloarcula st. D1 was then isolated and capable of aerobically degrading 4-hydroxybenzoic acid which is a pollutant in certain industrial wastewaters [23]. The degradation pathway consisted of a gentisate-1,2-dioxygenase pathway which was found key in the degradation pathways for Haloferax volcanii st. D1227 as well [24, 25]. A sampling of hypersaline lakes in Turkey resulted in 33 isolates of Halobacteriaceae across 9 genera [26]. Though these isolates were not directly tested for degradation of crude oil or related hydrocarbons, all 33 isolates tested positive for catalase and oxidase activity and 15 tested positive for Tween 80 hydrolysis [26]. A recent manuscript reported the isolation of four further Halobacteriaceae that could also hydrolyze Tween 20 and Tween 80 [27]. Though the Tween 80 and Tween 20 tests are used as a standardized physiological lipase test for microbes [28], it is potentially of particular interest in bioremediation because Tween 80 and related compounds are used as surfactants in oil spill remediation and in hydraulic fracturing mixtures [29, 30].

The study of haloarchaea in bioremediation has gained significant traction in recent years. Four heptadecane-degrading halophilic archaeal strains were isolated from an uncontaminated salt crystallization pond in Camargue, France (Haloarcula st. MSNC 2, Haloferax st. MSNC 2, Haloferax st. MSNC 14, and Haloferax st. MSNC 16) [18]. Haloferax st. MSNC 14 also grew on phenanthrene while the other three isolates could not [18]. Later research found that Haloferax st. MSNC 14 produced surfactants during growth on n-heptadecane, pristane, and phenanthrene, but not during growth on acetate [31]. Thus, it was able to increase the bioavailability of low-solubility hydrocarbons during their degradation [31]. Four strains were also isolated from soil and water in a hypersaline coastal area of the Arabian Gulf (Haloferax st. HA-1, Haloferax st. HA-2, Halobacterium st. HA-3, and Halococcus st. HA-4) with a multitude of alkane and aromatic degradation abilities [16]. Ten strains of Haloarchaea closely related to Haloferax were isolated from salt marshes, salterns, crystallizer ponds, salt flats, and the Dead Sea and were found to degrade a mixture of polycyclic aromatic hydrocarbons and crude oil [17]. This study also found that Haloferax volcanii st. DS2 could degrade these polycyclic aromatic compounds [32]. This strain, which was isolated from the Dead Sea on glycine and yeast autolysate [33], has just prior had its genome sequenced [34]. Haloterrigena mahii sp. H13, collected from a saltern pond in San Diego, CA, USA, also had its genome sequenced and contains genes that may be involved in the degradation of 1,2-dichloroethane, naphthalene/anthracene, γ-hexachlorocyclohexane, 1-/2-methylnapthalene, and benzoate [17, 35]. A literature search has not uncovered any research that directly tested the aforementioned biodegradation capabilities with this pure culture.

The diversity of haloarchaea-degrading hydrocarbons, and of xenobiotics that they can degrade, has been expanding. A strain of Halobacteriaceae (named L1) was isolated from the Dead Sea and could grow on benzoic acid [36]. Natrialba sp. st. C21 has also been isolated from oil-contaminated saline water in Ain Salah, Algeria [37]. This strain can degrade phenol, naphthalene, and pyrene through an ortho-cleavage pathway and exhibits catalase, oxidase, and Tween 80 esterase activity [37]. Acikgoz and Ozcan [38] found eight Halobacteriaceae out of a screening library of 103 isolates that could degrade and tolerate above 200 ppm phenol. The fastest phenol-degrading strain was identified as a Haloarcula sp., but more detailed phylogenetic characterization was not provided [38]. In another study, nine isolates were found that can use aromatic hydrocarbons for carbon and energy sources [39]. These isolates were identified as members of Haloferax sp. (isolates C-24 and C-27), Halobacterium piscisalsi (st. C-37), Halobacterium salinarum (st. C-51), Halorubrum ezzemoulense (st. C-41 and C-46), and Halorubrum sp. (st. C-43), and two strains (C-50 and C-52) reported with less than 93% 16S rRNA gene identity to any isolated strains [39]. Upon inspection of the deposited sequences in NCBI’s GenBank, the sequence for strain C-50 appears to have poor sequence quality; a BLAST search of the first 280 bp recovered zero alignments to sequences in GenBank. Strain C-52 has 99% identity along the more recently deposited 16S rRNA gene of Halorubrum trapanicum CBA1232, which has a deposited genome (NCBI BioProject PRJDB4921); however, no publications are associated with this genome [40]. All nine strains degraded naphthalene, phenanthrene, and pyrene, and all but strain C-37 and C-51 degraded p-hydroxybenzoate [39]. Degradation in all cases was through ortho-oxidation through a catechol 1,2-dioxygenase or a protocatechuate 3,4-dioxygenase pathway [39]. A microbial community enriched from the Great Salt Lake (Utah, USA) consisted of several genera entirely of the class Halobacteria, with 91% belonging to the genera Halopenitus as determined by 454 sequencing of 16S rRNA genes [41]. This community could grow on 4-hydroxybenzoate but not the other carbon sources tested, and the degradative pathways and genes were analyzed with PCR approaches of functional genes [41].

Though the isolation of haloarchaeal strains from contaminated sites is successful and haloarchaea are often found in natural environments (i.e., [42, 43]), the understanding of the microbial ecology of these strains on oil contamination under in situ conditions is not well developed. A few studies investigating the distribution of the haloarchaea have been done. The archaeal community in a saline-alkali soil in the Dagang Oilfield (China) differed significantly along a petroleum contamination gradient, with four groups of Archaea, including Haloferax and Natronomonas, being abundant in the contaminated soils while five different groups of Archaea were dominant in noncontaminated soils [44]. Other studies have profiled further diversity of haloarchaeal groups in oilfield sites, including the genera Halalkalicoccus, Natronomonas, Haloterrigena, and Natrinema, suggesting that varied haloarchaea are widely present in these contaminated environments [45]. Though Haloferax has a number of isolates known to degrade aromatics, Natronomonas is not as well established to oil degradation, though it does contain fatty acid degradation pathways and is thus putatively able to degrade alkanes [46]. Thus, these genera are likely degrading the organics in situ. In contrast, in a hypersaline-produced water from the Campos Basin (Brazil) contaminated with phenol and aromatics, the archaeal community consisted of no detected haloarchaea in situ but was rather dominated by methanogens (59% Methanosaeta and 37% Methanoplanus) [47]. Methanogens have a role in the final degradation of hydrocarbons in coculture with hydrocarbon-degrading Bacteria (see below); the presence of methanogens and the lack of haloarchaea suggest a highly reduced environment. Hydrocarbon-degrading halophilic bacteria (specifically, Halomonas) were isolated from these waters and could degrade these contaminants, especially with biostimulation [48]. The contaminants in this production water were also degraded more significantly in a previous study with the bioaugmentation of haloarchaea strains [32]. The bacteria Halomonas and haloarchaea survive in similar salinities and contain similar degradative capabilities [4]; however, it is not known what drives the competitive advantage of one over the other.

Recently, further studies have progressed towards evaluating bioremediation techniques with haloarchaeal communities. A recent study focused on how vitamin amendments may stimulate crude oil degradation [49]. Vitamin B₁₂ enhanced the degradation of crude oil from five Archaea strains tested (Haloferax lucentense st. AO1, Halobacterium salinarum st. AO2, Halobacterium piscisalsi st. AO3, Haloferax mucosum st. AO4, and Halobacterium sulfurifontis st. AO5) [49]. Pyridoxine enhanced the biodegradation of oil by four of these strains (A01, A02, A04, and A05), riboflavin enhanced the degradation by three strains (A01, A02, and A05), folic acid enhanced the degradation by three strains (A01, A03, and A05), and thiamin enhanced the degradation by one strain (AO5), but biotin did not enhance oil degradation significantly by any of the five strains [49]. The biostimulation with vitamins is not surprising, as earlier work has shown that a nutritional yeast extract amendment significantly increases hydrocarbon degradation [32]. The strains were found to also degrade Tween 80, n-octadecane, and phenanthrene and were also enhanced with 0.75 M KCl and 2.25 M MgSO₄ [49, 50]. In another study, continuous illumination and casamino acids were found to increase oil biodegradation by mixed cultures dominated by Haloferax sp. and by four isolates (two identified as Haloferax, one as a Halobacterium, and one as a Halococcus) [51]. Haloferax elongans st. M4 and Halobacterium salinarum st. M5 were found capable of being cultured onto a Bacteria-Archaea biofilm community for the degradation of crude oil, n-hexadecane, and phenanthrene [52]. Such biofilm communities have advantages in bioremediation technologies. There too, vitamins stimulated crude oil degradation in the biofilm [52]. In yet another study with a mixed community of Bacteria and Archaea, the addition of casamino acids and citrate was required for oil degradation and the microbial community dynamics were observed [53]. After adding crude oil to the culture, biotic degradation could not occur and the archaeal community shifted away from what was previously high levels of Haloquandratum, to one in which only Natronomonas spp. remained, while the bacterium Salinibacter was selected [53]. With the additional amendment of casamino acids and citrate, the community could degrade oil with an archaeal enrichment of Haloarcula, Haloterrigena, and Halorhabdus [53]. A recent study investigated the biostimulation of oil-degrading cultures derived from a hypersaline sabkha and found that Fe⁺³, Ca⁺², Mg⁺², K⁺, animal blood, and commercial yeast all had a stimulatory effect towards oil degradation [54]. Haloarchaeal communities were dominated by Haloferax spp. and Halobacterium spp., and eight strains were isolated (two associated with Halobacterium noricense, two with Haloferax larsenii, a Halobacterium salinarium, and a Halobacterium sp.) [54]. These strains could grow on a variety of alkanes and aromatics and degraded between 22 and 36% of amended crude oil over 2 weeks [54].

Cocontamination of different types of pollutants often complicates bioremediation, and a recent study has investigated the effect of heavy metal cocontamination with hydrocarbon degradation in hypersaline systems [55]. Strains of both Archaea (a strain of Haloferax elongans and a Halobacterium salinarum) and Bacteria (a strain each of Arhodomonas, Marinobacter, and Halomonas) were inhibited with elevated levels of Hg, Pb, Cu, Cd, and As and were more sensitive to these metals in the presence of crude oil [55]. Overall, the archaeal strains had less tolerance for heavy metals than three halophilic/halotolerant Bacteria tested, though the bacterial genus Kocuria had similar levels of sensitivity to heavy metal toxicity [55]. For the Haloferax elongans, Fe^III amendment lessened the toxicity of Hg, Pb, Cu, and Cd, while for the Halobacterium salinarum, Fe^III amendment lessened the toxicity of Cu, Cd, and As and proline lessened the toxicity limit of Cd [55]. For the Halobacterium salinarum, the rate of crude oil consumption was tested under heavy metal stress with and without Fe^III or proline amendment. The crude oil degradation rate increased significantly under Hg or Pb stresses with Fe^III or proline amendment, while the enhancement of oil consumption rates in Cu-, Cd-, and As-stressed cultures were more nuanced [55]. At low-salt concentrations (<1.5 M), many of these heavy metals, to a certain concentration, increased cell growth presumably from affecting cytoplasmic osmolality [55]. In previous research, the strain Haloferax sp. st. BBK2 was affected by 0.5 mM concentrations of Cd but was resistant to Cd toxicity up to 4 mM levels and it accumulated Cd intracellularly [56].

The progress within this area from simple discovery to in-depth biostimulation analysis over the last decade is tremendous despite the relatively few investigators that have been steadily producing significant findings in this area. The diversity of strains and isolates within the haloarchaea is large, but not exhaustive [41, 57]. The study of haloarchaea benefits from moderate growth rates (doubling times of ~24–32 hr), fruitful isolation attempts, and easy culturing conditions (aerobic, diverse organic substrates, etc.) [14–17]; however, more molecular-based research to monitor and detect in situ degradation is needed to better understand these archaeal biodegradation processes in contaminated hypersaline environments. Though they have relatively warm temperature preferences (generally greater than 30°C) and have vitamin needs [14–17, 32, 49], the broad distribution of haloarchaea in hypersaline environments, the broad metabolic capabilities found on xenobiotics and crude oil, and the relatively quick degradation rates all provide promise that if properly stimulated, bioremediation of hydrocarbons in hypersaline environments should proceed quickly.

3. Degradation of Organics with Thermophilic Sulfolobus solfataricus

A few strains of thermophilic and acidophilic Archaea have been found capable of pollutant degradation. Such biodegradation capabilities are of interest, as many industrial wastewater streams are hot. Genomic sequencing of Sulfolobus solfataricus st. P2 found genes for aromatic degradation and it was found to be able to degrade phenol aerobically through meta-ring cleavage [58]. A strain of the closely related thermophilic Sulfolobus solfataricus st. 98/2 was later found to be able to degrade phenol at 80°C and 3.2 pH [59, 60] through meta-ring cleavage also [61]. A dienelactone hydrolase from Sulfolobus solfataricus st. P1 was also identified and characterized [62]. This enzyme is important for chloroaromatic degradation, such as 2,4-dichlorophenoxyacetic acid [63], though direct testing of this enzyme on chloroaromatics was not reported. To our findings, this seems to be the extent of current research on Sulfolobus in terms of bioremediation applications, but a review of Sulfolobus in broader biotechnology applications has recently been published [64]. This research field is still developing and there are likely more thermophilic hydrocarbon degraders; however, culturing thermophilic strains is difficult due to maintaining high temperatures for cellular growth, the increased volatility of the hydrocarbons at high temperatures, and for aerobes, the low oxygen solubility at high temperatures.

4. Degradation of Hydrocarbons in Soils with Archaea

In nonextreme environments, Bacteria are better known to perform the degradation of hydrocarbons; however, Archaea, particularly the methanogens, are often a component of the degradation process. Hydrogenotrophic and acetoclastic methanogens convert hydrogen and acetate, respectively, to methane gas in anaerobic conditions [65]. In degradative processes where hydrogen or acetate are waste products, these methanogens can thus increase the thermodynamic favorability by reducing hydrogen and acetate concentrations and in effect drive the degradative process forward [66]. This forms a syntrophic relationship between Bacteria that degrades the compound of interest and the methanogenic Archaea that removes the waste products of that degradation [67]. Acetoclastic methanogens are found in the order Methanosarcinales, notably the genera Methanosaeta and Methanosarcina, while hydrogenotrophic methanogens are found in the orders Methanococcales, Methanobacteriales, Methanosarcinales, Methanomicrobiales, Methanopyrales, and Methanocellales [68]. Here, we review the key roles of Archaea in soils and freshwater systems contaminated with hydrocarbons. A recent review was published that more broadly covers microbial community responses to petroleum contamination [69].

Two decades ago, an analysis of the microbial communities in a jet fuel and chlorinated solvent-contaminated aquifer found that Methanosaeta spp. dominated the archaeal community and it was proposed that it performs the terminal step in hydrocarbon degradation in methanogenic zones [70]. Soon thereafter, enrichment cultures showed that long-chain alkanes can be degraded anaerobically to methane with a culture of Syntrophus spp. (including one closely related to a sequence recovered from the jet fuel/chlorinated solvent-contaminated aquifer in [69]) and both acetoclastic (Methanosaeta sp.) and hydrogenotrophic (Methanoculleus sp. and Methanospirillum sp.) methanogens [71]. Since then, many field studies with in situ hydrocarbon degradation have investigated for the presence of methanogenic Archaea. Soil contaminated with petroleum and undergoing remediation was found enriched significantly for Methanosarcinales strains with a denaturing gradient gel electrophoresis (DGGE) method [72]. Methanomicrobiales, Methanosarcinales, Methanobacteriales, and Thermoplasmatales were all found in other soil samples contaminated with petroleum hydrocarbons [73]. High abundances of Methanosaeta were observed in a diesel-contaminated soil—up to 30% of all 16S rRNA genes in some of the samples [74]. This compares to normal abundances of 2% Archaea in natural soils, which are also typically dominated by Crenarchaeota and not the Euryarchaeota of which the methanogens belong [75]. Processed oil sands were also found to contain archaeal communities dominated by the acetoclastic Methanosaeta spp. [76]. A coculture of Anaerolineae and Methanosaeta was found to predominate in an alkane degradation culture over 1300 days with similar 16S rRNA gene concentrations of each, presumably with Anaerolineae breaking down alkane chains through acetate and Methanosaeta fermenting acetate into methane [77]. Another study found that the genus Methanoculleus was the more abundant methanogen in an anaerobic alkane degrading culture containing the bacteria Thermodesulfovibrio and Anaerolineaceae [78].

Often, the diversity of Archaea detected in hydrocarbon degrading cultures is low but the diversity of Archaea in one heavy crude oil-contaminated soil was found to be higher than the diversity of Archaea in a pristine soil [79]. Clone libraries indicated that the contaminated soil contained many members of deeply branching Methanomicrobiales, Halobacteriales, Methanosarcinales, and many Euryarchaeota and Crenarchaeota of uncultured genera, while the pristine soil only contained Natronomonas-like sequences among the Archaea [79]. In a hydrocarbon-contaminated sludge from an oil storage facility, β-Proteobacteria was found in coculture with a diverse archaeal community consisting of Thermoprotei (54%), Methanocellales (33%), and then Methanosarcinales/Methanosaetacaea (8%) [80].

The study of syntrophic hydrocarbon degradation has advanced to studying systems under biostimulation conditions. The anaerobic degradation of benzene is oftentimes slow or nonexistent [4]. In a field-based study comparing the natural attenuation of B20 biodiesel blend and a biostimulation with an ammonium acetate injection, it was found that Archaea populations significantly increased from less than 10³ to 3.7 × 10⁸ 16S rRNA genes·g⁻¹ under the biostimulation conditions commensurately with enhanced BTEX degradation [81]. Conversely, in a recent study of an Alpine Petroleum-contaminated site, the archaeal community was mostly found unchanged on the phyla level (based on read depth analysis of a 16S rRNA gene amplification) and overall archaeal abundance (measured with qPCR) decreased during fertilization biostimulation or increased temperature [82]. The only archaeal enrichment appeared to be Woesearchaeota which became more abundant compared to other archaeal phyla with a temperature increase to 20°C [82]. This study did not report data on finer phylogenetic scales.

The syntrophic relationship between hydrocarbon-degrading Bacteria and methanogenic Archaea is not always present in degradation cultures. Euryarchaeota and Thaumarchaeota completely disappeared in one set of microcosms amended with spent motor oil [83]. Similarly, Illumina sequencing of a 16S rRNA gene amplification did not widely detect Archaea in one petroleum enrichment culture [84]. A GeoChip analysis of the archaeal community in a different study found that archaeal abundance was negatively impacted by oil contamination in an aerobic soil with numbers reduced to 10% of the archaeal abundance in noncontaminated soil [85]. A DGGE-based community profile of an Antarctic soil contaminated with diesel under various remediation conditions found no substantial differences in the archaeal community during bioremediation [86]. Another study found that Archaea were scarce (<1% of the population) in an aquifer above a coal-tar DNAPL with only a low abundance of methanogens [87]. Other than the reduced redox conditions required for methanogenesis, it is not clear why Archaea respond strongly to oil contamination in certain environments and not others.

A diverse and varying dominance of archaeal members (as well as bacterial members) exists in soils and groundwater during hydrocarbon bioremediation. Controlled experiments in which physicochemical conditions (such as redox, salinity, temperature, and trace element availability) are varied in hydrocarbon-contaminated soils may help determine the role that these factors play in selecting the specific archaeal communities (if any at all) that are stimulated. The research in this area also uses a variety of methodologies to study the Archaea, and similar methodologies (clone libraries) still often use different primer sets. Studies in which these methodologies are compared for the same sample would help elucidate the extent that the varying results above are a function of the chosen methodology.

5. Archaea in the Degradation of Oil in Oceans and Marine Sediments

The role of Archaea in the degradation of oil in marine systems is oftentimes unclear as well. It is believed that Bacteria play the dominant role in oil biodegradation in oceans [88], but the role of Archaea in oil degradation in oceans is not fully understood. Archaea in many studies have been found to be sensitive to oil compounds. In a lab-based study of beach sediment microcosms, Archaea 16S rRNA genes became difficult to amplify with a PCR method after incubation with oil, suggesting a large decrease in archaeal populations [89]. That study however only detected two tight clusters of Archaea in its analysis, a group of Marine Group II Euryarchaeota and a group of Crenarchaeota [89]. A later study found that the nitrifying Nitrosopumilus maritimus, a member of the Marine Group I Archaea, was also very sensitive to crude oil presence [90]. In another study, the oil degrading bacteria that were found to grow were heavily dependent on temperature but the archaeal community structure was minimally affected [91]. The study also observed few Archaea groups—predominately a tight phylogenetic group of Marine Group II Archaea and eight other OTUs related to Euryarchaeota and Thaumarchaeota [91]. The isolation of hydrocarbon-degrading strains in coastal sediment contaminated with petroleum off of the coast of Sicily (Italy) recovered only isolates from the domain Bacteria [92]. The natural diversity of archaeal communities were determined with DGGE and was found to consist of uncultured Crenarchaeota and Thaumarchaeota which did not significantly change in crude oil-amended microcosms [92]. Though members of Thaumarchaeota are hypothesized to be able to aerobically degrade crude oil [93], no direct evidence with cultured strains yet exists.

Other studies have detected shifts in archaeal communities that suggest that some Archaea may at times play a role in degradation. One study tested the change in the archaeal community before and after adding either heptadecane, naphthalene, or crude oil in seawater and marine sediment at two locations near Rio de Janeiro (Brazil) [94]. While no Archaea could be identified in the water samples, the archaeal community in the marine sediment uniquely changed for each of the hydrocarbons that were added [94]. The method detected primarily uncultured Archaea, which were mostly Euryarchaeota [94]. In a field study, a DGGE analysis of archaeal 16S rRNA genes indicated that oil contamination in mangrove sediments differed compared to a pristine site [95]; again, the method predominately detected uncultured groups of Archaea. In a recent survey of Atlantic and Mediterranean coastal sediments around Europe, the presence and abundance of the Miscellaneous Crenarchaeotic Group (MCG) were also found to correlate to oil-contaminated sediments [96]. These findings suggest that some uncultured groups of Archaea may have roles in oil degradation in marine systems.

Methanogens have been connected to hydrocarbon degradation in some marine systems as well. Methanogenesis increased commensurately with hydrocarbon degradation in microcosms seeded with contaminated sediments taken from Halic Bay (Turkey) and stimulated with phosphorus and/or nitrogen [97]. A research study also found that adding methanol or acetate could stimulate degradation of petroleum hydrocarbons in marine sediment [98]. The acetoclastic methanogenic Methanosarcinales increased in the sediment with acetate stimulation and temporarily with methanol stimulation [98]. Methanomicrobiales, which are hydrogenotrophic methanogens, increased with methanol stimulation as well, but not with acetate stimulation [98].

Though haloarchaea contain many strains that require high levels of NaCl, recent evidence suggests that marine systems have phylogenetically related strains as well. Samples taken from the Amazon equatorial ocean basin and amended with oil droplets had significant variation in the community composition of the Archaea domain upon oil biodegradation as detected with metagenomic techniques, including a relative enrichment of the Halobacteriaceae [99]. In a mesocosm study of archaeal and bacterial diversity from oil contamination in mangrove sediments, bacterial diversity was more significantly affected from oil contamination than archaeal diversity [100]. The genus Nitrosopumilus, common in marine systems, was inhibited with oil degradation, but the read depth for the family Halobacteriaceae was stimulated from combined oil and nitrate additions, of which members related to Haloferax increased marginally with oil additions [100]. Archaea was not found to be affected by oil contamination in the coastal water of the Gulf of Finland, but they were impacted in the coastal sediments [101]. The Halobacteriaceae was significantly more abundant where the sediment was contaminated with oil [101]. Archaeal cytochrome 450 and retinol metabolism pathways were enhanced where oil was also present which signifies active oil degradation [101]. Altogether, these results indicate that some haloarchaea likely have roles in oil biodegradation at least in sediments. Degradation of oils in sediments is important, as coastal systems are oftentimes more contaminated with oil than open oceans.

In many of the studies above, a limited diversity of Archaea was measured, typically with methods relying on a PCR amplification with universal primers followed by an analysis. Interpreting results from these studies should be done cautiously because amplification-dependent methodologies may miss clades of Archaea due to primer mismatching and/or PCR biases [102]. With modern metagenomic sequences, it may be worthwhile to reexamine old assumptions based on these results. Indeed, recent metagenomic-based methods are elucidating much greater diversity of Archaea in marine systems than the earlier studies using methods dependent on PCR amplification were detecting (i.e., [99]).

6. Archaea in Heavy Metal Remediation

Bioremediation of metals can take many forms [103]. Oftentimes, it involves the redox cycling of the metals for the conversion of toxic redox states to nontoxic redox states. Alternatively, redox cycling may convert soluble metal redox states to insoluble redox states, or vice versa, and the effect of which is precipitation or mobilization of the metal. Additionally, metals may be removed through reactions that permit volatilization of heavy metals or through sorption into biomass. These processes are also important for radioactive metals [104], but Archaea are poorly studied in this area despite some archaeal strains having high tolerance of radioactivity [105]. A recent review over the bioremediation of heavy metals was published, but did not address Archaea [106]. A comprehensive review of metal-tolerant thermophiles has been published recently including significant information regarding Archaea and the significant context in terms of bioremediation [107]; thus, here, we do not cover thermophiles and metal bioremediation in as much detail.

Arsenite (As^III) is a toxic form of arsenic, but it can be oxidized to less toxic arsenate (As^V). In a study of an acidic, sulfuric thermal spring in Yellowstone National Park (USA), arsenite oxidation coincided with the appearance of unisolated Crenarchaeota and Euryarchaeota and it was thus hypothesized that Archaea could oxidize arsenite [108]. In earlier work, the Sulfolobus acidocaldarius st. BC was indeed confirmed to oxidize arsenite to arsenate [109]. From reviews of the deposited genomic sequences in GenBank, the Archaea strains Aeropyrum pernix st. K1, Pyrobaculum calidifontis st. JCM 11548, and Sulfolobus tokodaii st. 7 are found to contain arsenite oxidase genes [110, 111]. A recent metagenomic study of Diamante Lake (Argentina) found a large abundance of arsenate reduction and arsenite oxidation genes and haloarchaea [112]. Fourteen isolates of the genus Halorubrum were found to contain arsenite oxidation genes and one strain was confirmed capable of arsenite oxidation [112]. Arsenate reduction by Archaea is also common which in turn would increase arsenic toxicity (i.e., [113]).

Mercuric mercury (Hg^II) is highly toxic and one method of removal is via biological reduction to volatile zero-valent mercury (Hg⁰). This is carried about by enzymes encoded by mercury reductase genes which have been identified in several diverse Crenarchaeota and Euryarchaeota [114]. A study of a mercury-containing hot spring in Yellowstone National Park (USA) found novel and deeply rooted mercury reductase genes associated with Archaea [115]. Mercury reductase was found upregulated in Sulfolobus solfataricus and was needed for mercury resistance [116], and mercury volatilization was also measured from Halococcus, Halobacterium, and, to a lesser extent, Haloferax [117]. Direct study of zero-valent mercury volatilization from Archaea is otherwise rather scarce. Conversely, mercury methylation by methanogens, which increases toxicity, is well documented [118].

The precipitation of uranium by the reduction of U^VI to U^IV is one mechanism for the immobilization of uranium in environments where it may impact ground and surface waters [119]. Pyrobaculum sp., which are hyperthermophiles, are capable of uranium reduction [120]. These Archaea have large redox capabilities for other metals (i.e., [121]) and thus may be beneficial in many types of metal-contaminated hyperthermic waste streams.

Another way in which metals may be bioremediated is via intracellular or extracellular binding or sorption. Methanobacterium bryantii was found to excrete extracellular proteins to chelate copper [122]. Sulfolobus acidocaldarius was found to bind U^VI into organophosphate groups [123]. Halophilic microbes are often able to absorb heavy metals, as well [124]. Halobacterium sp. GUSF was found to be able to absorb manganese at high rates and high concentrations [125]. Halobacterium noricense was found to adsorb cadmium [126]. As noted above, Haloferax st. BBK2 was found to accumulate cadmium intracellularly [56]. The archaeon Halobacterium noricense DSM15987 was found to accumulate U^IV with phosphoryl and carboxylate groups compared to a direct biosorption process with the bacterium Brachybacterium sp. G1 [127, 128]. These results show promise that the haloarchaea can be used in the treatment of hypersaline environments and wastewaters for heavy metal removals.

7. Archaea in Acid Mine Drainage

Acid mine drainage is a major contributor to water pollution by introducing a highly acidic effluent with toxic metals in solution. Acid mine drainage occurs when oxygen, introduced due to mining activities, reacts with metal sulfide minerals (such as FeS₂) resulting in the production of sulfuric acid and lower pH; this reaction is often aided by aerobic iron- and sulfur-oxidizing microbes [129]. Many microorganisms including many Archaea tolerate and thrive in the acidic and metal dense environments found in acid mine drainage. Ferroplasma spp. are acidophilic metal oxidizers with preferences of very low pH (<1.5) and are major players in the production of acid mine drainage and the biogeochemical cycling of sulfur [130, 131]. At Iron Mountain (CA) which has acid mine drainage, Archaea are the major proportion of the prokaryotes and Ferroplasma dominates (85% of Archaea) [130]. Many other Archaea are involved in similar ways. For example, Sulfolobusmetallicus, which is also acidophilic, thermophilic, and chemolithoautotrophic, can oxidize elemental sulfur and sulfidic ores, producing sulfuric acid and causing the leaching of uranium, zinc, and copper [132]. Exploiting these Archaea may be important for mining of metals and biocatalysis under extreme conditions (i.e., [133]) but may not be helpful in an acid mine bioremediation context where increased toxic metal mobility and acidification is typically not a favorable outcome. However, the diversity of the Archaea in the order Thermoplasmatales and their resistance to toxic metal resistance [134] may prove useful for other metal remediation purposes.

The biological treatment applying sulfate-reducing bacteria is an attractive option to treat acid mine drainage and to recover metals [135]. The process produces alkalinity, neutralizing the acid mine drainage simultaneously. There are two lineages of archaeal sulfate reducers: the Archaeoglobus, within the Euryarchaeota, and Thermocladium and Caldivirga within the Crenarchaeota [136]. Archaeoglobus are thermophilic but not acidophilic [137]. Thermocladium and Caldivirga are moderately acidophilic and can tolerate pH down to about 2.3 but are still thermophilic and thus are not suitable for acid mine drainage [138, 139].

8. Archaea in Reductive Dehalogenation

Reductive dehalogenation removes halides from organic compounds resulting in lower halogenated or nonhalogenated products and is important in bioremediation. This field has been largely focused on the organohalide-respiring Bacteria that can use organohalides as terminal electron acceptors. However, the ability of methanogens to dehalogenate has been long established. Many papers were published in the 1980s and 1990s discovering the various substrates subject to dechlorination by methanogens. Various strains of Methanosarcina were found to dehalogenate pentachlorophenol [140], perchloroethylene [141], trichloroethene [142], chloroform [143], and trichlorofluoromethane [144]. Methanobacterium ivanovii strain T1N was able to degrade pentachlorophenol [140]. Cell suspensions of Methanosarcina barkeri (DSM 2948), Methanosarcina mazei (DSM 2053) (which was incorrectly referred to as Methanococcus mazei despite reclassification 8 years prior [145]), Methanobacterium thermoautotrophicum st. Marburg (DSM 2133) (which has since been reclassified as Methanothermobacter marburgensis [146]), and Methanothrix soehngenii (DSM 2139) dechlorinate 1,2-dichloroethane through dihaloelimination to the product ethylene and through hydrogenolysis to chloroethane [147]. The ability to dehalogenate is likely from the high concentrations of corrinoids, such as cobalamin, in methanogens which are needed for methanogenesis [148, 149]. Corrinoids are able to dehalogenate organics abiotically [150, 151].

Archaea are also commonly reported as a part of microbial communities dechlorinating chloroethenes (Table 2). Methanobacterium congolense was found in the well-studied chloroethene-dechlorinating ANAS culture [152]. Inhibition of the methanogens with 2-bromoethanesulphonate (BES) was reported to not affect the “ability to dechlorinate trichloroethene completely”; however, further information was not provided [152]. Methanothrix, Methanomethylovorans, and an unclassified Archaea were present in a column treating perchloroethene [153]. At a site undergoing remediation from trichloroethene to ethene, Methanosaeta sp., Methanospirillum sp., Methanosarcina, and an unclassified Methanomicrobiales were found present [154]. Methanosarcina, Methanomethylovorans, Methanomicrobiales, and Methanosaeta were reported as significant components of the well-studied and highly enriched KB-1 organochloride-dechlorinating culture [155]. Methanosarcina was found to be important for the dechlorination of vinyl chloride in an enriched Dehalococcoides-containing culture, while Methanosaeta had no impact [156]. It was hypothesized that the Methanosarcina were producing H₂ from acetate oxidation for the Dehalococcoides in these cultures [156]. Hydrogenotrophic methanogens in other cultures are conversely likely competing for H₂ substrate with the organohalide-respiring bacteria [157, 158]. Many dechlorinators, such as the versatile Dehalococcoides, lack the ability to synthesize needed corrinoids for reductive dehalogenation and instead have genes for corrinoid scavenging and import [159, 160]. Methanogens in these cultures may provide these key corrinoids for the organohalide-respiring bacteria in these communities, though this role may be fulfilled by other corrinoid-producing bacteria [158]. A recent review on cobalamin synthesis in the context of dehalogenation has been published [161]. The ability of methanogens to dechlorinate suggests that these Archaea may contribute to dechlorination activities even in systems dominated by organohalide respirers. The roles and antagonism of Archaea in reductive dechlorination systems are likely complex. Recent research has started investigating the natural cycling of organohalides but has only thus far focused on Bacteria [162–164].

9. Research Needs

A primary hurdle in the study of Archaea in bioremediation systems is methodological. Many studies on bioremediation do not study archaeal community members explicitly nor have methods that would allow for the discovery of archaeal diversity or activities. Additionally, many methodologies that have been used to study Archaea are prone to biases, which may cloud our understanding. A varied number of archaeal and “universal” amplification primer pairs are known and are used to study archaeal diversity [32, 37, 82, 83, 86]. Interpreting results from these methods should be done carefully. PCR amplifications of entire prokaryotes or entire domains are prone to biases, which can underrepresent and overrepresent various microbial community members [102]. Analyses that are based on a high phylogenetic level (i.e., phylum-based analyses) can also hide trends on the finer phylogenetic levels (i.e., genus). Recent publications above often rely on “relative read depth” analysis of the high throughput sequencing of a 16S rRNA gene amplification product to provide quantitative measurement of specific Archaea taxonomic groups; however, these methods are still exposed to PCR biases. For analysis of mixed cultures, metagenomic sequencing of unamplified DNA and more quantitative PCR (qPCR) methods should also be used. QPCR has a high sensitivity, can be designed for high specificity, and can be quality controlled [165] and thus makes a superior quantitative method to “relative read depth” analysis which lacks these characteristics. In a recent publication, read depth analysis from an Illumina-sequenced PCR product was able to identify enriched taxonomic groups, but the read depth analysis agreed poorly with the actual quantification with qPCR [164]. Some qPCR methods have been developed for certain Archaea (i.e., [155]); however, more methods need to be developed to further extend the study of Archaea in mixed microbial communities.

An additional hurdle in studying Archaea in bioremediation again is methodological. Dose growth response analysis is often used to measure community members that outcompete others at a given physicochemical condition on a given substrate. One hypothesis of Archaea evolution suggests that Archaea’s niche and advantage in the environment is operating under energy stress, and thus, dose growth response methods provide conditions where Archaea may easily be outcompeted [166]. In the environment, biodegradation activity often occurs in heterogeneous environments with microniches, energy stresses, and complex microbial communities where Archaea are thus theoretically more heavily involved than what will be found using many traditional microcosm/enrichment culture methodologies.

Though this field has made significant advances in the last several years, it is still developing and all forms of research will continue to advance the field. The potential of Archaea to serve in bioremediation applications (outside of hypersaline environments) is not well understood. The extremophilic nature of many Archaea make them uniquely suitable for biodegradation of “extreme” environments and waste streams, yet many of these possibilities are not yet tested. Future research in bioremediation should be conscious of the potential roles of Archaea in bioremediation processes, and thus, methods should be more routinely used to analyze the Archaea.

Conflicts of Interest

The authors declare that they have no conflict of interest.

Acknowledgments

This work was supported by the National Science Foundation (CBET 1511767).

References

J. T. Cookson Jr, Bioremediation Engineering: Design and Applications, McGraw-Hill Education, 1st edition, 1994.
O. Lefebvre and R. Moletta, “Treatment of organic pollution in industrial saline wastewater: a literature review,” Water Research, vol. 40, no. 20, pp. 3671–3682, 2006.
View at: Publisher Site | Google Scholar
S. Le Borgne, D. Paniagua, and R. Vazquez-Duhalt, “Biodegradation of organic pollutants by halophilic Bacteria and Archaea,” Journal of Molecular Microbiology and Biotechnology, vol. 15, no. 2-3, pp. 74–92, 2008.
View at: Publisher Site | Google Scholar
B. Z. Fathepure, “Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments,” Frontiers in Microbiology, vol. 5, article 173, 2014.
View at: Publisher Site | Google Scholar
L. C. Castillo-Carvajal, J. L. Sanz-Martín, and B. E. Barragán-Huerta, “Biodegradation of organic pollutants in saline wastewater by halophilic microorganisms: a review,” Environmental Science and Pollution Research, vol. 21, no. 16, pp. 9578–9588, 2014.
View at: Publisher Site | Google Scholar
M. A. Amoozegar, M. Siroosi, S. Atashgahi, H. Smidt, and A. Ventosa, “Systematics of haloarchaea and biotechnological potential of their hydrolytic enzymes,” Microbiology, vol. 163, no. 5, pp. 623–645, 2017.
View at: Publisher Site | Google Scholar
A. Oren, “Halophilic microbial communities and their environments,” Current Opinion in Biotechnology, vol. 33, pp. 119–124, 2015.
View at: Publisher Site | Google Scholar
D. K. Maheshwari and M. Saraf, Halophiles: Biodiversity and Sustainable Exploitation, Volume 6 in the Sustainable Development and Biodiversity Series, K. G. Ramawat, Ed., Springer, 2015.
M. J. Bonete, V. Bautista, J. Esclapez et al., “New uses of Haloarchaeal species in bioremediation processes,” in Advances in Bioremediation of Wastewater and Polluted Soil, InTech, 2015.
View at: Publisher Site | Google Scholar
S. Aracil-Gisbert, J. Torregrosa-Crespo, and R. M. Martínez-Espinosa, “Recent trend on bioremediation of polluted salty soils and waters using Haloarchaea,” in Advances in Bioremediation and Phytoremediation, Chapter 4, pp. 63–77, InTech, 2018.
View at: Publisher Site | Google Scholar
A. Loukas, I. Kappas, and T. J. Abatzopoulos, “HaloDom: a new database of halophiles across all life domains,” Journal of Biological Research-Thessaloniki, vol. 25, no. 1, p. 2, 2018.
View at: Publisher Site | Google Scholar
S. Kleinsteuber, V. Riis, I. Fetzer, H. Harms, and S. Müller, “Population dynamics within a microbial consortium during growth on diesel fuel in saline environments,” Applied and Environmental Microbiology, vol. 72, no. 5, pp. 3531–3542, 2006.
View at: Publisher Site | Google Scholar
M. T. García, E. Mellado, J. C. Ostos, and A. Ventosa, “Halomonas organivorans sp. nov., a moderate halophile able to degrade aromatic compounds,” International Journal of Systematic and Evolutionary Microbiology, vol. 54, no. 5, pp. 1723–1728, 2004.
View at: Publisher Site | Google Scholar
J. C. Bertrand, M. Almallah, M. Acquaviva, and G. Mille, “Biodegradation of hydrocarbons by an extremely halophilic archaebacterium,” Letters in Applied Microbiology, vol. 11, no. 5, pp. 260–263, 1990.
View at: Publisher Site | Google Scholar
E. B. M. Denner, T. J. McGenity, J.-J. Busse, W. D. Grant, G. Wanner, and H. Stan-Lotter, “Halococcus salifodinae sp. nov., an archaeal isolate from an Austrian salt mine,” International Journal of Systematic and Evolutionary Microbiology, vol. 44, no. 4, pp. 774–780, 1994.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, N. A. Sorkhoh, H. Al-Awadhi, M. Eliyas, and S. S. Radwan, “Biodegradation of crude oil and pure hydrocarbons by extreme halophilic archaea from hypersaline coasts of the Arabian Gulf,” Extremophiles, vol. 14, no. 3, pp. 321–328, 2010.
View at: Publisher Site | Google Scholar
J.-Y. Ding, S.-C. Chen, M.-C. Lai, and T.-L. Liao, “Haloterrigena mahii sp. nov., an extremely halophilic archaeon from a solar saltern,” International Journal of Systematic and Evolutionary Microbiology, vol. 67, no. 5, pp. 1333–1338, 2017.
View at: Publisher Site | Google Scholar
Y. H. Tapilatu, V. Grossi, M. Acquaviva, C. Militon, J.-C. Bertrand, and P. Cuny, “Isolation of hydrocarbon-degrading extremely halophilic archaea from an uncontaminated hypersaline pond (Camargue, France),” Extremophiles, vol. 14, no. 2, pp. 225–231, 2010.
View at: Publisher Site | Google Scholar
I. S. Kulichevskaya, E. I. Milekhina, I. A. Borzenkov, I. S. Zvyagintseva, and S. S. Belyaev, “Oxidation of petroleum hydrocarbons by extremely halophilic archeobacteria,” Mikrobiologiya, vol. 60, no. 5, pp. 596–601, 1991.
View at: Google Scholar
D. Emerson, S. Chauhan, P. Oriel, and J. A. Breznak, “Haloferax sp. D1227, a halophilic Archaeon capable of growth on aromatic compounds,” Archives of Microbiology, vol. 161, no. 6, pp. 445–452, 1994.
View at: Publisher Site | Google Scholar
W. Fu and P. Oriel, “Degradation of 3-phenylpropionic acid by Haloferax sp. D1227,” Extremophiles, vol. 3, no. 1, pp. 45–53, 1999.
View at: Publisher Site | Google Scholar
I. Zvyagintseva, S. Belyaev, I. Borzenkov, N. Kostrikina, E. Milekhina, and M. Ivanov, “Halophilic archaebacteria from the Kalamkass oil field,” Mikrobiologiya, vol. 64, no. 1, pp. 83–87, 1995.
View at: Google Scholar
D. J. Fairley, D. R. Boyd, N. D. Sharma, C. C. R. Allen, P. Morgan, and M. J. Larkin, “Aerobic metabolism of 4-hydroxybenzoic acid in Archaea via an unusual pathway involving an intramolecular migration (NIH shift),” Applied and Environmental Microbiology, vol. 68, no. 12, pp. 6246–6255, 2002.
View at: Publisher Site | Google Scholar
D. J. Fairley, G. Wang, C. Rensing, I. L. Pepper, and M. J. Larkin, “Expression of gentisate 1, 2-dioxygenase (gdoA) genes involved in aromatic degradation in two haloarchaeal genera,” Applied Microbiology and Biotechnology, vol. 73, no. 3, pp. 691–695, 2006.
View at: Publisher Site | Google Scholar
W. Fu and P. Oriel, “Gentisate 1,2-dioxygenase from Haloferax sp. D1227,” Extremophiles, vol. 2, no. 4, pp. 439–446, 1998.
View at: Publisher Site | Google Scholar
B. Ozcan, G. Ozcengiz, A. Coleri, and C. Cokmus, “Diversity of halophilic Archaea from six hypersaline environments in Turkey,” Journal of Microbiology and Biotechnology, vol. 17, no. 6, pp. 985–992, 2007.
View at: Google Scholar
S. Mazguene, M. Rossi, M. Gogliettino et al., “Isolation and characterization from solar salterns of North Algeria of a haloarchaeon producing a new halocin,” Extremophiles, vol. 22, no. 2, pp. 259–270, 2018.
View at: Publisher Site | Google Scholar
L. G. Wayne, H. C. Engbaek, H. W. B. Engel et al., “Highly reproducible techniques for use in systematic bacteriology in the genus Mycobacterium: tests for pigment, urease, resistance to sodium chloride, hydrolysis of Tween 80, and β-galactosidase,” International Journal of Systematic and Evolutionary Microbiology, vol. 24, no. 4, pp. 412–419, 1974.
View at: Publisher Site | Google Scholar
J. D. Rogers, T. L. Burke, S. G. Osborn, and J. N. Ryan, “A framework for identifying organic compounds of concern in hydraulic fracturing fluids based on their mobility and persistence in groundwater,” Environmental Science and Technology Letters, vol. 2, no. 6, pp. 158–164, 2015.
View at: Publisher Site | Google Scholar
E. Nyankson, D. Rodene, and R. B. Gupta, “Advancements in crude oil spill remediation research after the Deepwater Horizon oil spill,” Water, Air, and Soil Pollution, vol. 227, no. 1, p. 29, 2016.
View at: Publisher Site | Google Scholar
I. Djeridi, C. Militon, V. Grossi, and P. Cuny, “Evidence for surfactant production by the haloarchaeon Haloferax sp. MSNC14 in hydrocarbon-containing media,” Extremophiles, vol. 17, no. 4, pp. 669–675, 2013.
View at: Publisher Site | Google Scholar
M. R. L. Bonfá, M. J. Grossman, E. Mellado, and L. R. Durrant, “Biodegradation of aromatic hydrocarbons by Haloarchaea and their use for the reduction of the chemical oxygen demand of hypersaline petroleum produced water,” Chemosphere, vol. 84, no. 11, pp. 1671–1676, 2011.
View at: Publisher Site | Google Scholar
M. F. Mullakhanbhai and H. Larsen, “Halobacterium volcanii spec. nov. a Dead Sea halobacterium with a moderate salt requirement,” Archives of Microbiology, vol. 104, no. 1, pp. 207–214, 1975.
View at: Publisher Site | Google Scholar
A. L. Hartman, C. Norais, J. H. Badger et al., “The complete genome sequence of Haloferax volcanii DS2, a model archaeon,” PLoS One, vol. 5, no. 3, article e9605, 2010.
View at: Publisher Site | Google Scholar
J.-Y. Ding and M.-C. Lai, “The biotechnological potential of the extreme halophilic archaea Haloterrigena sp. H13 in xenobiotic metabolism using a comparative genomics approach,” Environmental Toxicology, vol. 31, no. 8-9, pp. 905–914, 2010.
View at: Publisher Site | Google Scholar
S. Cuadros-Orellana, M. Pohlschröder, M. J. Grossman, and L. R. Durrant, “Biodegradation of aromatic compounds by a halophilic archaeon isolated from the dead sea,” Chemical Engineering Transactions, vol. 27, pp. 13–18, 2012.
View at: Google Scholar
S. Khemili-Talbi, S. Kebbouche-Gana, S. Akmoussi-Toumi, Y. Angar, and M. L. Gana, “Isolation of an extremely halophilic arhaeon Natrialba sp. C21 able to degrade aromatic compounds and to produce stable biosurfactant at high salinity,” Extremophiles, vol. 19, no. 6, pp. 1109–1120, 2015.
View at: Publisher Site | Google Scholar
E. Acikgoz and B. Ozcan, “Phenol biodegradation by halophilic archaea,” International Biodeterioration and Biodegradation, vol. 107, pp. 140–146, 2016.
View at: Publisher Site | Google Scholar
S. F. Erdoğmuş, B. Mutlu, S. E. Korcan, K. Güven, and M. Konuk, “Aromatic hydrocarbon degradation by halophilic archaea isolated from Çamaltı Saltern, Turkey,” Water, Air and Soil Pollution, vol. 224, no. 3, article 1449, 2013.
View at: Publisher Site | Google Scholar
S. W. Roh and H. S. Song, “Complete genome sequence of Halorubrum trapanicum CBA1232,” Submission to NCBI GENBANK, 01-Jul-2016, Bioproject PRJDB4921, Accession number AP017569, accessed 02-May-2018.
View at: Google Scholar
S. Dalvi, N. H. Youssef, and B. Z. Fathepure, “Microbial community structure analysis of a benzoate-degrading halophilic archaeal enrichment,” Extremophiles, vol. 20, no. 3, pp. 311–321, 2016.
View at: Publisher Site | Google Scholar
M. S. Elshahed, F. Z. Najar, B. A. Roe, A. Oren, T. A. Dewers, and L. R. Krumholz, “Survey of archaeal diversity reveals an abundance of halophilic Archaea in a low-salt, sulfide- and sulfur-rich spring,” Applied and Environmental Microbiology, vol. 70, no. 4, pp. 2230–2239, 2004.
View at: Publisher Site | Google Scholar
A. K. Borsodi, T. Felföldi, I. Máthé et al., “Phylogenetic diversity of bacterial and archaeal communities inhabiting the saline Lake Red located in Sovata, Romania,” Extremophiles, vol. 17, no. 1, pp. 87–98, 2013.
View at: Publisher Site | Google Scholar
X. Wang, Z. Han, Z. Bai et al., “Archaeal community structure along a gradient of petroleum contamination in saline-alkali soil,” Journal of Environmental Sciences, vol. 23, no. 11, pp. 1858–1864, 2011.
View at: Publisher Site | Google Scholar
W. Sun, J. Li, L. Jiang, Z. Sun, M. Fu, and X. Peng, “Profiling microbial community structures across six large oilfields in China and the potential role of dominant microorganisms in bioremediation,” Applied Microbiology and Biotechnology, vol. 99, no. 20, pp. 8751–8764, 2015.
View at: Publisher Site | Google Scholar
K. Konstantinidis, A. Tebbe, C. Klein et al., “Genome-wide proteomics of Natronomonas pharaonis,” Journal of Proteome Research, vol. 6, no. 1, pp. 185–193, 2007.
View at: Publisher Site | Google Scholar
F. Piubeli, M. J. Grossman, F. Fantinatti-Garboggini, and L. R. Durrant, “Phylogenetic analysis of the microbial community in hypersaline petroleum produced water from the Campos Basin,” Environmental Science and Pollution Research, vol. 21, no. 20, pp. 12006–12016, 2014.
View at: Publisher Site | Google Scholar
F. Piubeli, M. J. Grossman, F. Fantinatti-Garboggini, and L. R. Durrant, “Enhanced reduction of COD and aromatics in petroleum-produced water using indigenous microorganisms and nutrient addition,” International Biodeterioration and Biodegradation, vol. 68, pp. 78–84, 2012.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, M. Eliyas, and S. Radwan, “Enhanced bioremediation of oil-polluted, hypersaline, coastal areas in Kuwait via vitamin-fertilization,” Environmental Science and Pollution Research, vol. 21, no. 5, pp. 3386–3394, 2014.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, M. Eliyas, and S. S. Radwan, “Bioremediation of oily hypersaline soil and water via potassium and magnesium amendment,” Canadian Journal of Microbiology, vol. 59, no. 12, pp. 837–844, 2013.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, M. Eliyas, and S. S. Radwan, “Enhanced haloarchaeal oil removal in hypersaline environments via organic nitrogen fertilization and illumination,” Extremophiles, vol. 16, no. 5, pp. 751–758, 2012.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, M. Eliyas, M. Khanafer, and S. S. Radwan, “Biofilms constructed for the removal of hydrocarbon pollutants from hypersaline liquids,” Extremophiles, vol. 19, no. 1, pp. 189–196, 2015.
View at: Publisher Site | Google Scholar
Y. Y. Corsellis, M. M. Krasovec, L. L. Sylvi, P. P. Cuny, and C. C. Militon, “Oil removal and effects of spilled oil on active microbial communities in close to salt-saturation brines,” Extremophiles, vol. 20, no. 3, pp. 235–250, 2016.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, M. Al-Deieg, M. Eliyas, and S. S. Radwan, “Biostimulation of indigenous microorganisms for bioremediation of oily hypersaline microcosms from the Arabian Gulf Kuwaiti coasts,” Journal of Environmental Management, vol. 193, pp. 576–583, 2017.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, M. Eliyas, and S. S. Radwan, “Ferric sulfate and proline enhance heavy-metal tolerance of halophilic/halotolerant soil microorganisms and their bioremediation potential for spilled-oil under multiple stresses,” Frontiers in Microbiology, vol. 9, article 394, 2018.
View at: Publisher Site | Google Scholar
D. Das, B. B. Salgaonkar, K. Mani, and J. M. Braganca, “Cadmium resistance in extremely halophilic archaeon Haloferax strain BBK2,” Chemosphere, vol. 112, pp. 385–392, 2014.
View at: Publisher Site | Google Scholar
N. H. Youssef, K. N. Ashlock-Savage, and M. S. Elshahed, “Phylogenetic diversities and community structure of members of the extremely halophilic archaea (order Halobacteriales) in multiple saline sediment habitats,” Applied and Environmental Microbiology, vol. 78, no. 5, pp. 1332–1344, 2012.
View at: Publisher Site | Google Scholar
V. Izzo, E. Notomista, A. Picardi, F. Pennacchio, and A. di Donato, “The thermophilic archaeon Sulfolobus solfataricus is able to grow on phenol,” Research in Microbiology, vol. 156, no. 5-6, pp. 677–689, 2005.
View at: Publisher Site | Google Scholar
P. Christen, A. Vega, L. Casalot, G. Simon, and R. Auria, “Kinetics of aerobic phenol biodegradation by the acidophilic and hyperthermophilic archaeon Sulfolobus solfataricus 98/2,” Biochemical Engineering Journal, vol. 62, pp. 56–61, 2012.
View at: Publisher Site | Google Scholar
P. Christen, S. Davidson, Y. Combet-Blanc, and R. Auria, “Phenol biodegradation by the thermoacidophilic archaeon Sulfolobus solfataricus 98/2 in a fed-batch bioreactor,” Biodegradation, vol. 22, no. 3, pp. 475–484, 2011.
View at: Publisher Site | Google Scholar
A. Comte, P. Christen, S. Davidson et al., “Biochemical, transcriptional and translational evidences of the phenol-meta-degradation pathway by the hyperthermophilic Sulfolobus solfataricus 98/2,” PLoS One, vol. 8, no. 12, article e82397, 2013.
View at: Publisher Site | Google Scholar
Y.-J. Park, S.-J. Yoon, and H.-B. Lee, “A novel dienelactone hydrolase from the thermoacidophilic archaeon Sulfolobus solfataricus P1: Purification, characterization, and expression,” Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1800, no. 11, pp. 1164–1172, 2010.
View at: Publisher Site | Google Scholar
A. Kumar, N. Trefault, and A. O. Olaniran, “Microbial degradation of 2,4-dichlorophenoxyacetic acid: insight into the enzymes and catabolic genes involved, their regulation and biotechnological implications,” Critical Reviews in Microbiology, vol. 42, no. 2, pp. 1–15, 2016.
View at: Publisher Site | Google Scholar
J. Quehenberger, L. Shen, S.-V. Albers, B. Siebers, and O. Spadiut, “Sulfolobus-a potential key organism in future biotechnology,” Frontiers in Microbiology, vol. 8, article 2474, 2017.
View at: Publisher Site | Google Scholar
W. B. Whitman, T. L. Bowen, and D. R. Boone, “The methanogenic bacteria,” in The Prokaryotes, vol. 1, A. Balows, H. G. Truper, M. Dworkin, W. Harder, and K. H. Schleifer, Eds., Springer-Verlag, New York, NY, USA, 1992.
View at: Google Scholar
M. J. McInerney, C. G. Struchtemeyer, J. Sieber et al., “Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism,” Annals of the New York Academy of Sciences, vol. 1125, no. 1, pp. 58–72, 2008.
View at: Publisher Site | Google Scholar
B. Tan, X. Dong, C. W. Sensen, and J. Foght, “Metagenomic analysis of an anaerobic alkane-degrading microbial culture: potential hydrocarbon-activating pathways and inferred roles of community members,” Genome, vol. 56, no. 10, pp. 599–611, 2013.
View at: Publisher Site | Google Scholar
F. Enzmann, F. Mayer, M. Rother, and D. Holtmann, “Methanogens: biochemical background and biotechnological applications,” AMB Express, vol. 8, no. 1, p. 1, 2018.
View at: Publisher Site | Google Scholar
A. Mukherjee and D. Chattopadhyay, “Exploring environmental systems and processes through next-generation sequencing technologies: insights into microbial response to petroleum contamination in key environments,” The Nucleus, vol. 60, no. 2, pp. 175–186, 2017.
View at: Publisher Site | Google Scholar
M. A. Dojka, P. Hugenholtz, S. K. Haack, and N. R. Pace, “Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation,” Applied and Environmental Microbiology, vol. 64, no. 10, pp. 3869–3877, 1998.
View at: Google Scholar
K. Zengler, H. H. Richnow, R. Rossello-Mora, W. Michaelis, and F. Widdel, “Methane formation from long-chain alkanes by anaerobic microorganisms,” Nature, vol. 401, no. 6750, pp. 266–269, 1999.
View at: Publisher Site | Google Scholar
Y. Kasai, Y. Takahata, T. Hoaki, and K. Watanabe, “Physiological and molecular characterization of a microbial community established in unsaturated, petroleum-contaminated soil,” Environmental Microbiology, vol. 7, no. 6, pp. 806–818, 2005.
View at: Publisher Site | Google Scholar
D.-C. Zhang, C. Mörtelmaier, and R. Margesin, “Characterization of the bacterial archaeal diversity in hydrocarbon-contaminated soil,” Science of the Total Environment, vol. 421-422, pp. 184–196, 2012.
View at: Publisher Site | Google Scholar
N. B. Sutton, F. Maphosa, J. A. Morillo et al., “Impact of long-term diesel contamination on soil microbial community structure,” Applied and Environmental Microbiology, vol. 79, no. 2, pp. 619–630, 2012.
View at: Publisher Site | Google Scholar
S. T. Bates, D. Berg-Lyons, J. G. Caporaso, W. A. Walters, R. Knight, and N. Fierer, “Examining the global distribution of dominant archaeal populations in soil,” ISME Journal, vol. 5, no. 5, pp. 908–917, 2011.
View at: Publisher Site | Google Scholar
T. J. Penner and J. M. Foght, “Mature fine tailings from oil sands processing harbour diverse methanogenic communities,” Canadian Journal of Microbiology, vol. 56, no. 6, pp. 459–470, 2010.
View at: Publisher Site | Google Scholar
B. Liang, L.-Y. Wang, S. M. Mbadinga et al., “Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation,” AMB Express, vol. 5, no. 1, p. 37, 2015.
View at: Publisher Site | Google Scholar
B. Liang, L.-Y. Wang, Z. Zhou et al., “High frequency of Thermodesulfovibrio spp. and Anaerolineaceae in association with Methanoculleus spp. in a long-term incubation of n-alkanes-degrading methanogenic enrichment culture,” Frontiers in Microbiology, vol. 7, article 1431, 2016.
View at: Publisher Site | Google Scholar
R. Liu, Y. Zhang, R. Ding, D. Li, Y. Gao, and M. Yang, “Comparison of archaeal and bacterial community structures in heavily oil-contaminated and pristine soils,” Journal of Bioscience and Bioengineering, vol. 108, no. 5, pp. 400–407, 2009.
View at: Publisher Site | Google Scholar
R. Das and S. K. Kazy, “Microbial diversity, community composition and metabolic potential in hydrocarbon contaminated oily sludge: prospects for in situ bioremediation,” Environmental Science and Pollution Research, vol. 21, no. 12, pp. 7369–7389, 2014.
View at: Publisher Site | Google Scholar
D. T. Ramos, M. L. B. da Silva, H. S. Chiaranda, P. J. J. Alvarez, and H. X. Corseuil, “Biostimulation of anaerobic BTEX biodegradation under fermentative methanogenic conditions at source-zone groundwater contaminated with a biodiesel blend (B20),” Biodegradation, vol. 24, no. 3, pp. 333–341, 2013.
View at: Publisher Site | Google Scholar
J. A. Siles and R. Margesin, “Insights into microbial communities mediating the bioremediation of hydrocarbon-contaminated soil from an Alpine former military site,” Applied Microbiology and Biotechnology, vol. 102, no. 10, pp. 4409–4421, 2018.
View at: Publisher Site | Google Scholar
L. B. Salam, S. O. Obayori, F. O. Nwaokorie, A. Suleiman, and R. Mustapha, “Metagenomic insights into effects of spent engine oil perturbation on the microbial community composition and function in a tropical agricultural soil,” Environmental Science and Pollution Research, vol. 24, no. 8, pp. 7139–7159, 2017.
View at: Publisher Site | Google Scholar
S. Fuentes, B. Barra, J. G. Caporaso, and M. Seeger, “From rare to dominant: a fine-tuned soil bacterial bloom during petroleum hydrocarbon bioremediation,” Applied and Environmental Microbiology, vol. 82, no. 3, pp. 888–896, 2016.
View at: Publisher Site | Google Scholar
Y. Liang, G. Li, J. D. van Nostrand et al., “Microarray-based analysis of microbial functional diversity along an oil contamination gradient in oil field,” FEMS Microbiology Ecology, vol. 70, no. 2, pp. 324–333, 2009.
View at: Publisher Site | Google Scholar
H. E. de Jesus, R. S. Peixoto, J. C. Cury, J. D. van Elsas, and A. S. Rosado, “Evaluation of soil bioremediation techniques in an aged diesel spill at the Antarctic Peninsula,” Applied Microbiology and Biotechnology, vol. 99, no. 24, pp. 10815–10827, 2015.
View at: Publisher Site | Google Scholar
K. E. Scherr, D. Backes, A. G. Scarlett, W. Lantschbauer, and M. Nahold, “Biogeochemical gradients above a coal tar DNAPL,” Science of the Total Environment, vol. 563-564, pp. 741–754, 2016.
View at: Publisher Site | Google Scholar
T. C. Hazen, R. C. Prince, and N. Mahmoudi, “Marine oil biodegradation,” Environmental Science and Technology, vol. 50, no. 5, pp. 2121–2129, 2016.
View at: Publisher Site | Google Scholar
W. F. M. Röling, I. R. Couto de Brito, R. P. J. Swannell, and I. M. Head, “Response of Archaeal communities in beach sediments to spilled oil and bioremediation,” Applied and Environmental Microbiology, vol. 70, no. 5, pp. 2614–2620, 2004.
View at: Publisher Site | Google Scholar
H. Urakawa, J. C. Garcia, P. D. Barreto, G. A. Molina, and J. C. Barreto, “A sensitive crude oil bioassay indicates that oil spills potentially induce a change of major nitrifying prokaryotes from the Archaea to the Bacteria,” Environmental Pollution, vol. 164, pp. 42–45, 2012.
View at: Publisher Site | Google Scholar
M. C. Redmond and D. L. Valentine, “Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 50, pp. 20292–20297, 2012.
View at: Publisher Site | Google Scholar
V. Catania, S. Cappello, V. Di Giorgi et al., “Microbial communities of polluted sub-surface marine sediments,” Marine Pollution Bulletin, vol. 131, part A, pp. 396–406, 2018.
View at: Publisher Site | Google Scholar
A. Mikkonen, M. Santalahti, K. Lappi, A.-M. Pulkkinen, L. Montonen, and L. Suominen, “Bacterial and archaeal communities in long-term contaminated surface and subsurface soil evaluated through coextracted RNA and DNA,” FEMS Microbiology Ecology, vol. 90, no. 1, pp. 103–114, 2014.
View at: Publisher Site | Google Scholar
D. Jurelevicius, C. R. de Almeida Couto, V. M. Alvarez, R. E. Vollú, F. de Almeida Dias, and L. Seldin, “Response of the archaeal community to simulated petroleum hydrocarbon contamination in marine and hypersaline ecosystems,” Water, Air & Soil Pollution, vol. 225, no. 2, article 1871, 2014.
View at: Publisher Site | Google Scholar
A. C. F. Dias, F. Dini-Andreote, R. G. Taketani et al., “Archaeal communities in the sediments of three contrasting mangroves,” Journal of Soils and Sediments, vol. 11, no. 8, pp. 1466–1476, 2011.
View at: Publisher Site | Google Scholar
M. Jeanbille, J. Gury, R. Duran et al., “Chronic polyaromatic hydrocarbon (PAH) contamination is a marginal driver for community diversity and prokaryotic predicted functioning in coastal sediments,” Frontiers in Microbiology, vol. 7, article 1303, 2016.
View at: Publisher Site | Google Scholar
M. Kolukirik, O. Ince, and B. K. Ince, “Increment in anaerobic hydrocarbon degradation activity of Halic Bay sediments via nutrient amendment,” Microbial Ecology, vol. 61, no. 4, pp. 871–884, 2011.
View at: Publisher Site | Google Scholar
Z. Zhang and I. M. C. Lo, “Biostimulation of petroleum-hydrocarbon-contaminated marine sediment with co-substrate: involved metabolic process and microbial community,” Applied Microbiology and Biotechnology, vol. 99, no. 13, pp. 5683–5696, 2015.
View at: Publisher Site | Google Scholar
M. E. Campeão, L. Reis, L. Leomil et al., “The deep-sea microbial community from the Amazonian Basin associated with oil degradation,” Frontiers in Microbiology, vol. 8, article 1019, 2017.
View at: Publisher Site | Google Scholar
L. Wang, X. Huang, and T.-L. Zheng, “Responses of bacterial and archaeal communities to nitrate stimulation after oil pollution in mangrove sediment revealed by Illumina sequencing,” Marine Pollution Bulletin, vol. 109, no. 1, pp. 281–289, 2016.
View at: Publisher Site | Google Scholar
L. Yan, D. Yu, N. Hui et al., “Distribution of Archaeal communities along the coast of the Gulf of Finland and their response to oil contamination,” Frontiers in Microbiology, vol. 9, p. 15, 2018.
View at: Publisher Site | Google Scholar
A. J. Pinto and L. Raskin, “PCR biases distort Bacterial and Archaeal community structure in pyrosequencing datasets,” PLoS One, vol. 7, no. 8, article e43093, 2012.
View at: Publisher Site | Google Scholar
M. Singh, P. K. Srivastava, V. K. Jaiswal, and R. N. Kharwar, “Biotechnological applications of microbes for the remediation of environmental pollution,” in Biotechnology: Trends and Applications, R. Singh and M. Trivedi, Eds., pp. 179–214, Stadium Press LLC, USA, 2016.
View at: Google Scholar
D. Prakash, P. Gabani, A. K. Chandel, Z. Ronen, and O. V. Singh, “Bioremediation: a genuine technology to remediate radionuclides from the environment,” Microbial Biotechnology, vol. 6, no. 4, pp. 349–360, 2013.
View at: Publisher Site | Google Scholar
Y. Zivanovic, J. Armengaud, A. Lagorce et al., “Genome analysis and genome-wide proteomics of Thermococcus gammatolerans, the most radioresistant organism known amongst the Archaea,” Genome Biology, vol. 10, no. 6, article R70, 2009.
View at: Publisher Site | Google Scholar
M. Choudhary, R. Kumar, A. Datta, V. Nehra, and N. Greg, “Bioremediation of heavy metals by microbes,” in Bioremediation of Salt Affected Soils: An Indian Perspective, S. Arora, A. Singh, and Y. Singh, Eds., pp. 233–255, Springer, Cham, 2017.
View at: Google Scholar
P. Ranawat and S. Rawat, “Metal-tolerant thermophiles: metals as electron donors and acceptors, toxicity, tolerance and industrial applications,” Environmental Science and Pollution Research, vol. 25, no. 5, pp. 4105–4133, 2018.
View at: Publisher Site | Google Scholar
C. R. Jackson, H. W. Langner, J. Donahoe-Christiansen, W. P. Inskeep, and T. R. McDermott, “Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring,” Environmental Microbiology, vol. 3, no. 8, pp. 532–542, 2001.
View at: Publisher Site | Google Scholar
H. M. Sehline and E. B. Linström, “Oxidation and reduction of arsenic by Sulfolobus acidocaldarius strain BC,” FEMS Microbiology Letters, vol. 93, no. 1, pp. 87–92, 1992.
View at: Publisher Site | Google Scholar
E. Lebrun, M. Brugna, F. Baymann et al., “Arsenite oxidase, an ancient bioenergetic enzyme,” Molecular Biology and Evolution, vol. 20, no. 5, pp. 686–693, 2003.
View at: Publisher Site | Google Scholar
A. Heinrich-Salmeron, A. Cordi, C. Brochier-Armanet et al., “Unsuspected diversity of arsenite-oxidizing bacteria as revealed by widespread distribution of the aoxB gene in prokaryotes,” Applied and Environmental Microbiology, vol. 77, no. 13, pp. 4685–4692, 2011.
View at: Publisher Site | Google Scholar
O. F. Ordoñez, M. C. Rasuk, M. N. Soria, M. Contreras, and M. E. Farías, “Haloarchaea from the Andean Puna: biological role in the energy metabolism of arsenic,” Microbial Ecology, vol. 76, 2018.
View at: Publisher Site | Google Scholar
R. Huber, M. Sacher, A. Vollmann, H. Huber, and D. Rose, “Respiration of arsenate and selenate by hyperthermophilic Archaea,” Systematic and Applied Microbiology, vol. 23, no. 3, pp. 305–314, 2000.
View at: Publisher Site | Google Scholar
E. S. Boyd and T. Barkay, “The mercury resistance operon: from an origin in a geothermal environment to an efficient detoxification machine,” Frontiers in Microbiology, vol. 3, p. 349, 2012.
View at: Publisher Site | Google Scholar
Y. Wang, E. Boyd, S. Crane et al., “Environmental conditions constrain the distribution and diversity of Archaeal merA in Yellowstone National Park, Wyoming, USA,” Microbial Ecology, vol. 62, no. 4, pp. 739–752, 2011.
View at: Publisher Site | Google Scholar
J. Schelert, V. Dixit, V. Hoang, J. Simbahan, M. Drozda, and P. Blum, “Occurrence and characterization of mercury resistance in the hyperthermophilic Archaeon Sulfolobus solfataricus by use of gene disruption,” Journal of Bacteriology, vol. 186, no. 2, pp. 427–437, 2003.
View at: Publisher Site | Google Scholar
D. M. Al-Mailem, H. Al-Awadhi, N. A. Sorkhoh, M. Eliyas, and S. S. Radwan, “Mercury resistance and volatilization by oil utilizing haloarchaea under hypersaline conditions,” Extremophiles, vol. 15, no. 1, pp. 39–44, 2011.
View at: Publisher Site | Google Scholar
C. C. Gilmour, M. Podar, A. L. Bullock et al., “Mercury methylation by novel microorganisms from new environments,” Environmental Science and Technology, vol. 47, no. 20, pp. 11810–11820, 2013.
View at: Publisher Site | Google Scholar
L. Newsome, K. Morris, and J. R. Lloyd, “The biogeochemistry and bioremediation of uranium and other priority radionuclides,” Chemical Geology, vol. 363, pp. 164–184, 2014.
View at: Publisher Site | Google Scholar
K. Kashefi, B. M. Moskowitz, and D. R. Lovley, “Characterization of extracellular minerals produced during dissimilatory Fe(III) and U(VI) reduction at 100°C by Pyrobaculum islandicum,” Geobiology, vol. 6, no. 2, pp. 147–154, 2008.
View at: Publisher Site | Google Scholar
K. Kashefi and D. R. Lovley, “Reduction of Fe(III), Mn(IV), and toxic metals at 100°C by Pyrobaculum islandicum,” Applied and Environmental Microbiology, vol. 66, no. 3, pp. 1050–1056, 2000.
View at: Publisher Site | Google Scholar
B. K. Kim, T. D. Pihl, J. N. Reeve, and L. Daniels, “Purification of the copper response extracellular proteins secreted by the copper-resistant methanogen Methanobacterium bryantii BKYH and cloning, sequencing, and transcription of the gene encoding these proteins,” Journal of Bacteriology, vol. 177, no. 24, pp. 7178–7185, 1995.
View at: Publisher Site | Google Scholar
T. Reitz, M. L. Merroun, and S. Selenska-Pobell, “Interactions of Paenibacillus sp. and Sulfolobus acidocaldarius strains with U(VI),” in Uranium, Mining, and Hydrogeology, B. J. Merkel and A. Hasche-Berger, Eds., Springer, Berlin, Heidelberg, 2008.
View at: Publisher Site | Google Scholar
X. Zhuang, Z. Han, Z. Bai, G. Zhuang, and H. Shim, “Progress in decontamination by halophilic microorganisms in saline wastewater and soil,” Environmental Pollution, vol. 158, no. 5, pp. 1119–1126, 2010.
View at: Publisher Site | Google Scholar
S. Naik and I. Furtado, “Equilibrium and kinetics of adsorption of Mn⁺² by Haloarchaeon Halobacterium sp. GUSF (MTCC3265),” Geomicrobiology Journal, vol. 31, no. 8, pp. 708–715, 2014.
View at: Publisher Site | Google Scholar
A. R. Showalter, J. E. S. Szymanowski, J. B. Fein, and B. A. Bunker, “An x-ray absorption spectroscopy study of Cd binding onto a halophilic archaeon,” Journal of Physics: Conference Series, vol. 712, article 012079, 2016.
View at: Publisher Site | Google Scholar
M. Bader, K. Müller, H. Foerstendorf et al., “Comparative analysis of uranium bioassociation with halophilic bacteria and archaea,” PLoS One, vol. 13, no. 1, article e0190953, 2018.
View at: Publisher Site | Google Scholar
M. Bader, K. Müller, H. Foerstendorf et al., “Multistage bioassociation of uranium onto an extremely halophilic archaeon revealed by a unique combination of spectroscopic and microscopic techniques,” Journal of Hazardous Materials, vol. 327, pp. 225–232, 2017.
View at: Publisher Site | Google Scholar
D. K. Nordstrom and G. Southham, “Geomicrobiology:interactions between microbes and minerals,” in Reviews in Mineralogy, vol. 35, J. F. Banfield and K. H. Nealson, Eds., pp. 361–390, Mineralogical Society of America, Washington, DC, USA, 1997.
View at: Google Scholar
K. J. Edwards, P. L. Bond, T. M. Gihring, and J. F. Banfield, “An Archaeal iron-oxidizing extreme acidophile important in acid mine drainage,” Science, vol. 287, no. 5459, pp. 1796–1799, 2000.
View at: Publisher Site | Google Scholar
O. V. Golyshina and K. N. Timmis, “Ferroplasma and relatives, recently discovered cell wall-lacking archaea making a living in extremely acid, heavy metal-rich environments,” Environmental Microbiology, vol. 7, no. 9, pp. 1277–1288, 2005.
View at: Publisher Site | Google Scholar
G. Huber and K. O. Stetter, “Sulfolobus metallicus, sp. nov., a novel strictly chemolithoautotrophic thermophilic archaeal species of metal-mobilizers,” Systematic and Applied Microbiology, vol. 14, no. 4, pp. 372–378, 1991.
View at: Publisher Site | Google Scholar
D. E. Rawlings, “Heavy metal mining using microbes,” Annual Review of Microbiology, vol. 56, no. 1, pp. 65–91, 2002.
View at: Publisher Site | Google Scholar
A. P. Yelton, L. R. Comolli, N. B. Justice et al., “Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea,” BMC Genomics, vol. 14, no. 1, p. 485, 2013.
View at: Publisher Site | Google Scholar
K. B. Hallberg, “New perspectives in acid mine drainage microbiology,” Hydrometallurgy, vol. 104, no. 3-4, pp. 448–453, 2010.
View at: Publisher Site | Google Scholar
G. Muyzer and A. J. M. Stams, “The ecology and biotechnology of sulphate-reducing bacteria,” Nature Reviews Microbiology, vol. 6, no. 6, pp. 441–454, 2008.
View at: Publisher Site | Google Scholar
J. Beeder, R. K. Nilsen, J. T. Rosnes, T. Torsvik, and T. Lien, “Archaeoglobus fulgidus isolated from hot north sea oil field waters,” Applied and Environmental Microbiology, vol. 60, no. 4, pp. 1227–1231, 1994.
View at: Google Scholar
T. Itoh, K.-I. Suzuki, P. C. Sanchez, and T. Nakase, “Caldivirga maquilingensis gen. nov., sp. nov., a new genus of rod-shaped crenarchaeote isolated from a hot spring in the Philippines,” International Journal of Systemic and Evolutionary Microbiology, vol. 49, no. 3, pp. 1157–1163, 1999.
View at: Publisher Site | Google Scholar
T. Itoh, K.-I. Suzuki, and T. Nakase, “Thermocladium modestius gen. nov., sp. nov., a new genus of rod-shaped, extremely thermophilic crenarchaeote,” International Journal of Systemic and Evolutionary Microbiology, vol. 48, pp. 879–887, 1998.
View at: Publisher Site | Google Scholar
L. Bhatnagar, S. P. Li, M. K. Jain, and J. G. Zeikus, “Growth of methanogenic and acidogenic bacteria with pentachlorophenol as a co-substrate,” in Biotechnology applications in hazardous waste treatment, pp. 383–393, Engineering Foundation, New York, NY, USA, 1989.
View at: Google Scholar
B. Z. Fathepure, J. P. Nengu, and S. A. Boyd, “Anaerobic bacteria that dechlorinate perchloroethene,” Applied and Environmental Microbiology, vol. 53, no. 11, pp. 2671–2674, 1987.
View at: Google Scholar
P. E. Jablonski and J. G. Ferry, “Reductive dechlorination of trichloroethylene by the CO-reduced CO dehydrogenase enzyme complex from Methanosarcina thermophila,” FEMS Microbiology Letters, vol. 96, no. 1, pp. 55–59, 1992.
View at: Publisher Site | Google Scholar
M. D. Mikesell and S. A. Boyd, “Dechlorination of chloroform by Methanosarcina strains,” Applied and Environmental Microbiology, vol. 56, no. 4, pp. 1198–1201, 1990.
View at: Google Scholar
U. E. Krone and R. K. Thauer, “Dehalogenation of trichlorofluoromethane (CFC-11) by Methanosarcina barkeri,” FEMS Microbiology Letters, vol. 90, no. 2, pp. 201–204, 1992.
View at: Publisher Site | Google Scholar
R. A. Mah and D. A. Kuhn, “Transfer of the type species of the genus Methanococcus to the genus Methanosarcina, naming it Methanosarcina mazei (Barker 1936) comb. nov. et emend. and conservation of the genus Methanococcus (Approved Lists 1980) with Methanococcus vannielii (Approved Lists 1980) as the type species,” International Journal of Systematic and Evolutionary Microbiology, vol. 34, no. 2, pp. 263–265, 1984.
View at: Publisher Site | Google Scholar
A. Wasserfallen, J. Nölling, P. Pfister, J. Reeve, and E. Conway de Macario, “Phylogenetic analysis of 18 thermophilic Methanobacterium isolates supports the proposals to create a new genus, Methanothermobacter gen. nov., and to reclassify several isolates in three species, Methanothermobacter thermautotrophicus comb. nov., Methanothermobacter wolfeii comb. nov., and Methanothermobacter marburgensis sp. nov,” International Journal of Systemic and Evolutionary Microbiology, vol. 50, pp. 43–53, 2000.
View at: Publisher Site | Google Scholar
C. Holliger, G. Schraa, A. J. M. Stams, and A. J. B. Zehnder, “Reductive dechlorination of 1,2-dichloroethane and chloroethane by cell suspensions of methanogenic bacteria,” Biodegradation, vol. 1, no. 4, pp. 253–261, 1990.
View at: Publisher Site | Google Scholar
J. R. Roth, J. G. Lawrence, and T. A. Bobik, “COBALAMIN (COENZYME B₁₂): synthesis and biological significance,” Annual Review of Microbiology, vol. 50, no. 1, pp. 137–181, 1996.
View at: Publisher Site | Google Scholar
D. Jan, “Thermodynamic considerations for dehalogenation,” in Dehalogenation: Microbial Processes and Environmental Applications, M. M. Häggblom and I. D. Bossert, Eds., Kluwer Academic Publishers, Boston, MA, USA, 2003.
View at: Publisher Site | Google Scholar
U. E. Krone, R. K. Thauer, and H. P. C. Hogenkamp, “Reductive dehalogenation of chlorinated C1-hydrocarbons mediated by corrinoids,” Biochemistry, vol. 28, no. 11, pp. 4908–4914, 1989.
View at: Publisher Site | Google Scholar
B. Heckel, K. McNeill, and M. Elsner, “Chlorinated ethene reactivity with vitamin B₁₂ is governed by cobalamin chloroethylcarbanions as crossroads of competing pathways,” ACS Catalysis, vol. 8, no. 4, pp. 3054–3066, 2018.
View at: Publisher Site | Google Scholar
R. E. Richardson, V. K. Bhupathiraju, D. L. Song, T. A. Goulet, and L. Alvarez-Cohen, “Phylogenetic characterization of microbial communities that reductively dechlorinate TCE based upon a combination of molecular techniques,” Environmental Science and Technology, vol. 36, no. 12, pp. 2652–2662, 2002.
View at: Publisher Site | Google Scholar
P. C. Dennis, B. E. Sleep, R. R. Fulthorpe, and S. N. Liss, “Phylogenetic analysis of bacterial populations in an anaerobic microbial consortium capable of degrading saturation concentrations of tetrachloroethylene,” Canadian Journal of Microbiology, vol. 49, no. 1, pp. 15–27, 2003.
View at: Publisher Site | Google Scholar
T. W. Macbeth, D. E. Cummings, S. Spring, L. M. Petzke, and K. S. Sorenson Jr., “Molecular characterization of a dechlorinating community resulting from in situ biostimulation in a trichloroethene-contaminated deep, fractured basalt aquifer and comparison to a derivative laboratory culture,” Applied and Environmental Microbiology, vol. 70, no. 12, pp. 7329–7341, 2004.
View at: Publisher Site | Google Scholar
M. Duhamel and E. A. Edwards, “Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides,” FEMS Microbiology Ecology, vol. 58, no. 3, pp. 538–549, 2006.
View at: Publisher Site | Google Scholar
A. C. Heimann, D. J. Batstone, and R. Jakobsen, “Methanosarcina spp. drive vinyl chloride dechlorination via interspecies hydrogen transfer,” Applied and Environmental Microbiology, vol. 72, no. 4, pp. 2942–2949, 2006.
View at: Publisher Site | Google Scholar
D. E. Fennell and J. M. Gossett, “Modeling the production of and competition for hydrogen in a dechlorinating culture,” Environmental Science and Technology, vol. 32, no. 16, pp. 2450–2460, 1998.
View at: Publisher Site | Google Scholar
Y. Men, H. Feil, N. C. VerBerkmoes et al., “Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analyses,” The ISME Journal, vol. 6, no. 2, pp. 410–421, 2012.
View at: Publisher Site | Google Scholar
S. Yi, E. C. Seth, Y.-J. Men et al., “Versatility in corrinoid salvaging and remodeling pathways supports corrinoid-dependent metabolism in Dehalococcoides mccartyi,” Applied and Environmental Microbiology, vol. 78, no. 21, pp. 7745–7752, 2012.
View at: Publisher Site | Google Scholar
M. Fincker and A. M. Spormann, “Biochemistry of catabolic reductive dehalogenation,” Annual Review of Biochemistry, vol. 86, no. 1, pp. 357–386, 2017.
View at: Publisher Site | Google Scholar
M. Guo and Y. Chen, “Coenzyme cobalamin: biosynthesis, overproduction and its application in dehalogenation – a review,” Reviews in Environmental Science and Biotechnology, vol. 17, no. 2, pp. 259–284, 2018.
View at: Publisher Site | Google Scholar
M. J. Krzmarzick, B. B. Crary, J. J. Harding et al., “Natural niche for organohalide-respiring Chloroflexi,” Applied and Environmental Microbiology, vol. 78, no. 2, pp. 393–401, 2011.
View at: Publisher Site | Google Scholar
M. J. Krzmarzick, P. J. McNamara, B. B. Crary, and P. J. Novak, “Abundance and diversity of organohalide-respiring bacteria in lake sediments across a geographical sulfur gradient,” FEMS Microbiology Ecology, vol. 84, no. 2, pp. 248–258, 2013.
View at: Publisher Site | Google Scholar
M. L. Lim, M. D. Brooks, M. A. Boothe, and M. J. Krzmarzick, “Novel bacterial diversity is enriched with chloroperoxidase-reacted organic matter under anaerobic conditions,” FEMS Microbiology Ecology, vol. 94, no. 5, article fiy050, 2018.
View at: Publisher Site | Google Scholar
C. J. Smith and A. M. Osborn, “Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology,” FEMS Microbiology Ecology, vol. 67, no. 1, pp. 6–20, 2009.
View at: Publisher Site | Google Scholar
D. L. Valentine, “Adaptations to energy stress dictate the ecology and evolution of the Archaea,” Nature Reviews Microbiology, vol. 5, no. 4, pp. 316–323, 2007.
View at: Publisher Site | Google Scholar
K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar, “MEGA6: molecular evolutionary genetics analysis version 6.0,” Molecular Biology and Evolution, vol. 30, no. 12, pp. 2725–2729, 2013.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2018 Mark James Krzmarzick et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

9018

Downloads

2880

Citations