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). adj. The subgroups MCG-18, -19 and -20 were firstly named in Lazar et al.s study, but only MCG-19 was represented in the phylogenetic tree (Lazaretal.2015). The archaeal phylum Bathyarchaeota, which is composed of a large number of diverse lineages, is widespread and abundant in marine sediments. The central product, acetyl-CoA, would either (i) be involved in substrate-level phosphorylation to generate acetate and ATP, catalyzed by an ADP-forming acetyl-CoA synthase as in other peptide-degrading archaea; (ii) be metabolized to generate acetate through the Pta-Ack pathway, similarly to bona fide bacterial homoacetogens; or (iii) be utilized for biosynthesis, e.g. 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. Thus, this systematic nomenclature based on clear monophyletic or phylogenetically stable subgroups not only facilitates further sequence assignment, but also provides useful information for understanding the evolutionary separation of specific lineages subjected to natural selection (Filloletal.2016). Subgroup-5 thrives in the euxinic bottom water layer, characterized as anoxic and sulfide-rich, with accumulated inorganic and organic reduced compounds; Subgroup-6 is a group of generalists that are adapted to both planktonic and sediment habitats with a wide range of sulfidic conditions. The product, acetate, would then be used by acetate-consuming SRB to benefit the thermodynamic efficiency of AOM. Primers and probes for molecular detection and quantification of Bathyarchaeota subgroups. On the other hand, the proportion of bathyarchaeotal sequence in the total archaeal community sequence increases with depth, and they may favor anoxic benthic sediments with iron-reducing conditions. Devereux R, Mosher JJ, Vishnivetskaya TA et al. Some Bathyarchaeota ASVs showed close interaction with 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). A subsequent heterologous expression and activity assays of the bathyarchaeotal acetate kinase gene ack demonstrated the ability of these bathyarchaeotal members to grow as acetogens. 3). The Subgroup-15 genome contained genes encoding extracellular peptidases, consistent with previous findings for this subgroup (Lloydetal.2013); however, other bathyarchaeotal subgroups lack genes responsible for extracellular protein degradation, suggesting that they can only utilize small amino acids or oligopeptides, as suggested by their genomes. 3B). 2) based on currently available bathyarchaeotal 16S rRNA gene sequences from SILVA SSU 128 by adding the information from pervious publications (Kuboetal.2012; Lazaretal.2015; Filloletal.2016; Heetal.2016; Xiangetal.2017). In terms of energy metabolism, these archaea contain the WoodLjungdahl pathway, capable of generating acetyl-CoA autotrophically by CO2 and H2. The potential AOM metabolic capacity of Bathyarchaeota could help to fully address the isotopic relationship between the archaeal biomass and the ambient environmental carbon pools, as follows. In total, 17 subgroups with 76% similarity shared by the most remote sequences were designated; however, 12% of all sequences remained ungrouped. (2018) described a predominance of the phylum Bathyarchaeota (now class Bathyarchaeia from phylum Crenarchaeota) in mid-latitude estuaries, However, their life strategies have remained largely elusive. Since these two genomic bins represent only a small fraction of all bathyarchaeotal lineages, and no evidence of methanogenic machinery is apparent in the recent parallel genomic binning data, the ability to metabolize methane might not be shared by all subgroup lineages (Lloydetal.2013; Mengetal.2014; Heetal.2016; Lazaretal.2016). 1 and Table S 5 ), and the average proportion of Bathyarchaeota in the mangrove sediments (43.32%, sd = 0.106) was significantly higher than that in the mud flat sediments (36.47%, sd = 0.084) ( p < The currently available bathyarchaeotal genomes shared 63.5% similarity on average, indicating a wide phylogenetic diversity at the genome scale (Fig. 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). Genomic inferences from the two reconstructed bathyarchaeotal genomic bins from the coal-bed methane wells suggest that some Bathyarchaeota are methylotrophic methanogens feeding on a wide variety of methylated compounds, possessing an additional ability to ferment peptides, glucose and fatty acids (Evansetal.2015). Metabolic versatility of freshwater sedimentary archaea feeding Furthermore, in contrast to the consistent vertical distribution of all archaeal lineages in freshwater sediments with almost no abundance changes, the total abundance of all Bathyarchaeota and the fraction of Subgroup-15 increase along with the depths of sediments, with significantly high abundance within the archaeal community (Liuetal.2014). Bathyarchaeota: globally distributed metabolic Hallam SJ, Putnam N, Preston CM et al. Subgroups were assigned from the corresponding 16S rRNA gene phylogenic tree (Fig. It also contains typical methane metabolism genes (hdrABC and mvhADG) but lacks hdrE, similar to Methanomassiliicoccales genomes (Evansetal.2015). Biddle JF, Fitz-Gibbon S, Schuster SC et al. Reconsideration of the potential methane-oxidizing contribution of Bathyarchaeota would refine the congruency between the predicted and observed microbial communities, i.e. (Fig. 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). S. butanivorans protein extracts; they are probably responsible for the initial step of butane activation to generate butyl-CoM. Phylogenetic analysis of the Pta and Ack coding sequences in He et al.s study revealed that these genes form a monophyletic clade and are different from all other know sequences, indicating that they evolved independently of the currently known bacterial counterparts (Heetal.2016). The diversity of bathyarchaeotal community turns out to be similar in the four cultivation treatments (basal medium, addition of an amino acid mix, H2-CO2 headspace and initial aerobic treatment). This will have a profound impact not only on deciphering the metabolic properties of Bathyarchaeota, by using butanetriol dibiphytanyl glycerol tetraethers as biomarkers to trace carbon acquisition by isotopic labeling, but also by representing their pivotal contribution, associated with their global abundance, to biogeochemical carbon cycling on a large ecological scale. Vertical Distribution of Bathyarchaeotal Communities in 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). Members of Bathyarchaeota are able to use CO2 and H2 from natural sources and fermentation products to fuel acetogenesis (Heetal.2016; Martinetal.2016). Members of the archaeal phylum Bathyarchaeota are widespread and abundant in the energy-deficient marine subsurface sediments. Hence, Bathyarchaeota acquired the core heterotrophic metabolic capacity for processing complex carbohydrates, and an additional ability to utilize peptides and amino acids, as suggested before (Seyler, McGuinness and Kerkhof 2014). Metagenomic sequencing of fracture fluid from South Africa recovered a nearly complete " Candidatus Bathyarchaeota" archaeon genome. The group was termed miscellaneous because of its occurrence in diverse habitats; it is not only abundant in marine sediments but is also widely distributed in terrestrial, freshwater, hot spring, hydrothermal, etc., environments (Kuboetal.2012). Newberry CJ, Webster G, Cragg BA et al. Considering that the marine subseafloor environment is one of the largest reservoirs of the prokaryotic biomass on Earth, with an estimated microbial abundance of 2.9 1029 cells and harboring ca 9.131.5% of all prokaryotes on Earth (Kallmeyeretal.2012), the predominance and activity of Bathyarchaeota in the marine subsurface sediments indicates that these microbes might play a crucial role in global biogeochemical nutrient cycling. In a recent study exploring the stratified distribution of archaeal groups in a tropical water column, the analysis of archaeal 16S rRNA community distribution was combined with isoprenoid glycerol dialkyl glycerol tetraether lipid abundance information to reveal that glycerol dibiphytanyl glycerol tetraether lacking the cyclopentane rings [GDGT(0)] likely originated from the Bathyarchaeota-enriched layer in the water column (Bucklesetal.2013). Bathyarchaeota possesss a bona fide homoacetogenesis pathway of archaeal phylogenetic origin, as confirmed by functional studies, indicating a distinct evolutionary pathway of acetogenesis in archaea, different from horizontal transfer from bacteria (Heetal.2016). A group called Peat MCG (pMCG) (Xiangetal.2017) was also listed on the tree; however, because there was only one represented sequence after dereplication at 90% similarity of all bathyarchaeotal 16S rRNA gene sequences, we did not list pMCG as a separate subgroup in this tree (Fig. The archaeal community structure, including Bathyarchaeota, is not correlated with a general geochemical categorization, but with the depth and sulfate concentration, subsequently linking to the redox potential, age and the (increasing) degree of organic matter recalcitrance. It is well known that isoprenoid glycerol dialkyl glycerol tetraether lipids are specifically synthesized by archaea. (A) Phylogenetic tree of ribosomal proteins obtained from currently available bathyarchaeotal genomes (from GenBank, 29 November 2017 updated). Methane would be oxidized in a stepwise manner to methyl-tetrahydromethanopterin (CH3-H4MPT); the methyl group of CH3-H4MPT and CO2 would then be subjected to a CO dehydrogenase/acetyl-CoA synthase (CODH/ACS complex); CO2 would be fixed by a reverse CO dehydrogenation to CO, and then coupled with a methyl group and CoA to generate acetyl-CoA; ATP would be generated in the course of substrate-level phosphorylation from ADP, with one acetate molecule simultaneously generated by a reverse ADP-forming acetyl-CoA synthase. Given that they are abundant, globally distributed and phylogenetically diverse, continued exploration of new potential bathyarchaeotal subgroups is encouraged. The isolation source information was parsed from gbk files of bathyarchaeotal 16S rRNA gene sequences. 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. 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. Bathyarchaeotal SAGs also encode pathways for the intracellular breakdown of amino acids. Community, Distribution, and Ecological Roles Characterization of Bathyarchaeota genomes assembled from First, successful enrichment methods that would allow harvesting sufficient bathyarchaeotal biomass to explore their physiological and genomic characteristics have not yet been established. Background Bathyarchaeota, a newly proposed archaeal phylum, is considered as an important driver of the global carbon cycle. This review summarizes the recent findings pertaining to the ecological, physiological and genomic aspects of Bathyarchaeota, highlighting the vital role of this phylum in global carbon cycling. Callac N, Rommevaux-Jestin C, Rouxel O et al. The Bathyarchaeota formerly known as the Miscellaneous Crenarchaeotal Group is an evolutionarily diverse group of microorganisms found in a wide In addition, the catalyzed reporter deposition-fluorescent in situ hybridization (CARD-FISH) studies for the detection and quantification of bathyarchaeotal cells suggest that they are abundant in the center and marine invertebrate-inhabited layers in the Haakon Mosby Mud Volcano, and in the marine subsurface sediments in the Equatorial ODP site 1125 and Peru Basin ODP site 1231 (Kuboetal.2012). Based on the lineage distribution pattern analysis of the archaeal community of seven major eco-niches, it is also evident that the different evolutionary lineages are habitat-specific, and salinity rather than temperature is the primary driving force of the variation of global archaea distribution, with a similar pattern also evident for the global bacterial distribution (Lozupone and Knight 2007; Auguet, Barberan and Casamayor 2010). These findings expand the metabolic potential of archaea and argue for a revision of the role of archaea in the carbon cycle in marine sediments (Heetal.2016). 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). Diversity, metabolism and cultivation of archaea 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. However, after allowing for a single nucleotide mismatch, the coverage efficiency markedly increased, to around 8090%. 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). Summary. Bathyarchaeota, a recently proposed archaeal phylum, is globally distributed and highly abundant in anoxic sediments. All sequences were aligned using SINA v1.2.11 (vision 21227) with SSU ARB database version 128, and poorly aligned columns (gaps in 50% or more of the sequences) were deleted by using trimAl v1.4.rev15 (Ludwigetal.2004; Capella-Gutirrez, Silla-Martnez and Gabaldn 2009; Pruesse, Peplies and Gloeckner 2012). Viral Host. Future experiments investigating substrate specificity of these proteins and analyses of the intermediate metabolites will help establish their actual functions. Genomic and enzymatic evidence for acetogenesis among The evidence for the presence of respiratory metabolism in other bathyarchaeotal subgroups is ambiguous although it cannot be excluded (Lazaretal.2016). The first two separation nodes representing the hypersaline, saline and fresh environments accounted for 9.1% of the total phylogenetic lineage variance. Along with the widespread distribution of Bathyarchaeota, i.e. Microbial communities of deep marine subsurface sediments: molecular and cultivation surveys, Methanogenic archaea: ecologically relevant differences in energy conservation, Methylotrophic methanogenesis discovered in the archaeal phylum, Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways, Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru Margin, Prokaryotic functional diversity in different biogeochemical depth zones in tidal sediments of ?the Severn Estuary, UK, revealed by stable-isotope probing, Enrichment and cultivation of prokaryotes associated with the sulphate-methane transition zone of diffusion-controlled sediments of Aarhus Bay, Denmark, under heterotrophic conditions, The physiology and habitat of the last universal common ancestor, Distribution of Bathyarchaeota communities across different terrestrial settings and their potential ecological functions, Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences, A large-scale evaluation of algorithms to calculate average nucleotide identity, High occurrence of Bathyarchaeota (MCG) in the deep-sea sediments of South China Sea quantified using newly designed PCR primers, Growth of sedimentary Bathyarchaeota on lignin as an energy source, Genomic and transcriptomic evidence for carbohydrate consumption among microorganisms in a cold seep brine pool, This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (, Illuminating the Oral Microbiome and its Host Interactions: Animal models of disease, Engineering lanthipeptides by introducing a large variety of RiPP modifications to obtain new-to-nature bioactive peptides, Meat fermentation at a crossroads: where the age-old interplay of human, animal, and microbial diversity and contemporary markets meet, Incorporation, fate, and turnover of free fatty acids in cyanobacteria, Ruminococcus gnavus: friend or foe for human health, About the Federation of European Microbiological Societies, GLOBAL DISTRIBUTION AND HIGH DIVERSITY OF BATHYARCHAEOTA, DISTRIBUTION PATTERN AND MOLECULAR DETECTION, PHYSIOLOGICAL AND GENOMIC CHARACTERIZATION, ECOLOGICAL FUNCTIONS AND EVOLUTION OF BATHYARCHAEOTA, https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model, Receive exclusive offers and updates from Oxford Academic, Copyright 2023 Federation of European Microbiological Societies. 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). Bathyarchaeota is of great interest to microbial ecologists for its wide distribution, high abundance, and diversity, as well as its potential ability to degrade detrital organic matter in aquatic environments and drive global elements cycling . It has been suggested that Bathyarchaeota is one of the cosmopolitan groups frequently detected in the freshwater and marine sediments (68% of all sediments analyzed), accounting for a large proportion of the sediment microbial communities (average 36 22%) (Filloletal.2016). Three fosmid clones harboring bathyarchaeotal genomic fragments were screened from the South China Sea sediments (05 cm depth) (Lietal.2012). 4), although these might not necessarily exist in all bathyarchaeotal subgroups (Fig. A detailed knowledge of the phylogenetic structure of the Bathyarchaeota phylum is crucial for the understanding of their ecological significance in global sedimentary processes. The incorporation of 13C-bicarbonate into the archaeal lipids (potential bathyarchaeotal-specific biphytanes) was significantly observed only with lignin addition. In this study, the abundance and Amend JP, McCollom TM, Hentscher M et al. The wide availability of buried organic matter in the marine subsurface would favor the heterotrophic feeding of Bathyarchaeota. In one study, small amounts of stable isotope-labeled substrates, including glucose, acetate and CO2, were introduced multiple times into slurries from different biogeochemical depths of tidal sediments from the Severn estuary (UK) to better reflect the in situ environmental conditions (Websteretal.2010). Here we reported the abundance of Bathyarchaeota members across different ecosystems and their correlation with environmental factors by constructing 16S A complete set of active sites and signal sequences for extracellular transport is also encoded by bathyarchaeotal SAGs (Lloydetal.2013). Thauer RK, Kaster A-K, Seedorf H et al. Subgroup-6 persists in such suboxic, sulfide-depleted shallow sediment layers, while Subgroups-1, -5 and -8 preferentially occur in deeper, more reducing subsurface layers (Lazaretal.2015). Further membrane lipid characterization of enriched or pure bathyarchaeotal cultures will help to validate this discovery. ( 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. It is evident that the phylogenetically diverse subgroups are heterotrophs with metabolism centralized around acetyl-CoA generation. 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). 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). Similarly, rRNA slot blot hybridization indicates the existence of functionally active Bathyarchaeota not only in the surface and subsurface sediments from the Nyegga site 272-02, Cascadia Margin, Gulf of Mexico, Hydrate Ridge ODP site 1245 and Janssand (North Sea), but also in the oxic mats in the Arabian Gulf and subsurface White Oak River sediments (Kuboetal.2012). Bathyarchaeia occurrence in rich methane sediments from Recently, another meta-analysis using newly acquired global sediment bathyarchaeotal sequences resulted in the addition of two more subgroups, Subgroups-18 and -19, with high bootstrap supporting values (96% and 86%, respectively) (Filloletal.2016). Among the presently recognized 25 bathyarchaeotal subgroups, eight are delineated as significantly niche-specific based on their marine/freshwater segregation. (2016), it appears that these microbes rely on the acetyl-CoA synthetase (Acd) to generate acetate (Heetal.2016). It has been proposed that the deduced last common ancestor was most likely a saline-adapted organism, and the evolutionary progression occurred most likely in the saline-to-freshwater direction, with few environmental transitional events. Because of the universal distribution and predominance of Bathyarchaeota, not only in the marine sediments but also in terrestrial sediments and various other eco-niches, and because of their versatile metabolism (including acetogenesis, methane metabolism, and dissimilatory nitrate and sulfate reduction) and potential interactions with ANME archaea, acetoclastic methanogens and heterotrophic bacteria, the ecological importance of this group of generalists has entered the limelight and needs further exploration. Taxonomy browser (Candidatus Bathyarchaeota) - National Characteristics of the Bathyarchaeota community in Currently available bathyarchaeotal genomes (from GenBank, 29 November 2017 updated) with 16S rRNA gene sequences were labeled in the tree. stands for formamide concentration in the hybridization buffer (%, vol/vol). The IndVal species with statistical support in terrestrial environments indicated by this study were pMCG and Subgroup-5b in peat; Subgroup-5a in hot springs; Subgroup-6 in the soil; Subgroups-3, -4, -13 and -16 in estuaries; and Subgroup-15 in mangroves. 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. Search for other works by this author on: State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, People's Republic of China, State Key Laboratory of Ocean Engineering, Shanghai Jiao Tong University, Shanghai, People's Republic of China, Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types, Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system, Global ecological patterns in uncultured Archaea, Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences, A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the 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anaerobic oxidation of methane: new insights in microbial ecology and biogeochemistry, Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk, Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin, Archaeal tetraether bipolar lipids: Structures, functions and applications, Stratification of Archaeal communities in shallow sediments of the Pearl River Estuary, Southern China, Global distribution of microbial abundance and biomass in subseafloor sediment, BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences, Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities, Anaerobic oxidation of methane: progress with an unknown process, Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments, CARD-FISH for 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