A segregated distribution of bathyarchaeotal subgroups was also observed in the water column and sediments in freshwater karstic lakes (Filloletal.2015). Stahl DA, Flesher B, Mansfield HR 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). Considering the total fractions within all horizons from the sediment cores, members of Bathyarchaeota accounted for 92% of the archaeal community in the Peru Margin Site 1229; 48% in the Peru Margin Site 1227; 71% in volcanic ash layers in the Okhotsk Sea; 47.5% in the forearc basin in the Nankai Trough; 20.6% in the accretionary wedge at the Nankai Trough ODP site 1173; and 83.3% in all layers of the Mediterranean Pleistocene sapropel (Coolenetal.2002; Reedetal.2002; Inagakietal.2003; Newberryetal.2004; Parkesetal.2005; Inagakietal.2006; Teske 2006). This study is also a contribution to the Deep Carbon Observatory. Archaea are abundant in lake sediments [14].Particularly, members of the phylum Bathyarchaeota and the class Thermoplasmata are widespread and considered as core generalists in sediment habitats [], where they have been recognized as key players in the carbon cycle [69].Archaea are also common 2). This approach revealed that the separation of subgroups according to saline and anoxic levels could explain 13% of the phylogenetic lineage variance. 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. Tree building intermediate files are publicly available (https://github.com/ChaoLab/Bathy16Stree). WebBathyarchaeota dominated the archaeal interaction network with 82% nodes, 96% edges, and 71% keystone species. Furthermore, a principal coordinate analysis also clearly separates the bathyarchaeotal community into freshwater and saline sediment groups. JCYJ20170818091727570). The major bathyarchaeotal community comprises Subgroups-1, -8, -12 and -15, and is relatively stable during the hypoxic/oxic change, thus being independent of the sedimentary chemistry change, such as manganese and iron redox cycling during different seasons (Devereuxetal.2015). The concatenated ribosomal protein (RP) alignment contained 12 RPs, and those genomes with <25% RPs were excluded from tree construction. 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. 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). While Subgroups-18 and -19 were named to be consistent with subgroups MCG-18 and MCG-19 as proposed in two previous reports (Lazaretal.2015; Filloletal.2016), Subgroup-20 was renamed to replace the subgroup MCG-19 in Fillol et al.s tree (Filloletal.2016). Oxford University Press is a department of the University of Oxford. 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. The discovery of BchG of archaeal origin in the genomic content of Bathyarchaeota also suggests that an archaeon-based photosynthetic pathway might exist in nature, and that photosynthesis might have evolved before the divergence of bacteria and archaea (Mengetal.2009). In the case of Subgroup-15, which branched away from other groups, MCG242dF would be associated with a relatively low coverage efficiency in the absence of nucleotide mismatches, but high (above 80%) coverage efficiency with 1 or 2 nucleotide mismatches; similarly, MCG678R would be associated with a limited coverage efficiency in the absence of nucleotide mismatches, but the coverage efficiency increases considerably with 1 or 2 nucleotide mismatches. Background Bathyarchaeota, a newly proposed archaeal phylum, is considered as an important driver of the global carbon cycle. In a recent study, Bathyarchaeota and ANME were shown to predominate on the flange of a hydrothermal chimney wall in the Soria Moria Vent field, where the local energy condition favors anaerobic methane oxidizers (Dahleetal.2015). 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. However, the ecological knowledge of Bathyarchaeota is limited in peatland ecosystems. The metabolic properties are also considerably diverse based on genomic analysis (Fig. Bathyarchaeota, reflecting its phylogenetic position as deeply branching with Aigarchaeota and Thaumarchaeota, and its prevalence in subsurface sediments (Mengetal.2014). the potential AOM metabolism of Bathyarchaeota in the flange of the hydrothermal vent would be consistent with the aforementioned genomic inferences (Evansetal.2015). Sousa FL, Neukirchen S, Allen JF et al. 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). (ii) Similar 13C signatures of the archaeal biomass and total organic carbon suggest that the organic matter assimilation contributes to the bulk of the archaeal biomass; the relatively small 13C signature of the archaeal biomass in comparison with the dissolved inorganic carbon suggests that only a small amount of archaeal biomass is derived from autotrophic CO2 fixation (Biddleetal.2006). Their results agree well and reflect the relatively higher bathyarchaeotal fraction in marine sediments with sulfate penetration (>0.15 m below seafloor) (Kuboetal.2012). 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). is bathyarchaeota multicellular. Bathyarchaeota was the most abundant archaeal phylum in most samples, accounting for 13.8164.14% of archaeal sequences (Fig. 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. the classification proposed by Zhou et al. ( 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. (C) The metabolic properties of 24 bathyarchaeotal genomes. Subsequent heterologous expression of bathyarchaeotal Ack revealed that the enzyme can catalyze the biochemical reaction in the direction from acetyl phosphate to acetate, with a higher affinity for the substrates than the products (Heetal.2016). 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). For example, Bathyarchaeota dominates the archaeal community within Louisiana continental shelf (LCS) surface sediment, in both hypoxic and oxic covering water conditions in two distinct seasons (Devereuxetal.2015). In this process, methane is not assimilated by Bathyarchaeota but serves as an energy source. Evans PN, Parks DH, Chadwick GL et al. WebBathyarchaeota are abundant in sediments, and they may involve in sedimentary organic matter degradation, acetogenesis, and, potentially, methane metabolism, based on genomics. A meta-analysis of the distribution of sediment archaeal communities towards environmental eco-factors (7098 archaeal operational taxonomic units from 207 sediment sites worldwide) was performed and a multivariate regression tree was constructed to depict the relationship between archaeal lineages and the environmental origin matrix (Filloletal.2016). The indicator subgroups in saline and freshwater sediments were depicted accordingly. Metagenomic evidence of sulfate reductase-encoding genes in the upper region of SMTZ of the OPD site 1229 provides more hints to the potential synergistic metabolism of AOM coupled with sulfate reduction (Biddleetal.2008). For instance, a study into the stratification of the archaeal community from a shallow sediment in the Pearl River Estuary defined bathyarchaeotal subgroups from MCG-A to -F (Jiangetal.2011), including the NT-A3 group, which is predominantly isolated from the hydrate stability zone in the deep subsurface hydrate-bearing marine sediment core in the Nankai Trough (Reedetal.2002); meanwhile, an investigation of archaeal composition in ca 200 m deep sub-seafloor sediment cores at the offshore Peru Margin ODP sites 1228 and 1229 listed Bathyarchaeota subgroups PM-1 to -8 (Websteretal.2006). 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). 1) (for details see Kuboetal.2012). Three fosmid clones harboring bathyarchaeotal genomic fragments were screened from the South China Sea sediments (05 cm depth) (Lietal.2012). Four genomes (Subgroups-1, -6, -7 and -15) were recovered from the sediment metagenome. Eight subgroups were delineated based on the freshwater/saline segregation, as suggested by the significant IndVal values (P < 0.01) pointing to freshwater/marine sediment distribution. Introduction. FA conc. 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. 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). Furthermore, the MCR complexes found in the BA1 and BA2 genomes are phylogenetically divergent from traditional MCR and they coevolved as a whole functional unit, indicating that methane metabolism began to evolve before the divergence of the Bathyarchaeota and Euryarchaeota common ancestors (Evansetal.2015). These archaeal groups are the phylogenetically closest ones to the protoeukaryote that served as the mitochondrion-acquiring host; this gave rise to a hydrogen hypothesis that explains their hydrogen-dependent metabolism to address the mitochondrion acquisition and subsequent endosymbiont processes. 2. The Bathyarchaeota formerly known as the Miscellaneous Crenarchaeotal Group is an evolutionarily diverse group of microorganisms found in a wide range of 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). The versatile metabolic properties of Bathyarchaeota, including acetogenesis, methane cycling, potential photosynthesis, and dissimilatory nitrite and sulfate reduction, etc., indicate that their ecological and phylogenetic characteristics are quite diverse, and given their basal phylogenetic position at the root of archaea, the evolutionary paths of those capabilities are also of great meaning for understanding the evolution of early life (Evansetal.2015; Heetal.2016; Lazaretal.2016; Zhangetal.2016). Barns SM, Delwiche CF, Palmer JD et al. Moreover, with the rapid development and application of 16S rRNA-based high-throughput sequencing techniques for microbial ecological profiling, and 16S rRNA-independent microbial metagenomic profiling that avoids the issue of polymerase chain reaction (PCR) primer bias, a much clearer distribution pattern of diverse bathyarchaeotal subgroups can be expected; at the same time, higher resolution of local physicochemical characteristics will facilitate classification of ecological niches of bathyarchaeotal subgroups into more detailed geochemical categories. Primers and probes for molecular detection and quantification of Bathyarchaeota subgroups. Phylogenetic analyses of 16S rRNA gene sequences were inferred by Maximum Likelihood implemented in RAxML 8.0 on the CIPRES Science Gateway using the GTR+GAMMA model and RAxML halted bootstrapping automatically (Miller, Pfeiffer and Schwartz 2010; Stamatakis 2014). 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. This is the first ever genomic evidence for homoacetogenesis, the ability to solely utilize CO2 and H2 to generate acetate, in an archaeal genome and of distinct archaeal phylogenetic origin other than that of Bacteria (Heetal.2016). The production of a putative 4-carboxymuconolactone decarboxylase was evident when the mangrove sediments were supplemented with protocatechuate, further suggesting the capacity of certain bathyarchaeotal members to degrade aromatic compounds (Mengetal.2014). For us, phenotypical and genotypical information on subgroups whose existing patterns have only been sporadically reported still remains elusive and more explicit investigations are lacking. The 13C-depleted nature of butanetriol dibiphytanyl glycerol tetraethers found in the study implied that members of Bathyarchaeota might be autotrophs or fueled by 13C-depleted organic substrates (Meadoretal.2015). The BA2 (Subgroup-8) genome contains MCR-encoding genes and additional genes of typical methane metabolism, like BA1, reflecting a similar methylotrophic methanogenesis activity. The members of the Bathyarchaeota are the most abundant archaeal components of the transitional zone between the freshwater and saltwater benthic sediments along the Pearl River, with a central position within the co-occurrence network among other lineages (Liuetal.2014). Meanwhile, the ability to utilize a wide variety of substrates could have allowed Bathyarchaeota to avoid a direct competition with other substrate specialists, such as methanogens and sulfate reducers; in contrast, organic matter degradation to generate acetate might be more energetically favorable for Bathyarchaeota than for other bacterial acetogens, as the former do not need to invest in ATP to activate formate; subsequently, Bathyarchaeota plays the role of active carbon transformers, especially in the subsurface sediments, to fuel the heterotrophy and acetoclastic methanogenesis processes and facilitate coupled carbon cycling (Fig. The emergence of freshwater-adapted lineages, including freshwater-indicative Subgroups-5, -7, -9 and -11, occurred after the first salinefreshwater transition event (Filloletal.2016). 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 exclusive archaeal origin of the Ack-Pta homoacetogenesis pathway is different from other archaeal acetogenesis systems but shares functional similarity with its bacterial origin counterparts, although it is phylogenetically divergent (Heetal.2016). WebHome Business Account Form is bathyarchaeota multicellular. 2012 ). Fillol M, Auguet J-C, Casamayor EO et al. No bathyarchaeotal species have as yet been successfully cultured in pure cultures, despite their widespread distribution in the marine, terrestrial and limnic environments (Kuboetal.2012), which hampers their direct physiological characterization. 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). 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). 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. This could be explained by the versatile pathways of organic matter assimilation present in the majority of Bathyarchaeota, reflected by inferences from genomic data. 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 (2015) presumed the syntrophy between Bathyarchaeota and sulfate-reducing bacteria (SRB) toward anaerobic oxidation of methane (AOM) (Evansetal.2015). The deduced last common ancestor of Bathyarchaeota might be a saline-adapted organism, which evolved from saline to freshwater habitats during the diversification process, with the occurrence of few environmental transitional events. Phylogenetic tree of bathyarchaeotal 16S rRNA genes. Some Bathyarchaeota ASVs showed close interaction with 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. Results In the current study, nine 3) (Lloydetal.2013; Evansetal.2015; Lazaretal.2015; Heetal.2016; Lazaretal.2016; Lever 2016). Candidatus Bathyarchaeota Click on organism name to get more information. Capella-Gutirrez S, Silla-Martnez JM, Gabaldn T. Coolen MJL, Cypionka H, Sass AM et al. 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. Zhichao Zhou, Jie Pan, Fengping Wang, Ji-Dong Gu, Meng Li, Bathyarchaeota: globally distributed metabolic generalists in anoxic environments, FEMS Microbiology Reviews, Volume 42, Issue 5, September 2018, Pages 639655, https://doi.org/10.1093/femsre/fuy023. 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). 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). 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). 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. The incorporation of 13C-bicarbonate into the archaeal lipids (potential bathyarchaeotal-specific biphytanes) was significantly observed only with lignin addition. Several pre-/non-enriched sediment cultures afforded preliminary evidence for the trophic properties and metabolic capacities of Bathyarchaeota. (2008) further summarized 47 clone libraries of 16S rRNA genes from the marine subsurface, with Bathyarchaeota accounting for 33% of all archaea. In contrast, Subgroup-15 (Crenarchaeota group C3) organisms dominate cDNA libraries from all sediment layers, albeit with minor contribution to the corresponding DNA libraries; this indicates that this group is metabolically active in the benthic euxinic, organic-rich sediments of karstic lakes (Filloletal.2015). According to the meta-analysis of archaeal sequences available in the ARB SILVA database (Kuboetal.2012), Bathyarchaeota was further recognized as a group of global generalists dwelling in various environments, including marine sediments, hydrothermal vents, tidal flat and estuary sediments, hypersaline sediments, terrestrial subsurface, biomats, limnic water and sediments, underground aquifers, hot springs, soils, municipal wastewaters, animal digestive tract, etc. 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. Subgroups were assigned from the corresponding 16S rRNA gene phylogenic 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 colonization of land, Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru, Metagenomic signatures 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