Along with the widespread distribution of Bathyarchaeota, i.e. During the enriching process with lignin addition, the Subgroup-8 abundance climbed over 10 times compared with the initial stage and became the most dominant archaeal species. The metagenomic binning of WOR estuarine sediment DNA led to the reconstruction of draft genomes of four widespread Bathyarchaeota, with the genome completeness in the range of 4898% (Lazaretal.2016). Some Bathyarchaeota ASVs showed close interaction with This suggests that methane metabolism might have evolved before the divergence of the ancient archaeal lineages of Bathyarchaeota and Euryarchaeota, in agreement with the assumption that methanogenesis might represent one of the earliest metabolic transformations (Battistuzzi, Feijao and Hedges 2004; Ferry and House 2006; Evansetal.2015; Lloyd 2015). Some of these Crenarchaeota were able to assimilate all 13C-organic compounds tested, including acetate, glycine, urea, simple biopolymers (extracted algal lipids) and complex biopolymers (ISOGRO), while others were only detected in specific substrates (acetate or urea). 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. the potential AOM metabolism of Bathyarchaeota in the flange of the hydrothermal vent would be consistent with the aforementioned genomic inferences (Evansetal.2015). Peat MCG group was represented with one sequence at 90% cutoff level (Xiangetal.2017). 4), although these might not necessarily exist in all bathyarchaeotal subgroups (Fig. pl. Interestingly, one of the highly abundant McrA subunits of Ca. 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). 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 model based on the thermodynamic considerations of chemicals and temperatures may be used to offer a framework linking the distribution of microbial groups and energy landscapes (Amendetal.2011; LaRowe and Amend 2014; Dahleetal.2015). However, after allowing for a single nucleotide mismatch, the coverage efficiency markedly increased, to around 8090%. S. butanivorans forms a distinct cluster with those of Bathyarchaeota origin, separately from other methanogens and methanotrophs (Laso-Prezetal.2016). To alleviate the nomenclature confusion, we constructed an updated RAxML tree (Fig. S. butanivorans protein extracts; they are probably responsible for the initial step of butane activation to generate butyl-CoM. (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. First, successful enrichment methods that would allow harvesting sufficient bathyarchaeotal biomass to explore their physiological and genomic characteristics have not yet been established. The phylogenetic species variability index, which reflects the phylogenetic relatedness of sequences originating from specific environments, suggests a non-random distribution of Bathyarchaeota assemblages in natural environments (Filloletal.2016). All assigned subgroups have minimum intra-group >90%, and are clustered into one clade with previously reported anchor sequences (Kuboetal.2012). Among these are Subgroups-1 and -8 with high IndVal values in marine sediments, and Subgroups-5 and -11 with high IndVal values in fresh sediments (Filloletal.2016). 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). 3A). Bathyarchaeota is characterized by high intragroup diversity, with most subgroups showing within-sequence similarity <92% (Kuboetal.2012; Filloletal.2016). 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. Bathyarchaeotal SAGs also encode pathways for the intracellular breakdown of amino acids. 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). After incubation with 13C-acetate, the archaeal population within a sulfate reduction zone, detected on the basis of 13C-DNA, was almost entirely dominated by Bathyarchaeota (65% by Subgroup-8 and 30% by Subgroup-15) (Websteretal.2010). Future efforts should be encouraged to address the fundamental issues of the diversity and distribution patterns of Bathyarchaeota, and their vital roles in global carbon cycling. Candidatus Bathyarchaeota Click on organism name to get more information. Subgroups were assigned from the corresponding 16S rRNA gene phylogenic tree (Fig. 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. However, according to the genomic information on most archaeal acetogens and bathyarchaeotal genomic bins obtained by Lazaretal. WebGiven the wide environmental and phylogenetic diversity of Bathyarchaeota, additional genomes are required to understand the metabolic capabilities of this understudied Background Bathyarchaeota, a newly proposed archaeal phylum, is considered as an important driver of the global carbon cycle. In addition, some regions of the bathyarchaeotal genome might have been acquired from bacteria because of the aberrant tetranucleotide frequency in the genomic fragments of Bathyarchaeota and bacterial phylogenetic origins of these genomic fragments (Lietal.2012). Abstract. Given that they are abundant, globally distributed and phylogenetically diverse, continued exploration of new potential bathyarchaeotal subgroups is encouraged. 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). A detailed knowledge of the phylogenetic structure of the Bathyarchaeota phylum is crucial for the understanding of their ecological significance in global sedimentary processes. Lomstein BA, Langerhuus AT, DHondt S et al. The incorporation of 13C-bicarbonate into the archaeal lipids (potential bathyarchaeotal-specific biphytanes) was significantly observed only with lignin addition. 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. Metabolic pathways of the These physiological, ecological and evolutionary features place Bathyarchaeota in the spotlight of current microbial ecology studies, encouraging further explorations of their impact on global and local biogeochemical carbon cycling. Boetius A, Ravenschlag K, Schubert CJ et al. Barns SM, Delwiche CF, Palmer JD et al. The emergence of freshwater-adapted lineages, including freshwater-indicative Subgroups-5, -7, -9 and -11, occurred after the first salinefreshwater transition event (Filloletal.2016). Metagenomic sequencing of fracture fluid from South Africa recovered a nearly complete " Candidatus Bathyarchaeota" archaeon genome. 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). Oxford University Press is a department of the University of Oxford. The current genomic and physiological information of these subgroups also suggests their potential ecological strategies and functions in specific habitats, further highlighting their important roles in global biogeochemical cycling (Xiangetal.2017). In the White Oak River estuary, the abundance of Bathyarchaeota decreases with decreasing reductive redox conditions of the sediment (Lazaretal.2015). 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). Td stands for dissociation temperature for RNA slot-bolt. These results have not only demonstrated multiple and important ecological functions of this archaeal phylum, but also paved the way for a detailed understanding of the evolution and metabolism of archaea as such. 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 of the Peru Margin subseafloor biosphere show a genetically distinct environment, A 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fractionation associated with methylotrophic methanogenesis, Archaeal diversity in waters from deep South African gold mines. This primer pair shows good specificity toward Bathyarchaeota; it allowed amplification of 10100 times more bathyarchaeotal 16S rRNA gene sequences from the sediment samples from the South China Sea, and the Atlantic and Antarctic Oceans than the MCG242dF/MCG678R primers (Yuetal.2017). 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 (2015) presumed the syntrophy between Bathyarchaeota and sulfate-reducing bacteria (SRB) toward anaerobic oxidation of methane (AOM) (Evansetal.2015). WebEtymology: Gr. The Subgroups-1, -6 and -15 genomes also encoded the methyl glyoxylate pathway, which is typically activated when slow-growing cells are exposed to an increased supply of sugar phosphates (Weber, Kayser and Rinas 2005). 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). Regarding the functional properties, metabolic pathway analysis revealed that BA1 is a peptide and glucose fermenter, while BA2 is a fatty-acid oxidizer (Evansetal.2015). Specific lipids, exclusively synthesized by certain archaea, can serve as a supplementary biomarker for tracing the existence and abundance of targeted archaeal groups; their isotopic composition can be used to indicate specific carbon acquisition pathways (Schouten, Hopmans and Damste 2013). In a recent global evaluation of the archaeal clone libraries from various terrestrial environmental settings, permutational analysis that tested the relationship between Bathyarchaeota and environmental factors suggested that salinity, total organic carbon and temperature are the most influential factors impacting community distribution across different terrestrial habitats (Xiangetal.2017). the census of energy availability for redox reactions, is used, to some extent, to constrain and predict the distribution of functional groups of chemotrophic microorganisms (Amendetal.2011; LaRowe and Amend 2014). This was confirmed by a permutational analysis of variance, with salinity as the best explanatory variable for the variance within the bathyarchaeotal community (R2 = 0.04, P < 0.001) (Filloletal.2016). 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). Genomic characterization and metabolic potentials of Bathyarchaeota. 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. Based on the physiological and genomic evidence, acetyl-coenzyme A-centralized heterotrophic pathways of energy conservation have been proposed to function in Bathyarchaeota; these microbes are able to anaerobically utilize (i) detrital proteins, (ii) polymeric carbohydrates, (iii) fatty acids/aromatic compounds, (iv) methane (or short chain alkane) and methylated compounds, and/or (v) potentially other organic matter. More recently, the proposed genus Candidatus Syntrophoarchaeum was shown to be able to anaerobically oxidize butane in a manner similar to ANME oxidation of methane, by reverse methanogenesis, a process that is initially mediated by MCR (Laso-Prezetal.2016). PubChem BioAssay. 1) (for details see Kuboetal.2012). 4) (Evansetal.2015; Heetal.2016; Lazaretal.2016). The branching order of Subgroups-13 to -17 was unstable when analyzed by different tree-construction methods, and they were presented as multifurcated branches. Given the substrate specificity of this MCR type in utilizing butane instead of methane, and amino acid divergence of this MCR type from its methane metabolizing related counterparts, it is possible that the MCR clusters in some members of Bathyarchaeota are responsible for butane oxidation instead of methane metabolism (Laso-Prezetal.2016). Bathyarchaeotal 16S rRNA gene sequences were collected from SILVA SSU database version 128 (sequences of Bathyarchaeota and Group C3; >750 bp) and sequences from pervious publications (Kuboetal.2012; Lazaretal.2015; Filloletal.2016; Heetal.2016; Xiangetal.2017). 3B). Institute for Advanced Study, Shenzhen University, Shenzhen 518060, People's Republic of China, Laboratory of Environmental Microbiology and Toxicology, School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong SAR, People's Republic of China. The wide phylogenetic coverage increases the difficulty of inferring the general metabolic properties across whole lineages. Because of their high sequence coverage and bathyarchaeotal sequence specificity, MCG528 and MCG732 primers are recommended for the detection and quantification of Bathyarchaeota (Kuboetal.2012); nevertheless, this primer pair is not suitable for quantifying Bathyarchaeota in freshwater columns and sediments (Filloletal.2015). Lineage (full): cellular organisms; Archaea; TACK group. (i) The 13C signature of the archaeal biomass suggests that only a small fraction of local archaea in SMTZ utilize methane, which might be explained by the contribution of Bathyarchaeota in the biomass; until now, only one line of evidence points to the acquisition of methane metabolism by Bathyarchaeota (Lloydetal.2013; Evansetal.2015; Lazaretal.2015; Heetal.2016). 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). Low collinear regions were found between bathyarchaeotal and reported archaeal genomic fragments, suggesting that the gene arrangement of Bathyarchaeota is distinct from that of sequenced archaea. The identification of key genes of the MCR complex (mcrA, mcrB and mcrG), and the presence of hdrABC and mcvhADG responsible for the cycling of coenzyme M (CoM) and coenzyme B (CoB), suggest their role in the methanogenesis machinery that mediates the CoM-S-S-CoB cycling, similar to Euryarchaeota methanogens (Evansetal.2015). The archaeal phylum Bathyarchaeota, which is composed of a large number of diverse lineages, is widespread and abundant in marine sediments. Details of markers refer to Supplementary Table S1 available online. In terms of energy metabolism, these archaea contain the WoodLjungdahl pathway, capable of generating acetyl-CoA autotrophically by CO2 and H2. 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. 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). They include Euryarchaeota, and members of the DPANN and Asgard archaea. 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). (A) Phylogenetic tree of ribosomal proteins obtained from currently available bathyarchaeotal genomes (from GenBank, 29 November 2017 updated). 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. Bathyarchaeota, reflecting its phylogenetic position as deeply branching with Aigarchaeota and Thaumarchaeota, and its prevalence in subsurface sediments (Mengetal.2014). 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). Obtaining direct physiological evidence for the generation or oxidization of methane by Bathyarchaeota in the future is also important. their relatively high abundance in the global marine subsurface ecosystem (Kuboetal.2012; Lloydetal.2013), they are also metabolically active in the subsurface sediments across geological time scales. Genes responsible for the dissimilatory nitrite reduction to ammonium (nirB and nrfD) were identified in Subgroups-1, -17 (formally Subgroup-7/17), -6 and -15, respectively, suggesting the potential existence of a respiratory pathway involving nitrite reduction (Lazaretal.2016).
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