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1. Phylogenomic analysis of novel Diaforarchaea is consistent with sulfite but not sulfate reduction in volcanic environments on early Earth

   https://doi.org/10.1038/s41396-020-0611-9  

   Colman, Daniel R.; Lindsay, Melody R.; Amenabar, Maximiliano J.; Fernandes-Martins, Maria C.; Roden, Eric R.; Boyd, Eric S. (February 2020, The ISME Journal)

   Abstract The origin(s) of dissimilatory sulfate and/or (bi)sulfite reducing organisms (SRO) remains enigmatic despite their importance in global carbon and sulfur cycling since at least 3.4 Ga. Here, we describe novel, deep-branching archaeal SRO populations distantly related to other Diaforarchaea from two moderately acidic thermal springs. Dissimilatory (bi)sulfite reductase homologs, DsrABC, encoded in metagenome assembled genomes (MAGs) from spring sediments comprise one of the earliest evolving Dsr lineages. DsrA homologs were expressed in situ under moderately acidic conditions. MAGs lacked genes encoding proteins that activate sulfate prior to (bi)sulfite reduction. This is consistent with sulfide production in enrichment cultures provided sulfite but not sulfate. We suggest input of volcanic sulfur dioxide to anoxic spring-water yields (bi)sulfite and moderately acidic conditions that favor its stability and bioavailability. The presence of similar volcanic springs at the time SRO are thought to have originated (>3.4 Ga) may have supplied (bi)sulfite that supported ancestral SRO. These observations coincide with the lack of inferred SO42− reduction capacity in nearly all organisms with early-branching DsrAB and which are near universally found in hydrothermal environments. 

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2. Ecological Dichotomies Arise in Microbial Communities Due to Mixing of Deep Hydrothermal Waters and Atmospheric Gas in a Circumneutral Hot Spring

   https://doi.org/10.1128/AEM.01598-21  

   Fernandes-Martins, Maria C.; Keller, Lisa M.; Munro-Ehrlich, Mason; Zimlich, Kathryn R.; Mettler, Madelyn K.; England, Alexis M.; Clare, Rita; Surya, Kevin; Shock, Everett L.; Colman, Daniel R.; et al (November 2021, Applied and Environmental Microbiology)

   Semrau, Jeremy D. (Ed.)

   ABSTRACT Little is known of how the confluence of subsurface and surface processes influences the assembly and habitability of hydrothermal ecosystems. To address this knowledge gap, the geochemical and microbial composition of a high-temperature, circumneutral hot spring in Yellowstone National Park was examined to identify the sources of solutes and their effect on the ecology of microbial inhabitants. Metagenomic analysis showed that populations comprising planktonic and sediment communities are archaeal dominated, are dependent on chemical energy (chemosynthetic), share little overlap in their taxonomic composition, and are differentiated by their inferred use of/tolerance to oxygen and mode of carbon metabolism. The planktonic community is dominated by putative aerobic/aerotolerant autotrophs, while the taxonomic composition of the sediment community is more evenly distributed and comprised of anaerobic heterotrophs. These observations are interpreted to reflect sourcing of the spring by anoxic, organic carbon-limited subsurface hydrothermal fluids and ingassing of atmospheric oxygen that selects for aerobic/aerotolerant organisms that have autotrophic capabilities in the water column. Autotrophy and consumption of oxygen by the planktonic community may influence the assembly of the anaerobic and heterotrophic sediment community. Support for this inference comes from higher estimated rates of genome replication in planktonic populations than sediment populations, indicating faster growth in planktonic populations. Collectively, these observations provide new insight into how mixing of subsurface waters and atmospheric oxygen create dichotomy in the ecology of hot spring communities and suggest that planktonic and sediment communities may have been less differentiated taxonomically and functionally prior to the rise of oxygen at ∼2.4 billion years ago (Gya). IMPORTANCE Understanding the source and availability of energy capable of supporting life in hydrothermal environments is central to predicting the ecology of microbial life on early Earth when volcanic activity was more widespread. Little is known of the substrates supporting microbial life in circumneutral to alkaline springs, despite their relevance to early Earth habitats. Using metagenomic and informatics approaches, water column and sediment habitats in a representative circumneutral hot spring in Yellowstone were shown to be dichotomous, with the former largely hosting aerobic/aerotolerant autotrophs and the latter primarily hosting anaerobic heterotrophs. This dichotomy is attributed to influx of atmospheric oxygen into anoxic deep hydrothermal spring waters. These results indicate that the ecology of microorganisms in circumneutral alkaline springs sourced by deep hydrothermal fluids was different prior to the rise of atmospheric oxygen ∼2.4 Gya, with planktonic and sediment communities likely to be less differentiated than contemporary circumneutral hot springs. 

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3. Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost

   https://doi.org/10.1128/msystems.00698-23  

   Ellenbogen, Jared B; Borton, Mikayla A; McGivern, Bridget B; Cronin, Dylan R; Hoyt, David W; Freire-Zapata, Viviana; McCalley, Carmody K; Varner, Ruth K; Crill, Patrick M; Wehr, Richard A; et al (January 2024, mSystems)

   Hernandez, Marcela (Ed.)

   ABSTRACT While wetlands are major sources of biogenic methane (CH₄), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH₄emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methanogenesis in the thawing permafrost peatland of Stordalen Mire in Arctic Sweden. In quadrupling the genomic representation of the site’s methanogens and examining their encoded metabolism, we revealed that nearly 20% of the metagenome-assembled genomes (MAGs) encoded the potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; forMethanosarcinalesandMethanobacterialesMAGs, these data indicated the use of methylated oxygen compounds (e.g., methanol), while forMethanomassiliicoccales, they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1,700 bacterial MAGs across 19 phyla encoded anaerobic methylotrophic potential, with expression across 12 phyla. Metabolomic analyses revealed the presence of diverse methylated compounds in the Mire, including some known methylotrophic substrates. Active methylotrophy was observed across all stages of a permafrost thaw gradient in Stordalen, with the most frozen non-methanogenic palsa found to host bacterial methylotrophy and the partially thawed bog and fully thawed fen seen to house both methanogenic and bacterial methylotrophic activities. Methanogenesis across increasing permafrost thaw is thus revised from the sole dominance of hydrogenotrophic production and the appearance of acetoclastic at full thaw to consider the co-occurrence of methylotrophy throughout. Collectively, these findings indicate that methanogenic and bacterial methylotrophy may be an important and previously underappreciated component of carbon cycling and emissions in these rapidly changing wetland habitats. IMPORTANCEWetlands are the biggest natural source of atmospheric methane (CH₄) emissions, yet we have an incomplete understanding of the suite of microbial metabolism that results in CH₄formation. Specifically, methanogenesis from methylated compounds is excluded from all ecosystem models used to predict wetland contributions to the global CH₄budget. Though recent studies have shown methylotrophic methanogenesis to be active across wetlands, the broad climatic importance of the metabolism remains critically understudied. Further, some methylotrophic bacteria are known to produce methanogenic by-products like acetate, increasing the complexity of the microbial methylotrophic metabolic network. Prior studies of Stordalen Mire have suggested that methylotrophic methanogenesis is irrelevantin situand have not emphasized the bacterial capacity for metabolism, both of which we countered in this study. The importance of our findings lies in the significant advancement toward unraveling the broader impact of methylotrophs in wetland methanogenesis and, consequently, their contribution to the terrestrial global carbon cycle. 

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4. Travertine records climate-induced transformations of the Yellowstone hydrothermal system from the late Pleistocene to the present

   https://doi.org/10.1130/B37317.1  

   Harrison, Lauren N.; Hurwitz, Shaul; Paces, James B.; Whitlock, Cathy; Peek, Sara; Licciardi, Joseph (February 2024, Geological Society of America Bulletin)

   Chemical changes in hot springs, as recorded by thermal waters and their deposits, provide a window into the evolution of the postglacial hydrothermal system of the Yellowstone Plateau Volcanic Field. Today, most hydrothermal travertine forms to the north and south of the ca. 631 ka Yellowstone caldera where groundwater flow through subsurface sedimentary rocks leads to calcite saturation at hot springs. In contrast, low-Ca rhyolites dominate the subsurface within the Yellowstone caldera, resulting in thermal waters that rarely deposit travertine. We investigated the timing and origin of five small travertine deposits in the Upper and Lower Geyser Basins to understand the conditions that allowed for travertine deposition. New 230Th-U dating, oxygen (δ18O), carbon (δ13C), and strontium (87Sr/86Sr) isotopic ratios, and elemental concentrations indicate that travertine deposits within the Yellowstone caldera formed during three main episodes that correspond broadly with known periods of wet climate: 13.9−13.6 ka, 12.2−9.5 ka, and 5.2−2.9 ka. Travertine deposition occurred in response to the influx of large volumes of cold meteoric water, which increased the rate of chemical weathering of surficial sediments and recharge into the hydrothermal system. The small volume of intracaldera travertine does not support a massive postglacial surge of CO2 within the Yellowstone caldera, nor was magmatic CO2 the catalyst for postglacial travertine deposition. 

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

   https://doi.org/10.1038/s43705-023-00225-9  

   Lynes, Mackenzie M.; Krukenberg, Viola; Jay, Zackary J.; Kohtz, Anthony J.; Gobrogge, Christine A.; Spietz, Rachel L.; Hatzenpichler, Roland (March 2023, ISME Communications)

   Abstract Metagenomic studies on geothermal environments have been central in recent discoveries on the diversity of archaeal methane and alkane metabolism. Here, we investigated methanogenic populations inhabiting terrestrial geothermal features in Yellowstone National Park (YNP) by combining amplicon sequencing with metagenomics and mesocosm experiments. Detection of methyl-coenzyme M reductase subunit A (mcrA) gene amplicons demonstrated a wide diversity of Mcr-encoding archaea inhabit geothermal features with differing physicochemical regimes across YNP. From three selected hot springs we recovered twelve Mcr-encoding metagenome assembled genomes (MAGs) affiliated with lineages of cultured methanogens as well as Candidatus (Ca.) Methanomethylicia, Ca. Hadesarchaeia, and Archaeoglobi. These MAGs encoded the potential for hydrogenotrophic, aceticlastic, hydrogen-dependent methylotrophic methanogenesis, or anaerobic short-chain alkane oxidation. While Mcr-encoding archaea represent minor fractions of the microbial community of hot springs, mesocosm experiments with methanogenic precursors resulted in the stimulation of methanogenic activity and the enrichment of lineages affiliated with Methanosaeta and Methanothermobacter as well as with uncultured Mcr-encoding archaea including Ca. Korarchaeia, Ca. Nezhaarchaeia, and Archaeoglobi. We revealed that diverse Mcr-encoding archaea with the metabolic potential to produce methane from different precursors persist in the geothermal environments of YNP and can be enriched under methanogenic conditions. This study highlights the importance of combining environmental metagenomics with laboratory-based experiments to expand our understanding of uncultured Mcr-encoding archaea and their potential impact on microbial carbon transformations in geothermal environments and beyond. 

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