Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

Spanning, Rob J.M. van; Guan, Qingtian; Melkonian, Chrats; Gallant, James; Polerecký, Lùbos; Flot, Jean-François; Brandt, Bernd W.; Braster, Martin; Espinoza, Paul Iturbe; Aerts, Joost W.; Meima-Franke, Marion; Piersma, Sander R.; Bunduc, Catalin M.; Ummels, Roy; Pain, Arnab; Fleming, Emily J.; Wel, Nicole N. van der; Gherman, Vasile Daniel; Sarbu, Serban M.; Bodelier, Paul L. E.; Bitter, Wilbert

doi:10.1038/s41564-022-01252-3

Cited by 27 publications

(27 citation statements)

References 72 publications

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“…These observations suggest that many of these lineages are potentially overlooked as methane oxidizers in these habitats. We highlight the Mycobacteriaceae as a case study in the Supplementary Results to place our phylogenomic analyses in the context of the recent discovery of methanotrophy in an isolate from this family, which clarifies the previous conflicting reports concerning methane oxidation in representatives of this family (71). In the future, it will be important to take advantage of the fact that many of these strains, in the Mycobacteriaceae but also from the other lineages profiled here, exist in culture collections, providing an opportunity to validate their predicted methane oxidation capacity.…”

Section: Resultssupporting

confidence: 66%

“…The detection of putative methanotrophs in the Nevskiaceae, Acetobacteraceae , which are families lacking in vivo evidence of methanotrophy, and the Mycobacteriaceae , which displayed conflicting physiological evidence surrounding the capacity for methanotrophy until very recently (71), prompted us to examine whether the methanotrophic potential observed for these genomes was unique to the landfill-derived populations or more widespread in each lineage. Phylogenomic analyses revealed that multiple genomes spread throughout each family’s tree carried the genes coding for complete pMMO and/or sMMO complexes, suggesting the capacity for methanotrophy has been acquired on several occasion within each lineage (See Supplemental Results for detailed descriptions; Fig S6, S7, S8 ).…”

Section: Resultsmentioning

confidence: 99%

Section: Phylogenomic Analyses Of Families With No Known Capacity For...mentioning

confidence: 99%

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Microbial methane cycling in a landfill on a decadal time scale

Grégoire

George

Hug

2023

Preprint

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Landfills generate outsized environmental footprints due to microbial degradation of organic matter in municipal solid waste, which produces the potent greenhouse gas methane. With global solid waste production predicted to increase 69% by the year 2050, there is a pressing need to better understand the biogeochemical processes that control microbial methane cycling in landfills. In this study, we had the rare opportunity to characterize the microbial community responsible for methane cycling in landfill waste covering a 39-year timeframe. We coupled long term geochemical analyses to whole-community DNA (i.e., metagenomic) sequencing and identified key features that shape methane cycling communities over the course of a landfill's lifecycle. Anaerobic methanogenic microbes are more abundant, diverse, and metabolically versatile in newer waste, fueling rapid methane production early in a landfill's lifecycle. Aerobic methanotrophs were repeatedly found in leachate where low levels of oxygen were present and exhibited adaptations that aid survival under steep redox gradients in landfills. The potential for anaerobic methane oxidation, which has historically been overlooked despite anoxic habitats dominating landfills, was prevalent in a 26-year-old landfill cell which was in a state of slow methanogenesis. Finally, we identified the metabolic potential for methane oxidation in lineages that are widespread in aquatic and terrestrial habitats, whose capacity to metabolize methane remains poorly characterized. Ultimately, this work expands the diversity of methane cycling guilds in landfills and outlines how these communities can curb methane emissions from municipal solid waste.

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Section: Resultssupporting

confidence: 66%

Section: Resultsmentioning

confidence: 99%

Section: Phylogenomic Analyses Of Families With No Known Capacity For...mentioning

confidence: 99%

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Microbial methane cycling in a landfill on a decadal time scale

Grégoire

George

Hug

2023

Preprint

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“…To date, two distinct varieties of MMOs have been elucidated. One is the diiron-containing soluble methane monooxygenase (sMMO) from which an extensive array of structural and spectroscopic insights has been garnered. ,− The alternative family is the membrane-bound and copper-containing particulate methane monooxygenase (pMMO). − ,− Across all methanotrophs, pMMO expression is pervasive, enabling methane-utilizing bacteria to annually consume tens of millions of metric tons of atmospheric methane. ,,, …”

Section: Introductionmentioning

confidence: 99%

Unraveling the Valence State and Reactivity of Copper Centers in Membrane-Bound Particulate Methane Monooxygenase

Peng,

Wang,

Zhang

et al. 2023

J. Am. Chem. Soc.

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Particulate methane monooxygenase (pMMO) plays a critical role in catalyzing the conversion of methane to methanol, constituting the initial step in the C1 metabolic pathway within methanotrophic bacteria. However, the membrane-bound pMMO’s structure and catalytic mechanism, notably the copper’s valence state and genuine active site for methane oxidation, have remained elusive. Based on the recently characterized structure of membrane-bound pMMO, extensive computational studies were conducted to address these long-standing issues. A comprehensive analysis comparing the quantum mechanics/molecular mechanics (QM/MM) molecular dynamics (MD) simulated structures with cryo-EM data indicates that both the CuC and CuD sites tend to stay in the Cu(I) valence state within the membrane environment. Additionally, the concurrent presence of Cu(I) at both CuC and CuD sites leads to the significant reduction of the ligand-binding cavity situated between them, making it less likely to accommodate a reductant molecule such as durohydroquinone (DQH2). Subsequent QM/MM calculations reveal that the CuD(I) site is more reactive than the CuC(I) site in oxygen activation, en route to H2O2 formation and the generation of Cu(II)–O•– species. Finally, our simulations demonstrate that the natural reductant ubiquinol (CoQH2) assumes a productive binding conformation at the CuD(I) site but not at the CuC(I) site. This provides evidence that the true active site of membrane-bound pMMOs may be CuD rather than CuC. These findings clarify pMMO’s catalytic mechanism and emphasize the membrane environment’s pivotal role in modulating the coordination structure and the activity of copper centers within pMMO.

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“…In particular in wetlands and landfills, methanotrophs also remove CH 4 produced in the soil by methanogenic archaea, and functionally thus act as a “biofilter” that eliminates a large fraction of potential soil CH 4 emissions (Conrad, 2009). Methanotrophic bacteria belong to either the Gammaproteobacteria (type I methanotrophs), Alphaproteobacteria (type II methanotrophs), Verrucomicrobia (type III methanotrophs; Knief, 2015; McDonald et al, 2008), or to a newly discovered methanotrophic type of Actinobacteria (van Spanning et al, 2022). In typical habitats, their diversity rarely exceeds a few dozen strains.…”

Section: Introductionmentioning

confidence: 99%

Experimental erosion of microbial diversity decreases soil CH₄ consumption rates

Schnyder,

Bodelier,

Hartmann

et al. 2023

Ecology

Self Cite

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Biodiversity‐ecosystem functioning (BEF) experiments have predominantly focused on communities of higher organisms, in particular plants, with comparably little known to date about the relevance of biodiversity for microbially‐driven biogeochemical processes. Methanotrophic bacteria play a key role in Earth's methane (CH4) cycle by removing atmospheric CH4 and reducing emissions from methanogenesis in wetlands and landfills. Here, we used a dilution‐to‐extinction approach to simulate diversity loss in a methanotrophic landfill cover soil community. Replicate samples were diluted 101 to 107‐fold, pre‐incubated under a high CH4 atmosphere for microbial communities to recover to comparable size, and then incubated for 86 days at constant or diurnally‐cycling temperature. We hypothesize that (1) CH4 consumption decreases as methanotrophic diversity is lost, and (2) this effect is more pronounced under variable temperature. Net CH4 consumption was determined by gas chromatography. Microbial community composition was determined by DNA extraction and sequencing of amplicons specific to methanotrophs and bacteria (pmoA and 16S gene fragments). The richness of operational taxonomic units (OTU) of methanotrophic and non‐methanotrophic bacteria decreased approximately linearly with log‐dilution. CH4 consumption decreased with the number of OTUs lost, independent of community size. These effects were independent of temperature cycling. The diversity effects we found occurred in relatively diverse communities, challenging the notion of high functional redundancy mediating high resistance to diversity erosion in natural microbial systems. The effects also resemble the ones for higher organisms, suggesting that BEF‐relationships are universal across taxa and spatial scales.

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Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

Cited by 27 publications

References 72 publications

Microbial methane cycling in a landfill on a decadal time scale

Microbial methane cycling in a landfill on a decadal time scale

Unraveling the Valence State and Reactivity of Copper Centers in Membrane-Bound Particulate Methane Monooxygenase

Experimental erosion of microbial diversity decreases soil CH₄ consumption rates

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Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

Cited by 27 publications

References 72 publications

Microbial methane cycling in a landfill on a decadal time scale

Microbial methane cycling in a landfill on a decadal time scale

Unraveling the Valence State and Reactivity of Copper Centers in Membrane-Bound Particulate Methane Monooxygenase

Experimental erosion of microbial diversity decreases soil CH4 consumption rates

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Experimental erosion of microbial diversity decreases soil CH₄ consumption rates