Within Bathyarchaeota, the sequences were classified into six subclades according to . Methanogens and acetogenic Clostridia are the most frequent basal-branching archaea and bacteria, respectively, in phylogenetic reconstructions reflecting the descendants of the last universal common ancestor; gene categories proposed for the last universal common ancestor also point to the acetogenic and methanogenic roots, reflecting its autotrophic lifestyle as H2-dependent and N2-fixing, utilizing the WoodLjungdahl pathway and originating from a hydrothermal environmental setting (Weissetal.2016). Bathyarchaeota Our results provide an overview of the archaeal population, Members of Bathyarchaeota are able to use CO2 and H2 from natural sources and fermentation products to fuel acetogenesis (Heetal.2016; Martinetal.2016). Evans PN, Parks DH, Chadwick GL et al. bathyarchaeota In the White Oak River estuary, the abundance of Bathyarchaeota decreases with decreasing reductive redox conditions of the sediment (Lazaretal.2015). 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. 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. WebArchaea (/ r k i / ar-KEE-; singular archaeon / r k i n /) is a domain of single-celled organisms.These microorganisms lack cell nuclei and are therefore prokaryotes.Archaea were initially classified as bacteria, receiving the name archaebacteria (in the Archaebacteria kingdom), but this term has fallen out of use.. Archaeal cells have Beyond methane 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. 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. Genomic and enzymatic evidence for acetogenesis among Subgroup-15 was recently found to be enriched in 13C-labeled DNA after a 3-month incubation experiment using sulfate-reducing sediments from Aarhus Bay, but was not present in the corresponding total DNA library or in a control incubation sample (i.e. Capella-Gutirrez S, Silla-Martnez JM, Gabaldn T. Coolen MJL, Cypionka H, Sass AM et al. 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. (2012) demonstrated that the developed primers and probes result in poor coverage of Subgroups-13 to -17. 4), although these might not necessarily exist in all bathyarchaeotal subgroups (Fig. A recent study found that the refractory aromatic polymer lignin stimulated the growth of Bathyarchaeota (Subgroup-8) and they incorporated CO2 as a carbon source autotrophically and utilized lignin as an energy source (Yuetal.2018). 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. 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 Fosmid clone 37F10 containing a genome fragment originating from a bathyarchaeotal member was isolated from a metagenomic library constructed from Pearl River sediment samples (Mengetal.2009); its G + C content indicated that this genomic fragment had two portions: an archaeon-like portion (42.2%) and a bacterium-like portion (60.1%) (Mengetal.2009; Lietal.2012). Some Bathyarchaeota ASVs showed close interaction with 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). Genomic and transcriptomic evidence of light-sensing, porphyrin 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). neut. 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). (2016), it appears that these microbes rely on the acetyl-CoA synthetase (Acd) to generate acetate (Heetal.2016). 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. More recently, acetogenesis, a metabolic process deemed to be restricted to the domain bacteria, was also suggested to take place in some lineages of Bathyarchaeota (Heetal.2016; Lazaretal.2016), expanding the metabolic potential of archaea. Open reading frames encoded by the three fosmid clones comprised genes related to lipid biosynthesis, energy metabolism and resistance to oxidants. 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. These indicative subgroups are the dominant ones in the environment, as evaluated by relatively abundant fraction of Bathyarchaeota in corresponding archaeal communities (on average 44% among all studies). Characteristics of the Bathyarchaeota community in 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. The branching order of Subgroups-13 to -17 was unstable when analyzed by different tree-construction methods, and they were presented as multifurcated branches. In some flange subsamples, Bathyarchaeota were even more dominant than ANME; however, compared with the well-studied metabolism of ANME, the exact function of Bathyarchaeota in that ecological setting remains unknown. BA1 (Subgroup-3) genome contains many genes of the reductive acetyl-CoA (WoodLjungdahl) pathway and key genes of the methane metabolism pathway. 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). (C) The metabolic properties of 24 bathyarchaeotal genomes. The percentages in every row stand for the proportions of subgroups in each environmental category. According to that hypothesis, the proto-mitochondrion bacterium was capable of both respiration and anaerobic H2-producing fermentation; anaerobic syntrophy with respect to H2 brought about a physical association with an H2-dependent host and initiated a symbiotic association with the host; this led to endosymbiosis, after engulfment by the host cell (Martin and Muller 1998; Martinetal.2016). In total, 17 subgroups with 76% similarity shared by the most remote sequences were designated; however, 12% of all sequences remained ungrouped. Recently, two more bathyarchaeotal fosmid clones were screened from estuarine mangrove sediments (Mengetal.2014). Ta stands for qPCR annealing temperature, Ta,e stands for annealing and extension temperature of two-step qPCR. Kuboetal. 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). Ancestral state reconstruction was used to estimate the diversification of bathyarchaeotal lineages previously subjected to the saline/freshwater transition. Materials and methods 2.1. WebEtymology: Gr. This group of lipids has not been found in natural environments or microorganism enrichments dominated by methanotrophic archaea before (Rosseletal.2008; Kellermannetal.2012), nor have they been detected after re-analyzing lipid extracts from the above two studies using the same method in the study (Meadoretal.2015). 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. 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. Their results agree well and reflect the relatively higher bathyarchaeotal fraction in marine sediments with sulfate penetration (>0.15 m below seafloor) (Kuboetal.2012). 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. Introduction. 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). Study sites and sampling 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. ( 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. Archaea 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. [43] (Figure 4). 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). Similar community structures across different bathyarchaeotal subgroups were revealed using the two primer pairs; however, both pairs performed poorly with respect to indicating the prevalence of Subgroup-15 in cDNA libraries from freshwater sediments (Filloletal.2015). Further, the IndVal index, which reflects the level of relative abundance and frequency of occurrence, suggests that selective bathyarchaeotal subgroups are bio-indicator lineages in both freshwater and saline environments, as determined by a multivariate regression tree analysis (Filloletal.2016). Bathyarchaeota, reflecting its phylogenetic position as deeply branching with Aigarchaeota and Thaumarchaeota, and its prevalence in subsurface sediments (Mengetal.2014). Newberry CJ, Webster G, Cragg BA et al. Gene arrangement in these two fosmid clones, together with the previously recovered bathyarchaeotal fosmid sequences, confirmed low collinearity with other known archaeal genomes. 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). (Fig. 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). To cover all bathyarchaeotal subgroups that are characterized by high intragroup diversity while retaining bathyarchaeotal sequence specificity is necessary but challenging. Methanogenesis and acetogenesis are considered to be the two most fundamental and ancient microbial biochemical energy conservation processes, and they both employ the WoodLjungdahl pathway for CO2 reduction and ATP generation (Weissetal.2016). Bathyarchaeota occupied about 60% of the total archaea in the Jiulong River, China (Li et al. Interestingly, one of the highly abundant McrA subunits of Ca. The marine/freshwater segregation is a distribution pattern widely shared by diverse microorganisms, including archaea, bacteria, viruses and eukaryotes (Logaresetal.2009). Kubo et al. 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). The Distribution of Bathyarchaeota in Surface Sediments 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). 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). 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). 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. Metabolic pathways of the 3C). 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). It is known that a methane microbiome can be established in methane seeps sites; however, they are still poorly characterised. On the other hand, because of the bidirectionality of these enzymes in methane metabolism (Boetiusetal.2000; Knittel and Boetius 2009), it is still possible that some members of Bathyarchaeota are involved in anaerobic methane oxidation. Subgroup-5 is divided into Subgroups-5a and -5b, each with intragroup similarity >90% according to a maximum-likelihood estimation. 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 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). 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. 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). Furthermore, both FISH labeling and intact polar lipid quantification suggest the presence of highly abundant and active bathyarchaeotal cells in the Peru offshore subsurface sediments collected during the Ocean Drilling Program Leg 201 (Biddleetal.2006; Lippetal.2008). The 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). High-throughput sequencing of the archaeal communities and the analysis of the relationship between the distribution pattern of bathyarchaeotal subgroups and the physicochemical parameters of study sites revealed that sediment depth and sulfate concentration were important environmental factors that shape the distribution of bathyarchaeotal subgroups; Subgroup-8 was shown to be predominantly distributed in the reducing and deeper sediment layers, while Subgroup-10 was preferentially distributed in the relatively more oxidizing and shallow sediment layers (Yuetal.2017). 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. is bathyarchaeota multicellular. Peat MCG group was represented with one sequence at 90% cutoff level (Xiangetal.2017). OTUs classified within Bathyarchaeota and Chloroflexi (Dehalococcoidia) showed positive correlation with methane concentrations, sediment depth and oxidation-reduction potential. 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. Until now, 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. Surprisingly, these genes fall closely to the Bathyarchaeota mcr genes. 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). It also contains typical methane metabolism genes (hdrABC and mvhADG) but lacks hdrE, similar to Methanomassiliicoccales genomes (Evansetal.2015). BATHYARCHAEOTA OCCURRENCE IN SHALLOW MARINE Bathyarchaeota Consequently, CO2 appears to be the only electron acceptor mediating AOM, like in a reverse acetoclastic methanogenesis (Hallametal.2004; Wangetal.2014). Draft Genome Sequence of " Candidatus Bathyarchaeotal SAGs also encode pathways for the intracellular breakdown of amino acids. Laso-Prez R, Wegener G, Knittel K et al. 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). 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 < Bathyarchaeota was the most abundant archaeal phylum in most samples, accounting for 13.8164.14% of archaeal sequences (Fig. This could be explained by the versatile pathways of organic matter assimilation present in the majority of Bathyarchaeota, reflected by inferences from genomic data. This review is supported by the National Natural Science Foundation of China (grant numbers 31622002, 41506163, 31600093, 41525011, 91428308), the State Key R&D project of China (grant number 2016YFA0601102), the Key Project of Department of Education of Guangdong Province (No. Membrane lipids are an informative indicator of the distribution and activity of living microbial cells, independently of their culturing (Sturtetal.2004; Jacquemetetal.2009; Lipp, Liu and Hinrichs 2009). However, after allowing for a single nucleotide mismatch, the coverage efficiency markedly increased, to around 8090%. 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). Although the Pta-Ack pathway has been previously identified in the methanogenic genus Methanosarcina, it was shown that the encoding pta-ack gene pair might be derived from a horizontal transfer of genes of bacterial origin (Fournier and Gogarten 2008). They include Euryarchaeota, and members of the DPANN and Asgard archaea. 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). (A) Phylogenetic tree of ribosomal proteins obtained from currently available bathyarchaeotal genomes (from GenBank, 29 November 2017 updated). 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). Lomstein BA, Langerhuus AT, DHondt S et al.
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