The members of Bathyarchaeota were positively and strongly correlated especially with the acetoclastic Methanosaeta; however, the second most abundant archaeal group, MG-I (subordinate to Thaumarchaeota) is negatively correlated with other groups, probably indicating segregation corresponding to two distinct lifestyles in this case (Liuetal.2014). Y He, et al., Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 1, 16035 (2016). L Jiang, Y Zheng, J Chen, X Xiao, F Wang, Stratification of achaeal communities in shallow sediments of the Pearl River Estuary, Southern China. 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 < Subgroups were assigned from the corresponding 16S rRNA gene phylogenic tree (Fig. Bathyarchaeota occupied about 60% of the total archaea in the Jiulong River, China (Li et al. Ancestral state reconstruction was used to estimate the diversification of bathyarchaeotal lineages previously subjected to the saline/freshwater transition. (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). Our results provide an overview of the archaeal population, Given the high phylogenetic diversity within the 25 subgroups of Bathyarchaeota, many efforts have been made to understand the key factors that control their distribution and evolution. Until now, 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. 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. A complete set of active sites and signal sequences for extracellular transport is also encoded by bathyarchaeotal SAGs (Lloydetal.2013). In this process, methane is not assimilated by Bathyarchaeota but serves as an energy source. 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. 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). In experiments towards cultivating Bathyarchaeota from the White Oak River estuary sediments, the abundance of Bathyarchaeota in control groups (basal medium) and in experimental groups containing various substrate additives and submitted to various culture processing steps were compared (Gagenetal.2013). Subgroup-5 is divided into Subgroups-5a and -5b, each with intragroup similarity >90% according to a maximum-likelihood estimation. stands for formamide concentration in the hybridization buffer (%, vol/vol). 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). Materials and methods 2.1. However, because of the high intragroup diversity and potential heterogeneous metabolic properties and adaptive strategies within the bathyarchaeotal subgroups, investigation into the subgroup distribution patterns at a fine-sorted phylotype level was recommended. (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). WebEtymology: Gr. 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). Following the four treatments, the viable bathyarchaeotal communities mainly comprised Subgroups-4 and -8, thus indicating that these two subgroups could tolerate the initial aerobic conditions (Gagenetal.2013). Heetal. Td stands for dissociation temperature for RNA slot-bolt. 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). 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). [43] (Figure 4). Collectively, these findings indicate a hybrid of archaeal and bacterial features for acetogenesis of Bathyarchaeota. Vanwonterghem I, Evans PN, Parks DH et al. Newberry CJ, Webster G, Cragg BA et al. 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. It was proposed that reduced ferredoxin generated by peptide and/or glucose might be used for the reduction of methyl groups on methylated compounds to subsequently generate methane (Evansetal.2015). Although the accumulated information paves the way for further clarification of the adaptation of different lineages to various environments, systematic understanding of the distribution pattern of bathyarchaeotal subgroups and influential factors is still needed. The indicator subgroups in saline and freshwater sediments were depicted accordingly. (Kuboetal.2012), and the outgroup sequences of Crenarchaeota, YNPFFA group and Korarchaeota were added. 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). 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). 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. FA conc. (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. 3C). Schematic figure representing major eco-niches of Bathyarchaeota. 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). It harbors methyl-coenzyme M reductase (MCR)-encoding genes, and many identified and unidentified methyltransferase-encoding genes for the utilization of various methylated compounds, but lacks most of the genes encoding the subunits of Na+-translocating methyl-H4MPT:coenzyme M methyltransferase, suggesting that the organism does not engage in hydrogenotrophic methanogenesis. This approach revealed that the separation of subgroups according to saline and anoxic levels could explain 13% of the phylogenetic lineage variance. 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 total RNA is blotted onto nylon membranes and subsequently hybridized with 33P-labeled Bathyarchaeota-specific probes (Table 1). 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). neut. Two highly abundant MCR variants were detected in Ca. It also contains typical methane metabolism genes (hdrABC and mvhADG) but lacks hdrE, similar to Methanomassiliicoccales genomes (Evansetal.2015). 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 . 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. 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. WebBathyarchaeota dominated the archaeal interaction network with 82% nodes, 96% edges, and 71% keystone species. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. 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. The phylogenetic affiliation of sequences found in peat suggest that members of the thus-far-uncultivated group Candidatus Bathyarchaeota (representing a fourth phylum) may be involved in methane cycling, either anaerobic oxidation of methane and/or methanogenesis, as at least a few organisms within this group contain the essential Candidatus Bathyarchaeota Click on organism name to get more information. On the other hand, the subgroups MCG-18 and MCG-19 were also named in Fillol et al.s research (Filloletal.2016). However, according to the genomic information on most archaeal acetogens and bathyarchaeotal genomic bins obtained by Lazaretal. Fillol M, Auguet J-C, Casamayor EO et al. Stahl DA, Flesher B, Mansfield HR et al. WebHome Business Account Form is bathyarchaeota multicellular. (2016) reconstructed six nearly complete bathyarchaeotal genomes (Subgroups-13, -15, -16, -18 and -19) from the Guaymas Basin subsurface sediment. 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). 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). Amend JP, McCollom TM, Hentscher M et al. The active microbial community in four SMTZ layers of the ODP Leg 201 subsurface sediment cores off Peru was dominated by MBG-B and Bathyarchaeota (Biddleetal.2006). It is known that a methane microbiome can be established in methane seeps sites; however, they are still poorly characterised. 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. 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. Jacquemet A, Barbeau J, Lemiegre L et al. Furthermore, the phylogeny of concatenated alignments constituting 12 ribosomal proteins obtained from currently available bathyarchaeotal genomes (from GenBank, 29 November 2017 updated) was also reconstructed, which showed a similar topology to those of 16S rRNA genes with a few exceptions in Subgroup-17 (Fig. Bathyarchaeota are believed to have roles in the carbon cycle in marine systems. Boetius A, Ravenschlag K, Schubert CJ et al. PubChem BioAssay. BA1 also lacks other genes for energy-conserving complexes, including F420H2 dehydrogenase, energy-converting hydrogenases A and B, Rhodobacter nitrogen fixation complex and V/A-type ATP synthase. Moreover, the carbonyl branch of the WoodLjungdahl pathway might reduce CO2 into acetyl-CoA. The currently available bathyarchaeotal genomes shared 63.5% similarity on average, indicating a wide phylogenetic diversity at the genome scale (Fig. 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). 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. It is one of the predominant groups in the marine subsurface archaeal community (Fryetal.2008; Teske and Srensen 2008; Lloydetal.2013). In terms of energy metabolism, these archaea contain the WoodLjungdahl pathway, capable of generating acetyl-CoA autotrophically by CO2 and H2. 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). Based on the above, it is proposed that Bathyarchaeota might mediate the AOM without assimilating the carbon in methane. The product, acetate, would then be used by acetate-consuming SRB to benefit the thermodynamic efficiency of AOM. 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. Because of the high diversity of Bathyarchaeota and various independent analyses of samples from diverse environments, the nomenclature for this archaeal group in previous reports was very complex. Viral Host. In the White Oak River estuary, the abundance of Bathyarchaeota decreases with decreasing reductive redox conditions of the sediment (Lazaretal.2015). A successful enrichment, with nearly pure biomass of certain subgroups of Bathyarchaeota, would enable a more efficient investigation of their metabolic capacities using stable isotope-labeled substrates, and establishing a direct link between the genotype and phenotype. 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.
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