2012 ). 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. Bathyarchaeota occupied about 60% of the total archaea in the Jiulong River, China (Li et al. Heetal. The isolation source information was parsed from gbk files of bathyarchaeotal 16S rRNA gene sequences. Hence, the primer pair MCG242dF and MCG678R was developed based on a collection of bathyarchaeotal sequences of freshwater origin (Filloletal.2016). 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. Other archaeal groups are also commonly detected in estuaries worldwide. Ancestral state reconstruction was used to estimate the diversification of bathyarchaeotal lineages previously subjected to the saline/freshwater transition. Second, determining whether the methane cycling capacity is confined to certain subgroups or whether numerous subgroups or lineages are capable of methane cycling, and if so, the nature of their shared evolutionary or genomic characteristics, is of utmost importance. However, the ecological knowledge of Bathyarchaeota is limited in peatland ecosystems. 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). Genomic characterization and metabolic potentials of Bathyarchaeota. Jacquemet A, Barbeau J, Lemiegre L et al. 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. Sequences longer than 940 bp were first used to construct the backbone of the tree, and additional sequences were then added without altering the general tree topology. Further, based on genomic inferences, Evansetal. Rossel PE, Lipp JS, Fredricks HF et al. 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). More recently, Heetal. 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). To increase the permeability of the cell wall and obtain a good amplification signal, a 10-min 0.01 M HCl treatment may be employed (Kuboetal.2012). Sousa FL, Neukirchen S, Allen JF et al. A complete set of active sites and signal sequences for extracellular transport is also encoded by bathyarchaeotal SAGs (Lloydetal.2013). S. butanivorans protein extracts; they are probably responsible for the initial step of butane activation to generate butyl-CoM. 2017KZDXM071), and the Science and Technology Innovation Committee of Shenzhen (Grant No. Both Bathyarchaeota and the recently identified more basally branched Lokiarchaeota acquired the H4MPT-dependent WoodLjungdahl pathway and the hydrogen-dependent electron bifurcating system MvhADG-HdrABC, viewed as typical for the anaerobic and hydrogen-dependent archaeal lifestyle (Lazaretal.2016; Sousaetal.2016). The subgroups MCG-18, -19 and -20 were firstly named in Lazar et al.s study, but only MCG-19 was represented in the phylogenetic tree (Lazaretal.2015). The 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). Candidatus Bathyarchaeota Click on organism name to get more information. Surprisingly, these genes fall closely to the Bathyarchaeota mcr genes. 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. The central product, acetyl-CoA, would either (i) be involved in substrate-level phosphorylation to generate acetate and ATP, catalyzed by an ADP-forming acetyl-CoA synthase as in other peptide-degrading archaea; (ii) be metabolized to generate acetate through the Pta-Ack pathway, similarly to bona fide bacterial homoacetogens; or (iii) be utilized for biosynthesis, e.g. The 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 Furthermore, both BA1 and BA2 lack ATP-synthase, indicating that they are restricted to substrate-level phosphorylation for energy, which was first found in methanogenic archaea (Evansetal.2015). This study is also a contribution to the Deep Carbon Observatory. WebBathyarchaeota are abundant in sediments, and they may involve in sedimentary organic matter degradation, acetogenesis, and, potentially, methane metabolism, based on genomics. 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. 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. Similarly, rRNA slot blot hybridization indicates the existence of functionally active Bathyarchaeota not only in the surface and subsurface sediments from the Nyegga site 272-02, Cascadia Margin, Gulf of Mexico, Hydrate Ridge ODP site 1245 and Janssand (North Sea), but also in the oxic mats in the Arabian Gulf and subsurface White Oak River sediments (Kuboetal.2012). the most persistent detrital matter in marine sediments (Lomsteinetal.2012; Lloydetal.2013). 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. 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. To cover all bathyarchaeotal subgroups that are characterized by high intragroup diversity while retaining bathyarchaeotal sequence specificity is necessary but challenging. Markers for individual pathway/function were scanned against genomes using the HMM and KEGG databases (Anantharamanetal.2016; Kanehisa, Sato and Morishima 2016; Spang, Caceres and Ettema 2017). Evans PN, Parks DH, Chadwick GL et al. Genomic fragments of the fosmid clone 75G8 harbor a putative methyl-accepting chemotaxis protein- and 4-carboxymuconolactone decarboxylase-encoding genes, suggesting that this bathyarchaeotal member (Subgroup-8) is able to utilize aromatic compounds. In this process, methane is not assimilated by Bathyarchaeota but serves as an energy source. Anantharaman K, Brown CT, Hug LA et al. Until now, However, their life strategies have remained largely elusive. The presence and relative abundance of bathyarchaeotal rRNA can then be estimated based on the hybridization intensity (Stahletal.1988; Kuboetal.2012). Open reading frames encoded by the three fosmid clones comprised genes related to lipid biosynthesis, energy metabolism and resistance to oxidants. 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). Peptidases targeting d-amino acids, which are highly enriched in the peptidoglycan of bacterial cell walls, are encoded as well, indicating that Bathyarchaeota may have acquired the capacity to degrade recalcitrant components of bacterial cell walls, i.e. Four major heterotrophic pathways centralized on the acetyl-CoA generation are summarized below, reflecting the core metabolism of fermentation and acetogenesis (Fig. 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). In this study, the abundance and (Kuboetal.2012), and the outgroup sequences of Crenarchaeota, YNPFFA group and Korarchaeota were added. 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. Considering the ubiquity and frequent predominance of Bathyarchaeota in marine sediments, as well as the high abundance and potential activity of extracellular peptidases that they encode, it has been proposed that Bathyarchaeota may play a previously undiscovered role in protein remineralization in anoxic marine sediments. (2016), it appears that these microbes rely on the acetyl-CoA synthetase (Acd) to generate acetate (Heetal.2016). The Archaebacteria kingdom is divided into three WebGiven the wide environmental and phylogenetic diversity of Bathyarchaeota, additional genomes are required to understand the metabolic capabilities of this understudied 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. 1) (Heetal.2016; Lazaretal.2016). 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. Multiple genomic and physiological traits of these microorganisms have been coming to light in recent decades with the advent of stable isotope labeling and metagenomic profiling methods. 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). 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). 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. 3C). 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). Recent genomic evidence suggests that Bathyarchaeota might potentially be involved in methane metabolism, a property that had only been confirmed to date in the Euryarchaeota domain (Evansetal.2015; Lloyd 2015). The possibility of the replacement of the AOM function of ANME by Bathyarchaeota was also suggested by a microbial community composition in a study of the microbial colonization within an artificial micro-niche, basaltic glass imposed by hydrothermal conditions (Callacetal.2013). Metabolic pathways of the (iii) The relatively small 13C signature of the archaeal intact polar lipids in comparison with the archaeal biomass suggests that the C isotopic fractionation during lipid biosynthesis is different from that of typical methylotrophic methanogens (Summons, Franzmann and Nichols 1998). Given the diverse and complex phylogeny of the Bathyarchaeota (Kuboetal.2012; Filloletal.2016), the occurrence of commonly shared physiological and metabolic properties in different lineages seems unlikely, with the evolutionary diversification of bathyarchaeotal lineages largely driven by the adaptation to various environmental conditions and available carbon and energy sources, etc. Our results provide an overview of the archaeal population, Recent data point to the global occurrence of Bathyarchaeota and their potential impact on global carbon transformation, highlighting their important role as a group of global generalists participating in carbon cycling, similar to euryarchaeotal methanogens and Thaumarchaeota. 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. 1) (for details see Kuboetal.2012). Combinations of MCG242dF with MCG678R or MCG732R were recommended for targeting relatively long 16S rRNA gene fragments to obtain more phylogenetic information; these might be used in clone library construction or for denaturing gradient gel electrophoresis-based community fingerprinting analysis. (2008) further summarized 47 clone libraries of 16S rRNA genes from the marine subsurface, with Bathyarchaeota accounting for 33% of all archaea. Given that they are abundant, globally distributed and phylogenetically diverse, continued exploration of new potential bathyarchaeotal subgroups is encouraged. In this tree, the Subgroups-1 to -17 were the same as Kubo's tree (Kuboetal.2012), and Subgroup-5 was divided into Subgroups-5a, -5b and -5bb as suggested in Fillol et al.s research (Filloletal.2016). Newberry CJ, Webster G, Cragg BA et al. 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). 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). On the other hand, the subgroups MCG-18 and MCG-19 were also named in Fillol et al.s research (Filloletal.2016). A segregated distribution of bathyarchaeotal subgroups was also observed in the water column and sediments in freshwater karstic lakes (Filloletal.2015). The use of MCG242dF resulted in an adequate coverage of almost all subgroups with 0/1 nucleotide mismatches, except for Subgroups-10 and -17, which showed low coverage efficiency with no nucleotide mismatches. 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. Buckles LK, Villanueva L, Weijers JWH et al. Uncultured archaea in deep marine subsurface sediments: have we caught them all? 2). 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. The branching order of Subgroups-13 to -17 was unstable when analyzed by different tree-construction methods, and they were presented as multifurcated branches. Interestingly, one of the highly abundant McrA subunits of Ca. 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). 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). Members of the Bathyarchaeota, formerly known as the Miscellaneous Crenarchaeota Group (MCG), are widely distributed in various environments such as freshwater lake, marine, and estuarine sediments [ 18, 19, 20, 21 ]. Kellermann MY, Wegener G, Elvert M et al. 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). 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). Abstract. 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). Thaumarchaeota MG-I was present in the 12C-DNA library in the corresponding zone but was not detected in the 13C-DNA library, suggesting that these microbes are not able to use 13C-acetate (Websteretal.2010). All sequences were clustered at 90% identity using Usearch v10.0.240 (https://www.drive5.com/usearch/), then the 16S rRNA gene sequences from available bathyarchaeotal genomes in public database, the anchor sequences from Kuboetal. 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. 3). Oxford University Press is a department of the University of Oxford. JCYJ20170818091727570). 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. Two highly abundant MCR variants were detected in Ca. It is known that a methane microbiome can be established in methane seeps sites; however, they are still poorly characterised. (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). Lloyd KG, Schreiber L, Petersen DG et al. (2018) described a predominance of the phylum Bathyarchaeota (now class Bathyarchaeia from phylum Crenarchaeota) in mid-latitude estuaries, 2). 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). Martin WF, Neukirchen S, Zimorski V et al. The incorporation of 13C-bicarbonate into the archaeal lipids (potential bathyarchaeotal-specific biphytanes) was significantly observed only with lignin addition. RNA slot blot hybridization can also be used for the quantification of functionally active bathyarchaeotal 16S rRNA. However, due to the great diversity of them, there is limited genomic information that accurately encompasses the metabolic potential of the entire archaeal phylum. 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). Bathyarchaeota is characterized by high intragroup diversity, with most subgroups showing within-sequence similarity <92% (Kuboetal.2012; Filloletal.2016). A phylogenetic tree based on the sequences of UbiA prenyltransferase superfamily proteins, including ChlG/BchG and additional five subfamilies of this superfamily, revealed that this unique BchG of archaeal origin groups within the ChlG/BchG family; however, it diverged earlier than the bacterial BchG proteins. The groups of B24 and B25 (Heetal.2016) were added into the tree representing Subgroups-21 and -22, respectively. Taxonomic classification revealed that between 0.1 and 2% of all classified sequences were assigned to Bathyarchaeota.

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