Genomic and Transcriptomic Evidence Supports Methane Metabolism in
            <i>Archaeoglobi</i>

Liu, Yifan; Chen, Jing; Wang, Liying; Mbadinga, Serge Maurice; Hou, Zhenshan; Wu, Xiaolin; Gu, Ji‐Dong; Zengler, Karsten; Mu, Bo‐Zhong

doi:10.1128/msystems.00651-19

Cited by 38 publications

(39 citation statements)

References 70 publications

(113 reference statements)

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“… 2019 ; Liu et al . 2020 ) underscores that (hydrogen-dependent) methylotrophic methanogenesis is widespread and—due to the high affinity for hydrogen—most likely limited by the availability of methyl groups.…”

Section: Resultsmentioning

confidence: 99%

The hydrogen threshold of obligately methyl-reducing methanogens

Feldewert

Lång

Brune

2020

FEMS Microbiology Letters

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Methanogenesis is the final step in the anaerobic degradation of organic matter. The most important substrates of methanogens are hydrogen plus carbon dioxide and acetate, but also the use of methanol, methylated amines, and aromatic methoxy groups appears to be more widespread than originally thought. Except for most members of the family Methanosarcinaceae, all methylotrophic methanogens require external hydrogen as reductant and therefore compete with hydrogenotrophic methanogens for this common substrate. Since methanogenesis from carbon dioxide consumes four molecules of hydrogen per molecule of methane, whereas methanogenesis from methanol requires only one, methyl-reducing methanogens should have an energetic advantage over hydrogenotrophic methanogens at low hydrogen partial pressures. However, experimental data on their hydrogen threshold is scarce and suffers from relatively high detection limits. Here, we show that the methyl-reducing methanogens Methanosphaera stadtmanae (Methanobacteriales), Methanimicrococcus blatticola (Methanosarcinales), and Methanomassiliicoccus luminyensis (Methanomassiliicoccales) consume hydrogen to partial pressures < 0.1 Pa, which is almost one order of magnitude lower than the thresholds for M. stadtmanae and M. blatticola reported in the only previous study on this topic. We conclude that methylotrophic methanogens should outcompete hydrogenotrophic methanogens for hydrogen and that their activity is limited by the availability of methyl groups.

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Section: Resultsmentioning

confidence: 99%

The hydrogen threshold of obligately methyl-reducing methanogens

Feldewert

Lång

Brune

2020

FEMS Microbiology Letters

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“…Three of them, based on synteny, are probably involved in pseudomurein biosynthesis (Supplementary Figure 35). Another case is the Hcg proteins in the biosynthetic pathway of the iron guanylylpyridinol cofactor of the Hmd hydrogenase in Methanomada and Desulfurobacteriales (Supplementary Figure 36, Supplementary Data 8,9). The second category consists of genes whose origin can be traced to the LMA either under the classic root of Archaea with respectively monophyletic Proteoarchaeota and Euryarchaeota or with a root within Euryarchaeota from Raymann et al 39 .…”

Section: Resultsmentioning

confidence: 99%

“…The Archaeoglobi member Ca. Methanomixophus hydrogenotrophicum 9 possesses an apparently vertically inherited Mtr. However, its Mcr and some of the associated methanogenesis markers are more recent acquisitions from within the Proteoarchaeota (Figure 1).…”

Section: Resultsmentioning

confidence: 99%

“…While the composition of Class I methanogens (Methanomada) has remained constant over the years, several methane metabolizing lineages are now known to be related to the Class II methanogens. Collectively they form the clade called Methanotecta 2 or Halobacterota 3,4 and include the Methanocellales, Methanoflorentaceae 5 , Methanonatronarchaeia 6 , Methanophagales (ANME-1), and Archaeoglobi [7][8][9] . The distribution of methane metabolism currently extends to most Euryarchaeota major clades and some Proteoarchaeota lineages 10,11 .…”

Section: Introductionmentioning

confidence: 99%

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Genomic remnants of ancestral hydrogen and methane metabolism in Archaea drive anaerobic carbon cycling

Adam

Kolyfetis

Bornemann

et al. 2021

Preprint

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Methane metabolism is among the hallmarks of Archaea, originating very early in their evolution. Other than its two main complexes, methyl-CoM reductase (Mcr) and tetrahydromethanopterin-CoM methyltransferase (Mtr), there exist other genes called "methanogenesis markers" that are believed to participate in methane metabolism. Many of them are Domains of Unknown Function. Here we show that these markers emerged together with methanogenesis. Even if Mcr is lost, the markers and Mtr can persist resulting in intermediate metabolic states related to the Wood-Ljungdahl pathway. Beyond the markers, the methanogenic ancestor was hydrogenotrophic, employing the anaplerotic hydrogenases Eha and Ehb. The selective pressures acting on Eha, Ehb, and Mtr partially depend on their subunits' membrane association. Integrating the evolution of all these components, we propose that the ancestor of all methane metabolizers was an autotrophic H2/CO2 methanogen that could perhaps use methanol but not oxidize alkanes. Hydrogen-dependent methylotrophic methanogenesis has since emerged multiple times independently, both alongside a vertically inherited Mcr or from a patchwork of ancient transfers. Through their methanogenesis genomic remnants, Thorarchaeota and two newly reconstructed order-level lineages in Archaeoglobi and Bathyarchaeota act as metabolically versatile players in carbon cycling of anoxic environments across the globe.

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“…Another new genus of Archaeoglobi, Ca. Methanomixophus, contains MTR complex genes as well as a complete mcrBDCGA operon, along with predicted ligand binding sites for HS-CoM, HS-CoB, and F 430 ( Liu et al, 2020 ). Metatranscriptomic experiments showed active hydrogen-dependent methylotrophic methanogenesis as well as heterotrophic fermentation.…”

Section: Other Divergent Mcrsmentioning

confidence: 99%

Overview of Diverse Methyl/Alkyl-Coenzyme M Reductases and Considerations for Their Potential Heterologous Expression

Gendron

Allen

2022

Front. Microbiol.

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Methyl-coenzyme M reductase (MCR) is an archaeal enzyme that catalyzes the final step of methanogenesis and the first step in the anaerobic oxidation of methane, the energy metabolisms of methanogens and anaerobic methanotrophs (ANME), respectively. Variants of MCR, known as alkyl-coenzyme M reductases, are involved in the anaerobic oxidation of short-chain alkanes including ethane, propane, and butane as well as the catabolism of long-chain alkanes from oil reservoirs. MCR is a dimer of heterotrimers (encoded by mcrABG) and requires the nickel-containing tetrapyrrole prosthetic group known as coenzyme F430. MCR houses a series of unusual post-translational modifications within its active site whose identities vary depending on the organism and whose functions remain unclear. Methanogenic MCRs are encoded in a highly conserved mcrBDCGA gene cluster, which encodes two accessory proteins, McrD and McrC, that are believed to be involved in the assembly and activation of MCR, respectively. The requirement of a unique and complex coenzyme, various unusual post-translational modifications, and many remaining questions surrounding assembly and activation of MCR largely limit in vitro experiments to native enzymes with recombinant methods only recently appearing. Production of MCRs in a heterologous host is an important step toward developing optimized biocatalytic systems for methane production as well as for bioconversion of methane and other alkanes into value-added compounds. This review will first summarize MCR catalysis and structure, followed by a discussion of advances and challenges related to the production of diverse MCRs in a heterologous host.

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Genomic and Transcriptomic Evidence Supports Methane Metabolism in Archaeoglobi

Cited by 38 publications

References 70 publications

The hydrogen threshold of obligately methyl-reducing methanogens

The hydrogen threshold of obligately methyl-reducing methanogens

Genomic remnants of ancestral hydrogen and methane metabolism in Archaea drive anaerobic carbon cycling

Overview of Diverse Methyl/Alkyl-Coenzyme M Reductases and Considerations for Their Potential Heterologous Expression

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