The first two separation nodes representing the hypersaline, saline and fresh environments accounted for 9.1% of the total phylogenetic lineage variance. The first comprehensive phylogenetic tree of Bathyarchaeota was constructed in 2012 (Kuboetal.2012); it was based on 4720 bathyarchaeotal sequences from the SILVA database (SSU Ref NR106 and SSU Parc106). Markers for individual pathway/function were scanned against genomes using the HMM and KEGG databases (Anantharamanetal.2016; Kanehisa, Sato and Morishima 2016; Spang, Caceres and Ettema 2017). Fosmid clone 37F10 containing a genome fragment originating from a bathyarchaeotal member was isolated from a metagenomic library constructed from Pearl River sediment samples (Mengetal.2009); its G + C content indicated that this genomic fragment had two portions: an archaeon-like portion (42.2%) and a bacterium-like portion (60.1%) (Mengetal.2009; Lietal.2012). In addition to the global distribution, expanding prokaryotic community investigations of deep ocean drilling sediments revealed that members of Bathyarchaeota occupy considerable fractions of the archaeal communities (Teske 2006). Given that they are abundant, globally distributed and phylogenetically diverse, continued exploration of new potential bathyarchaeotal subgroups is encouraged. Recently, Subgroup-15 was widely detected in both freshwater and marine benthic sediments; its persistent distribution along the sediment depth profile, with higher abundance within active archaeal communities, provides additional hints linking its members physiological traits to habitat preferences (Liuetal.2014). The available genomic evidence of various known and unknown methyltransferases harbored by BA1 and BA2 suggests the existence of a methylated compound utilization pathway, with the methyl group being ultimately reduced to CH3-H4MPT and integrated into the methyl-branch of the WoodLjungdahl pathway (Evansetal.2015). To avoid the confusion, Subgroups-18 and -19 were named to be consistent with subgroups MCG-18 and MCG-19 as proposed in two previous reports (respectively Lazaretal.2015; Filloletal.2016), while Subgroup-20 was renamed to replace the subgroup MCG-19 in Fillol et al.s tree (Filloletal.2016). It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. (C) The metabolic properties of 24 bathyarchaeotal genomes. In this process, methane is not assimilated by Bathyarchaeota but serves as an energy source. Based on the ancestral analysis, the phylum Bathyarchaeota is suggested to have a hot origin. Taken together, these findings are further steps toward the elucidation of the origin, evolution, and roles of Bathyarchaeota, a globally important archaeal phylum. Here we reported the abundance of Bathyarchaeota members across different ecosystems and their correlation with environmental factors by constructing 16S The inset table shows the distribution of subgroups in major environmental categories. Materials and methods 2.1. Tree building intermediate files are publicly available (https://github.com/ChaoLab/Bathy16Stree). The picked genomes are of high completeness (>70%) and good quality (excluding genomes with numerous long breaking parts with N). Bathyarchaeota was the most abundant archaeal phylum in most samples, accounting for 13.8164.14% of archaeal sequences (Fig. All sequences were clustered at 90% identity using Usearch v10.0.240 (https://www.drive5.com/usearch/), then the 16S rRNA gene sequences from available bathyarchaeotal genomes in public database, the anchor sequences from Kuboetal. Bathyarchaeota was initially proposed to form a distinct cluster closely related to Aigarchaeota and hyperthermophilic Crenarchaeota; because of their terrestrial origin (Barnsetal.1996) (such as freshwater lakes and hot springs), the name Terrestrial MCG was temporarily proposed (Takaietal.2001). WebEtymology: Gr. Peat MCG group was represented with one sequence at 90% cutoff level (Xiangetal.2017). Details of markers refer to Supplementary Table S1 available online. Furthermore, another study demonstrated that the archaeal communities of the sulfatemethane transition zone at diffusion-controlled sediments of Aarhus Bay (Denmark) contain considerable amounts of Bathyarchaeota; the overall archaeal community structure did not change greatly during the experimentits diversity was lower after 6 months of incubation under heterotrophic conditions, with periodic modest sulfate and acetate additions (Websteretal.2011). The gene for cytoplasmic flavin adenine dinucleotide-containing dehydrogenase (glcD) co-located with hdrD, indicating that BA1 uses lactate to reduce heterodisulfide in methanogenesis. 2017KZDXM071), and the Science and Technology Innovation Committee of Shenzhen (Grant No. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. Subgroup-5b was further split into 5b and 5bb, as additional sequences were added. They also acquired some subunits of coenzyme F420 hydrogenase; this enzyme generates reduced ferredoxin, with hydrogen as the electron donor, as an alternative to MvhADG in many Methanomicrobiales (Thaueretal.2008; Lazaretal.2016; Sousaetal.2016). The Miscellaneous Crenarchaeotal Group (MCG) archaea were firstly detected from a hot spring (Barnsetal.1996) and later proposed with a name in a study surveying 16S rRNA gene sequences from marine subsurface sediments (Inagakietal.2003). Second, determining whether the methane cycling capacity is confined to certain subgroups or whether numerous subgroups or lineages are capable of methane cycling, and if so, the nature of their shared evolutionary or genomic characteristics, is of utmost importance. Combined with the aforementioned specific heterotrophic metabolic potentials of members within bathyarchaeotal subgroups and their occurrence in sediment layers of distinct biogeochemical properties (Lazaretal.2015), it was proposed that the acquisition of diverse physiological capacities by Bathyarchaeota is driven by adaptation to specific habitats rather than there being a common metabolic capacity. Open reading frames encoded by the three fosmid clones comprised genes related to lipid biosynthesis, energy metabolism and resistance to oxidants. The clear growth stimulus and lignin-related 13C-bicarbonate incorporation into lipids strongly suggests that Bathyarchaeota (Subgroup-8) may be able to use the second-most abundant biopolymer lignin on Earth (Yuetal.2018). A recent study found that the refractory aromatic polymer lignin stimulated the growth of Bathyarchaeota (Subgroup-8) and they incorporated CO2 as a carbon source autotrophically and utilized lignin as an energy source (Yuetal.2018). (Kuboetal.2012), and the outgroup sequences of Crenarchaeota, YNPFFA group and Korarchaeota were added. [43] (Figure 4). Based on the phylogenetic analysis of concatenated rRNA, ribosome proteins and topomerase IB protein-encoding genes, MCG is phylogenetically distinct from the closely related Aigarchaeota and Thaumarchaeota, and comprises a parallel lineage that has perhaps evolved from a common ancestor (Mengetal.2014). Together with evidence of few phylogenetic changes throughout the incubation, it was suggested that the microbial community detected by stable isotopic probing could serve well in reflecting the metabolically active components. That approach revealed an order of magnitude increase in bathyarchaeotal abundance in both the control and experimental groups compared with time zero; however, no significant increase of bathyarchaeotal abundance was observed in experimental groups with substrate additives and various cultivation processing steps, compared with control groups with basal medium alone. Jacquemet A, Barbeau J, Lemiegre L et al. However, it has lost the majority of genes involved in the methyl branch of the WoodLjungdahl pathway and also lost energy-conserving complexes, similar to BA1. 2012 ). Lomstein BA, Langerhuus AT, DHondt S et al. Bathyarchaeota occupied about 60% of the total archaea in the Jiulong River, China (Li et al. A detailed knowledge of the phylogenetic structure of the Bathyarchaeota phylum is crucial for the understanding of their ecological significance in global sedimentary processes. Sousa FL, Neukirchen S, Allen JF et al. Vanwonterghem I, Evans PN, Parks DH et al. Bathyarchaeota, reflecting its phylogenetic position as deeply branching with Aigarchaeota and Thaumarchaeota, and its prevalence in subsurface sediments (Mengetal.2014). Until now, The incorporation of 13C-bicarbonate into the archaeal lipids (potential bathyarchaeotal-specific biphytanes) was significantly observed only with lignin addition. pl. Uncultured archaea in deep marine subsurface sediments: have we caught them all? Results In the current study, nine In summary, the most recent research advances have considerably expanded our knowledge of Bathyarchaeota, their distribution, ecology and physiological and genomic properties since their first discovery and definition about two decades ago. Introduction. Here we provide several lines of converging evidence suggesting the bathyarchaeotal group Bathy-8 is able to grow with lignin as an energy source and 2). WebHome Business Account Form is bathyarchaeota multicellular. As suggested by the classification of uncultured archaea based on nearly full-length 16S rRNA gene sequences, the bathyarchaeotal sequence boundary falls into the minimum sequence identity range of phylum level (74.9579.9%), and each subgroup generally falls into the median sequence identity range of family and order levels (91.6592.9% and 88.2590.1%, respectively) (Yarzaetal.2014). Due to their prevalence in the microbial community, we also performed phylogenetic analysis to understand the closeness of our Bathyarchaeota OTUs with Recently, two bathyarchaeotal genome bins (BA1 and BA2) were recovered from the formation waters of coal-bed methane wells within the Surat Basin (Evansetal.2015). (2016), it appears that these microbes rely on the acetyl-CoA synthetase (Acd) to generate acetate (Heetal.2016). ( 2012) conducted a comprehensive analysis of the biogeographical distribution of Bathyarchaeota and found that it was the dominant archaeal population in anoxic, low-activity subsurface sediments. The archaeal phylum Bathyarchaeota, which is composed of a large number of diverse lineages, is widespread and abundant in marine sediments. Hence, the primer pair MCG242dF and MCG678R was developed based on a collection of bathyarchaeotal sequences of freshwater origin (Filloletal.2016). (2017) investigated the bathyarchaeotal community in two sediment cores from the South China Sea; the authors revealed a direct strong positive correlation between bathyarchaeotal 16S rRNA gene abundance and total organic carbon content along the core depth, suggesting an overall heterotrophic lifestyle of Bathyarchaeota in the South China Sea. Both Bathyarchaeota and the recently identified more basally branched Lokiarchaeota acquired the H4MPT-dependent WoodLjungdahl pathway and the hydrogen-dependent electron bifurcating system MvhADG-HdrABC, viewed as typical for the anaerobic and hydrogen-dependent archaeal lifestyle (Lazaretal.2016; Sousaetal.2016). Energy flux analysis revealed that AOM and slow degradation of refractory sedimentary organic matter were the two principal energy generation pathways in the local community. Thauer RK, Kaster A-K, Seedorf H et al. According to that hypothesis, the proto-mitochondrion bacterium was capable of both respiration and anaerobic H2-producing fermentation; anaerobic syntrophy with respect to H2 brought about a physical association with an H2-dependent host and initiated a symbiotic association with the host; this led to endosymbiosis, after engulfment by the host cell (Martin and Muller 1998; Martinetal.2016). To alleviate the nomenclature confusion, we constructed an updated RAxML tree (Fig. Bathyarchaeota dominate 16S rRNA clone libraries of transcribed RNA constructed for the Peru Margin ODP site 1229 (Parkesetal.2005; Biddleetal.2006) and the upper 35 m of the subsurface sediments at the Peru Margin ODP site 1227 (Inagakietal.2006; Sorensen and Teske 2006). Laso-Prez R, Wegener G, Knittel K et al. Subgroup-5 is divided into Subgroups-5a and -5b, each with intragroup similarity >90% according to a maximum-likelihood estimation. Furthermore, the lack of genes for ATPases and membrane-bound electron transport enzymes in the two genomic bins (BA1 and BA2) and the presence of the ion pumping, energy-converting hydrogenase complex (only in BA1), which might allow solute transportation independently of energy-generation mechanisms, suggest that the soluble substrate transportation is solely responsible for energy conservation (Evansetal.2015). Based on the above, it is proposed that Bathyarchaeota might mediate the AOM without assimilating the carbon in methane. Species abundance distribution analysis indicates that Bathyarchaeota is one of the persistent and abundant core lineages of the sediment archaeal communities, showing, to some extent, habitat-specific distribution (Filloletal.2016). This method has been used to target the bathyarchaeotal 16S rRNA gene with specific probes, providing information on the active bathyarchaeotal community without culturing (Table 1). Anantharaman K, Brown CT, Hug LA et al. Surprisingly, these genes fall closely to the Bathyarchaeota mcr genes. Capella-Gutirrez S, Silla-Martnez JM, Gabaldn T. Coolen MJL, Cypionka H, Sass AM et al. This would be supported by a coupled AOM and syntrophic SRB metabolism, with methane consumed by Bathyarchaeota through reverse acetoclastic methanogenesis with the production of acetate, which is readily oxidized by sulfate in SRB. The groups of B24 and B25 (Heetal.2016) were added into the tree representing Subgroups-21 and -22, respectively. The primer pair MCG242dF/MCG528R may potentially be used for the determination of the bathyarchaeotal community abundance, with relatively high subgroup coverage and specificity in silico; however, experimental tests are needed to confirm this. Abstract. However, after allowing for a single nucleotide mismatch, the coverage efficiency markedly increased, to around 8090%. 3C). The results also revealed that some operational taxonomic units affiliated with Subgroups-2 and -15 are dominant in all surface and bottom sediment layers in these two cores, suggesting that these operational taxonomic units might be adaptive to redox changes (Yuetal.2017). Subgroups were assigned from the corresponding 16S rRNA gene phylogenic tree (Fig. The phylum Bathyarchaeota, which has high species and functional diversity, is abundant and widespread in marine sediments. Oxford University Press is a department of the University of Oxford. the potential AOM metabolism of Bathyarchaeota in the flange of the hydrothermal vent would be consistent with the aforementioned genomic inferences (Evansetal.2015). However, in a study investigating the archaeal lipidome in the White Oak River estuary, the presence of the recently discovered butanetriol dibiphytanyl glycerol tetraethers correlated well with bathyarchaeotal abundance along the sediment depth (Meadoretal.2015). Further, a close co-occurrence of Bathyarchaeota and Methanomicrobia hinted at a syntrophic association between them; the acetate production/consumption relationship between the two might be responsible for such a scenario, as proposed by metabolic predictions (Heetal.2016; Xiangetal.2017). No methane metabolism genes were recovered from bathyarchaeotal genomic bins or any contigs from the WOR estuarine sediments, in contrast to an earlier study (Evansetal.2015). The percentages in every row stand for the proportions of subgroups in each environmental category. This approach revealed that the separation of subgroups according to saline and anoxic levels could explain 13% of the phylogenetic lineage variance. The syntrophic relationship between Bathyarchaeota and SRB would be similar to the anaerobic methane-oxidizing archaea (ANME)/SRB consortium, and acetate would be maintained at a low level as a transient intermediate (Boetiusetal.2000; Hinrichs and Boetius 2002). Three fosmid clones harboring bathyarchaeotal genomic fragments were screened from the South China Sea sediments (05 cm depth) (Lietal.2012). Bathyarchaeota, a recently proposed archaeal phylum, is globally distributed and highly abundant in anoxic sediments. Gene arrangement in these two fosmid clones, together with the previously recovered bathyarchaeotal fosmid sequences, confirmed low collinearity with other known archaeal genomes. Lloyd KG, Schreiber L, Petersen DG et al. Furthermore, both FISH labeling and intact polar lipid quantification suggest the presence of highly abundant and active bathyarchaeotal cells in the Peru offshore subsurface sediments collected during the Ocean Drilling Program Leg 201 (Biddleetal.2006; Lippetal.2008). The emergence of freshwater-adapted lineages, including freshwater-indicative Subgroups-5, -7, -9 and -11, occurred after the first salinefreshwater transition event (Filloletal.2016). Bathyarchaeota, formerly known as the Miscellaneous Crenarchaeotal Group, is a phylum of global generalists that are widespread in anoxic sediments, which host relatively high abundance archaeal communities. 2. Recent genomic evidence suggests that Bathyarchaeota might potentially be involved in methane metabolism, a property that had only been confirmed to date in the Euryarchaeota domain (Evansetal.2015; Lloyd 2015). In this tree, the Subgroups-1 to -17 were the same as Kubo's tree (Kuboetal.2012), and Subgroup-5 was divided into Subgroups-5a, -5b and -5bb as suggested in Fillol et al.s research (Filloletal.2016). The wide phylogenetic coverage increases the difficulty of inferring the general metabolic properties across whole lineages. Bathyarchaeota is characterized by high intragroup diversity, with most subgroups showing within-sequence similarity <92% (Kuboetal.2012; Filloletal.2016). The uptake and breakdown of polymeric hydrocarbons is facilitated by extracellular hydrolases; Bathyarchaeota also acquired the EmbdenMeyerhof Parnas/EntnerDoudoroff glycolysis and gluconeogenesis pathway for the core hydrocarbon utilization metabolism. The analysis of the stable isotopic-probed microcosms from Cheesequake salt marsh sediment revealed that all Crenarchaeota groups, which still include Bathyarchaeota and Thaumarchaeota (formerly Crenarchaeota MG 1.a) and other Crenarchaeota groups, are heterotrophic and do not incorporate 13C-bicarbonate (Seyler, McGuinness and Kerkhof 2014). A pair of primers (Bathy-442F/Bathy-644R) was recently designed to target Subgroups-15 and -17; the in silico primer testing indicates that Bathy-442F can also adequately cover Subgroups-2, -4, -9 and -14, with Bathy-644R covering nearly all subgroups, except for Subgroups-6 and -11 (Yuetal.2017). Metabolic potential of Bathyarchaeota and their interactive relationships with other microorganisms. The in silico tests revealed that primers MCG528, MCG493, MCG528 and MCG732 cover 87, 79, 44 and 27% of sequences of Subgroups-1 to -12 on average, respectively. It also contains typical methane metabolism genes (hdrABC and mvhADG) but lacks hdrE, similar to Methanomassiliicoccales genomes (Evansetal.2015). Bathyarchaeota are believed to have roles in the carbon cycle in marine systems. Along with the widespread distribution of Bathyarchaeota, i.e. Evans PN, Parks DH, Chadwick GL et al. 4) (Evansetal.2015; Heetal.2016; Lazaretal.2016). JCYJ20170818091727570). (2016) demonstrated that half of the bathyarchaeotal genomes encode a set of phosphate acetyltransferase (Pta) and acetate kinase (Ack) for acetate production or assimilation, usually observed in bacteria. Based on the genomic evidence, the authors concluded that some lineages of Bathyarchaeota are similar to bona fide bacterial homoacetogens, with pathways for acetogenesis and fermentative utilization of a variety of organic substrates (Heetal.2016). (A) Phylogenetic tree of ribosomal proteins obtained from currently available bathyarchaeotal genomes (from GenBank, 29 November 2017 updated). In summary, there are a total of 25 subgroups of Bathyarchaeota based on all available 16S rRNA gene sequences at this moment, and the former names for each subgroup are also labeled in the tree (Fig. Liu et al. In terms of energy metabolism, these archaea contain the WoodLjungdahl pathway, capable of generating acetyl-CoA autotrophically by CO2 and H2. This group of lipids has not been found in natural environments or microorganism enrichments dominated by methanotrophic archaea before (Rosseletal.2008; Kellermannetal.2012), nor have they been detected after re-analyzing lipid extracts from the above two studies using the same method in the study (Meadoretal.2015). Two highly abundant MCR variants were detected in Ca. However, the global methane cycle should be reconsidered since the previously unrecognized methane metabolic capacity appears to be present within such a widespread and abundant phylum. Furthermore, bathyarchaeotal members have wide metabolic capabilities, including acetogenesis, methane metabolism, and dissimilatory nitrogen and sulfur reduction, and they also have potential interactions with anaerobic methane-oxidizing archaea, acetoclastic methanogens and heterotrophic bacteria. Obtaining direct physiological evidence for the generation or oxidization of methane by Bathyarchaeota in the future is also important. neut. The isolation source information was parsed from gbk files of bathyarchaeotal 16S rRNA gene sequences. PubChem BioAssay. Thaumarchaeota MG-I was present in the 12C-DNA library in the corresponding zone but was not detected in the 13C-DNA library, suggesting that these microbes are not able to use 13C-acetate (Websteretal.2010). Furthermore, evidence of fatty acid and aromatic compound utilization by Bathyarchaeota has been presented (Mengetal.2014; Evansetal.2015; Heetal.2016); these transformations would be supported by the beta-oxidation pathway and a potential anaerobic aromatic compound degradation pathway. is bathyarchaeota multicellular. Consequently, CO2 appears to be the only electron acceptor mediating AOM, like in a reverse acetoclastic methanogenesis (Hallametal.2004; Wangetal.2014). High-throughput sequencing of the archaeal communities and the analysis of the relationship between the distribution pattern of bathyarchaeotal subgroups and the physicochemical parameters of study sites revealed that sediment depth and sulfate concentration were important environmental factors that shape the distribution of bathyarchaeotal subgroups; Subgroup-8 was shown to be predominantly distributed in the reducing and deeper sediment layers, while Subgroup-10 was preferentially distributed in the relatively more oxidizing and shallow sediment layers (Yuetal.2017).
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