Abstract:Recent discoveries of methyl-coenzyme M reductase–encoding genes (
mcr
) in uncultured archaea beyond traditional euryarchaeotal methanogens have reshaped our view of methanogenesis. However, whether any of these nontraditional archaea perform methanogenesis remains elusive. Here, we report field and microcosm experiments based on
13
C-tracer labeling and genome-resolved metagenomics and metatranscriptomics, revealing that nontraditional archaea are predominant a… Show more
“…4 ), which were described in detail previously 27 . Even though some members of the Archaeoglobales and Nezhaarchaeales in Tengchong and other terrestrial spring systems have recently been shown to be methanogenic 42 , 43 , the number of transcripts mapping to mcrABG in our datasets were low. Fig.…”
Terrestrial geothermal springs are physicochemically diverse and host abundant populations of Archaea. However, the diversity, functionality, and geological influences of these Archaea are not well understood. Here we explore the genomic diversity of Archaea in 152 metagenomes from 48 geothermal springs in Tengchong, China, collected from 2016 to 2021. Our dataset is comprised of 2949 archaeal metagenome-assembled genomes spanning 12 phyla and 392 newly identified species, which increases the known species diversity of Archaea by ~48.6%. The structures and potential functions of the archaeal communities are strongly influenced by temperature and pH, with high-temperature acidic and alkaline springs favoring archaeal abundance over Bacteria. Genome-resolved metagenomics and metatranscriptomics provide insights into the potential ecological niches of these Archaea and their potential roles in carbon, sulfur, nitrogen, and hydrogen metabolism. Furthermore, our findings illustrate the interplay of competition and cooperation among Archaea in biogeochemical cycles, possibly arising from overlapping functional niches and metabolic handoffs. Taken together, our study expands the genomic diversity of Archaea inhabiting geothermal springs and provides a foundation for more incisive study of biogeochemical processes mediated by Archaea in geothermal ecosystems.
“…4 ), which were described in detail previously 27 . Even though some members of the Archaeoglobales and Nezhaarchaeales in Tengchong and other terrestrial spring systems have recently been shown to be methanogenic 42 , 43 , the number of transcripts mapping to mcrABG in our datasets were low. Fig.…”
Terrestrial geothermal springs are physicochemically diverse and host abundant populations of Archaea. However, the diversity, functionality, and geological influences of these Archaea are not well understood. Here we explore the genomic diversity of Archaea in 152 metagenomes from 48 geothermal springs in Tengchong, China, collected from 2016 to 2021. Our dataset is comprised of 2949 archaeal metagenome-assembled genomes spanning 12 phyla and 392 newly identified species, which increases the known species diversity of Archaea by ~48.6%. The structures and potential functions of the archaeal communities are strongly influenced by temperature and pH, with high-temperature acidic and alkaline springs favoring archaeal abundance over Bacteria. Genome-resolved metagenomics and metatranscriptomics provide insights into the potential ecological niches of these Archaea and their potential roles in carbon, sulfur, nitrogen, and hydrogen metabolism. Furthermore, our findings illustrate the interplay of competition and cooperation among Archaea in biogeochemical cycles, possibly arising from overlapping functional niches and metabolic handoffs. Taken together, our study expands the genomic diversity of Archaea inhabiting geothermal springs and provides a foundation for more incisive study of biogeochemical processes mediated by Archaea in geothermal ecosystems.
“…Collectively, our results and the studies by Wang et al . and Buessecker et al ., who reported that Mcr-encoding Archaeoglobi are present (35) and transcriptionally active in hot spring mesocosms (34), demonstrate the previously overlooked role Archaeoglobi might play in the anaerobic carbon cycle of geothermal environments.…”
Section: Resultsmentioning
confidence: 95%
“…Importantly, one of these Archaeoglobales MAGs represented the only Mcr-encoding archaeon that expressed mcrABG genes in methanogenic microcosms performed without substrate addition or with the addition of 10 mM methanol at 75 °C. This indirectly demonstrated the methanogenic nature of this archaeon (34). Last, Buessecker et al reported the establishment of a methanogenic enrichment culture of Ca.…”
Section: Introductionmentioning
confidence: 76%
“…Lynes, Krukenberg et al reported that Archaeoglobi can be enriched in hot spring mesocosms under methanogenic conditions (33). Wang et al reported that mcrABG and other methanogenesis marker genes encoded by two Archaeoglobales MAGs were highly expressed in hot spring microcosms incubated at 65 °C and 75 °C (34). Importantly, one of these Archaeoglobales MAGs represented the only Mcr-encoding archaeon that expressed mcrABG genes in methanogenic microcosms performed without substrate addition or with the addition of 10 mM methanol at 75 °C.…”
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.
“…Wang et al . reported that mcrABG and other methanogenesis marker genes encoded by two Archaeoglobales MAGs were highly expressed in hot spring microcosms incubated at 65°C and 75°C [ 34 ]. Importantly, one of these Archaeoglobales MAGs represented the only Mcr-encoding archaeon that expressed mcrABG genes in methanogenic microcosms performed without substrate addition or with the addition of 10 mM methanol at 75°C.…”
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 thermophilic euryarchaeotes that have long been considered to live non-methanogenic lifestyles. Here, we enriched Candidatus Methanoglobus 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 fluorescence in situ hybridization. Via genome-resolved metatranscriptomics and stable isotope tracing, we demonstrate that Ca. M. hypatiae expresses methylotrophic methanogenesis and energy-conserving pathways for reducing monomethylamine to methane. The detection of Archaeoglobi populations related to Ca. M. hypatiae in 36 geochemically diverse geothermal sites within Yellowstone National Park, as revealed through the examination of previously published gene amplicon datasets, implies a previously underestimated contribution to anaerobic carbon cycling in extreme ecosystems.
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