Culexarchaeia, a novel archaeal class of anaerobic generalists inhabiting geothermal environments

Kohtz, Anthony J.; Jay, Zackary J.; Lynes, Mackenzie M.; Krukenberg, Viola; Hatzenpichler, Roland

doi:10.1038/s43705-022-00175-8

Cited by 13 publications

(10 citation statements)

References 101 publications

(138 reference statements)

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“…Annotation of the assembled sequences was performed with Prokka v1.14.16 (62). Assembled scaffolds ≥2000 bp were binned using Maxbin v2.2.7 (63), Metabat v2.12.1 (with and without coverage) (64), Concoct v1.0.0 (65), Autometa v1 (bacterial and archaeal modes with the machine learning step) (66), followed by bin refinement with DAS_Tool v1.1.6 (67), as previously described (68). Bin completeness and redundancy were assessed with CheckM v1.2.2 (69).…”

Section: Methodsmentioning

confidence: 99%

Methylotrophic methanogenesis in the Archaeoglobi revealed by cultivation ofCa.Methanoglobus hypatiae from a Yellowstone hot spring

Lynes,

Jay,

Kohtz

et al. 2023

Preprint

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Over the past decade, environmental metagenomics and PCR-based marker gene surveys have revealed that several lineages beyond just a few well-established groups within the Euryarchaeota superphylum harbor the genetic potential for methanogenesis. One of these groups are the Archaeoglobi, a class of obligately thermophilic Euryarchaeotes that have long been considered to live a non-methanogenic lifestyle. Here, we enrichedCandidatusMethanoglobus hypatiae, a methanogen affiliated with the family Archaeoglobaceae, from a hot spring in Yellowstone National Park. The enrichment is sediment-free, grows at 64-70 °C and a pH of 7.8, and produces methane from mono-, di-, and tri-methylamine.Ca.M. hypatiae is represented by a 1.62 Mb metagenome-assembled genome with an estimated completeness of 100% and accounts for up to 67% of cells in the culture according to fluorescencein situhybridization. Via genome-resolved metatranscriptomics and stable isotope tracing, we demonstrate thatCa.M. hypatiae expresses methylotrophic methanogenesis and energy-conserving pathways for reducing monomethylamine to methane. The detection of Archaeoglobi populations related toCa.M. hypatiae in 36 geochemically diverse geothermal sites within Yellowstone National Park (pH 2.61-9.35; 18.4 to 93.8 °C), as revealed through the examination of previously published gene amplicon datasets, implies a previously underestimated contribution to anaerobic carbon cycling in extreme ecosystems.Significance statementThe majority of global methane emissions are attributed to the activity of methane-producing anaerobic archaea, the methanogens. Over the last decade, environmental DNA sequencing demonstrated that culture collections do not adequately represent the true taxonomic and metabolic diversity of methanogens present in nature. One group of archaea postulated to contribute to methane production in high temperature marine and terrestrial environments are the Archaeoglobi, a group of obligate thermophilic archaea within the Euryarchaeota superphylum. Here, we report the cultivation and physiological characterization of a methanogenic member of the Archaeoglobi,Ca.Methanoglobus hypatiae, from a hot spring in Yellowstone National Park. Via a combination of growth experiments, stable isotope tracing, metatranscriptomics, microscopy analyses, and re-examination of gene amplicon surveys, our study provides direct experimental evidence of methanogenesis in the Archaeoglobi and shows that closely related archaea are widely distributed in Yellowstone’s geothermal features.

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Section: Methodsmentioning

confidence: 99%

Methylotrophic methanogenesis in the Archaeoglobi revealed by cultivation ofCa.Methanoglobus hypatiae from a Yellowstone hot spring

Lynes,

Jay,

Kohtz

et al. 2023

Preprint

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“…LCB70 encodes several complexes that could be involved in the reduction of CoM-S-S-CoB, energy conservation, and hydrogen metabolism. We found genes encoding heterodisulfide reductase (HdrBC) adjacent to genes of the proposed [NiFe]-hydrogenase complex, Ehd, which could couple the oxidation of H2 to the reduction of CoM-S-S-CoB and translocation of H + or Na + ions across the membrane 3,26 . A group 4i [NiFe]-hydrogenase, Ehb, is also encoded in the LCB70 genome.…”

Section: Metabolic Potential Of Strain Lcb70mentioning

confidence: 99%

“…Resulting reads were assembled with SPAdes v3.15.3 (-k 33,55,77,99,111 -meta -only-assembler) and coverage was determined by mapping the cleaned and corrected reads to the assembled sequences with bbmap (ambiguous=random). Assembled sequences ≥2,000 bp in length were binned with four programs: Maxbin v2.2.7 49 , Concoct v1.0.0 50 , Metabat v2.12.1 (with and without coverage) 51 , and Autometa v1 (bacterial and archaeal modes, including the machine learning step) 52 followed by bin refinement with DAS_Tool v1.1.2 53 , as previously described 26 . CheckM v1.1.3 54 was used to assess MAG completeness and redundancy.…”

Section: Metagenome Assembly Binning and Quality Assessmentmentioning

confidence: 99%

Cultivation and visualization of a methanogen of the phylum Thermoproteota

Hatzenpichler

Kohtz

Krukenberg

et al. 2023

Preprint

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Methane is the second most abundant climate-active gas and understanding its sources and sinks is a crucial endeavor in microbiology, biogeochemistry, and climate sciences (1,2). For decades, it was thought that methanogenesis, the ability to conserve energy coupled to methane production, was restricted to a taxonomically and metabolically specialized group of archaea, the Euryarchaeota1. The discovery of marker genes for anaerobic alkane cycling in metagenome-assembled genomes obtained from diverse habitats has led to the hypothesis that archaeal lineages outside the Euryarchaeota are involved in methanogenesis (3-6). Here, we cultured Candidatus Methanosuratincola yellowstonensis, a member of the archaeal phylum Thermoproteota, from a terrestrial hot spring. Growth experiments combined with activity assays, stable isotope tracing, and genomic analyses confirmed that this thermophilic archaeon grows via methyl-reducing hydrogenotrophic methanogenesis. Cryo-electron tomography revealed that Ca. M. yellowstonensis cells are archaellated coccoid cells that form intercellular bridges, providing two to three cells with a continuous cytoplasm and S-layer. The wide environmental distribution of Ca. M. yellowstonensis suggests that they might play important and hitherto overlooked roles in carbon cycling within diverse anoxic habitats.

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“…The BLASTp searches of Hbs protein homologs in the NCBI database and the respiration features of archaea are derived from published studies (27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39). Taxonomic groups that contain at least one species with Hbs homologs are designated by black circles.…”

Section: Fig 3 the Distribution Of Hbs Homologs In Archaea Genomes An...mentioning

confidence: 99%

Biosynthesis of H-GDGTs linked to ocean oxygen deficiency

Li,

Yu,

Feng

et al. 2023

Preprint

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Archaeal membrane lipids GDGTs (glycerol dialkyl glycerol tetraethers) are biomarkers used for tracking Earth's historical environmental changes. Among these GDGTs, the H-shaped GDGTs (H-GDGTs, or GMGTs) represent a less-explored and often overlooked subset, with its biosynthetic pathway and geological significance remaining elusive. Here, we identified the gene responsible for biosynthesizing H-GDGTs, which encodes to a radical S-adenosyl-L-methionine (SAM) enzyme, named as H-GDGTs bridge synthase (Hbs). Heterologous expression of the gene hbs in a methanogen, as well as in vitro activity assay using the purified Hbs enzyme were performed. Additionally, we found that the genes encoding Hbs are exclusively present in obligate anaerobic archaea genomes and the metagenomes obtained from oxygen-deficient environments, but not in oxic settings. The H-GDGTs lipids were also consistently enriched in the modern oxygen-deficient environments, and remarkably accumulated in ancient sediments during oceanic anoxic event-2 (OAE-2, ~94 million years ago) period. Our findings indicate H-GDGTs holds significant promise as a novel biomarker for studying historical ocean oxygen deficiency supported by a well-established biological basis.

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Culexarchaeia, a novel archaeal class of anaerobic generalists inhabiting geothermal environments

Cited by 13 publications

References 101 publications

Methylotrophic methanogenesis in the Archaeoglobi revealed by cultivation ofCa.Methanoglobus hypatiae from a Yellowstone hot spring

Methylotrophic methanogenesis in the Archaeoglobi revealed by cultivation ofCa.Methanoglobus hypatiae from a Yellowstone hot spring

Cultivation and visualization of a methanogen of the phylum Thermoproteota

Biosynthesis of H-GDGTs linked to ocean oxygen deficiency

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