Diversity and function of methyl-coenzyme M reductase-encoding archaea in Yellowstone hot springs revealed by metagenomics and mesocosm experiments

Lynes, Mackenzie M.; Krukenberg, Viola; Jay, Zackary J.; Kohtz, Anthony J.; Gobrogge, Christine A.; Spietz, Rachel L.; Hatzenpichler, Roland

doi:10.1038/s43705-023-00225-9

Cited by 18 publications

(17 citation statements)

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“…S1, S2). Based on AAI, MAG LCB24 was most closely related to Archaeoglobi LCB024-003 MAG (AAI, 98.6%), which we had obtained from the same hot spring in a previous study (33). The ANI and AAI values to the closest cultured methanogen, Ca.…”

Section: Resultsmentioning

confidence: 61%

“…In our recent survey on the diversity of Mcr-encoding archaea in the geothermal features of YNP, mesocosms seeded with biomass from a hot spring located within the Lower Culex Basin (LCB024; pH 7-8, 56-74 °C), had shown potential to enrich for methanogenic Archaeoglobi (33). Using a sediment slurry collected from LCB024, we initiated incubations supplied with monomethylamine (MMA) and antibiotics incubated in anoxic media (pH 7.8, 70 °C) under a N 2 headspace.…”

Section: Resultsmentioning

confidence: 99%

“…In addition, mcrA gene ASVs affiliated with Archaeoglobi were PCR-amplified from 53 DNA samples. These were collected from microbial mats or sediments originating from 36 geothermal features distributed across various thermal regions within YNP by Lynes, Krukenberg et al (33). Archaeoglobi-related mcrA genes were found in geothermal features with a pH range of 2.61 to 9.32 and a temperature range of 18.4 °C to 93.8 °C.…”

Section: Resultsmentioning

confidence: 99%

“…In November 2021, a slurry of sediment and water (1:9) was collected from an unnamed hot spring in the Lower Culex Basin of Yellowstone National Park (YNP), WY, USA. In our previous survey of Mcr-encoding archaea in YNP (33), this hot spring was given the identifier LCB024 (44.573294, −110.795388; pH 7.8, 67 °C). A mixture of surface sediment (~1-2 cm deep) and hot spring water was collected into a glass bottle and sealed headspace-free with a thick butyl rubber stopper.…”

Section: Methodsmentioning

confidence: 99%

“…Liu et al reported the in situ expression of genes related to hydrogen-dependent methylotrophic methanogenesis and heterotrophic fermentation within populations of Archaeoglobi in a high-temperature oil reservoir (28). 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).…”

Section: Introductionmentioning

confidence: 99%

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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: Resultsmentioning

confidence: 61%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%