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1. Well-hidden methanogenesis in deep, organic-rich sediments of Guaymas Basin

   https://doi.org/10.1038/s41396-023-01485-y  

   Bojanova, Diana P.; De Anda, Valerie Y.; Haghnegahdar, Mojhgan A.; Teske, Andreas P.; Ash, Jeanine L.; Young, Edward D.; Baker, Brett J.; LaRowe, Douglas E.; Amend, Jan P. (November 2023, The ISME Journal)

   Abstract Deep marine sediments (>1mbsf) harbor ~26% of microbial biomass and are the largest reservoir of methane on Earth. Yet, the deep subsurface biosphere and controls on its contribution to methane production remain underexplored. Here, we use a multidisciplinary approach to examine methanogenesis in sediments (down to 295 mbsf) from sites with varying degrees of thermal alteration (none, past, current) at Guaymas Basin (Gulf of California) for the first time. Traditional (¹³C/¹²C and D/H) and multiply substituted (¹³CH₃D and¹²CH₂D₂) methane isotope measurements reveal significant proportions of microbial methane at all sites, with the largest signal at the site with past alteration. With depth, relative microbial methane decreases at differing rates between sites. Gibbs energy calculations confirm methanogenesis is exergonic in Guaymas sediments, with methylotrophic pathways consistently yielding more energy than the canonical hydrogenotrophic and acetoclastic pathways. Yet, metagenomic sequencing and cultivation attempts indicate that methanogens are present in low abundance. We find only one methyl-coenzyme M (mcrA) sequence within the entire sequencing dataset. Also, we identify a wide diversity of methyltransferases (mtaB, mttB), but only a few sequences phylogenetically cluster with methylotrophic methanogens. Our results suggest that the microbial methane in the Guaymas subsurface was produced over geologic time by relatively small methanogen populations, which have been variably influenced by thermal sediment alteration. Higher resolution metagenomic sampling may clarify the modern methanogen community. This study highlights the importance of using a multidisciplinary approach to capture microbial influences in dynamic, deep subsurface settings like Guaymas Basin. 

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2. Radiolytically reworked Archean organic matter in a habitable deep ancient high-temperature brine

   https://doi.org/10.1038/s41467-023-41900-8  

   Nisson, Devan M; Walters, Clifford C; Chacón-Patiño, Martha L; Weisbrod, Chad R; Kieft, Thomas L; Sherwood_Lollar, Barbara; Warr, Oliver; Castillo, Julio; Perl, Scott M; Cason, Errol D; et al (December 2023, Nature Communications)

   Abstract Investigations of abiotic and biotic contributions to dissolved organic carbon (DOC) are required to constrain microbial habitability in continental subsurface fluids. Here we investigate a large (101–283 mg C/L) DOC pool in an ancient (>1Ga), high temperature (45–55 °C), low biomass (10²−10⁴cells/mL), and deep (3.2 km) brine from an uranium-enriched South African gold mine. Excitation-emission matrices (EEMs), negative electrospray ionization (–ESI) 21 tesla Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR MS), and amino acid analyses suggest the brine DOC is primarily radiolytically oxidized kerogen-rich shales or reefs, methane and ethane, with trace amounts of C₃–C₆hydrocarbons and organic sulfides. δ²H and δ¹³C of C₁–C₃hydrocarbons are consistent with abiotic origins. These findings suggest water-rock processes control redox and C cycling, helping support a meagre, slow biosphere over geologic time. A radiolytic-driven, habitable brine may signal similar settings are good targets in the search for life beyond Earth. 

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3. Hydrogenotrophic methanogens overwrite isotope signals of subsurface methane

   https://doi.org/10.1126/science.ado0126  

   Mayumi, Daisuke; Tamaki, Hideyuki; Kato, Souichiro; Igarashi, Kensuke; Lalk, Ellen; Nishikawa, Yasunori; Minagawa, Hideki; Sato, Tomoyuki; Ono, Shuhei; Kamagata, Yoichi; et al (December 2024, Science)

   Methane, a greenhouse gas and energy source, is commonly studied using stable isotope signals as proxies for its formation processes. In subsurface environments, methane often exhibits equilibrium isotopic signals, but the equilibration process has never been demonstrated in the laboratory. We cocultured a hydrogenotrophic methanogen with an H₂-producing bacterium under conditions (55°C, 10 megapascals) simulating a methane-bearing subsurface. This resulted in near-complete reversibility of methanogenesis, leading to equilibria for both hydrogen and carbon isotopes. The methanogen not only equilibrated kinetic isotope signals of initially produced methane but also modified the isotope signals of amended thermogenic methane. These findings suggest that hydrogenotrophic methanogenesis can overwrite the isotope signals of subsurface methane, distorting proxies for its origin and formation temperature—insights crucial for natural gas exploration. 

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4. Primary to post‐depositional microbial controls on the stable and clumped isotope record of shoreline sediments at Fayetteville Green Lake

   https://doi.org/10.1111/gbi.12609  

   Leapaldt, Hanna C; Frantz, Carie M; Olsen‐Valdez, Juliana; Snell, Kathryn E; Trower, Elizabeth J; Ingalls, Miquela (July 2024, Geobiology)

   Abstract Lacustrine carbonates are a powerful archive of paleoenvironmental information but are susceptible to post‐depositional alteration. Microbial metabolisms can drive such alteration by changing carbonate saturationin situ, thereby driving dissolution or precipitation. The net impact these microbial processes have on the primary δ¹⁸O, δ¹³C, and Δ₄₇values of lacustrine carbonate is not fully known. We studied the evolution of microbial community structure and the porewater and sediment geochemistry in the upper ~30 cm of sediment from two shoreline sites at Green Lake, Fayetteville, NY over 2 years of seasonal sampling. We linked seasonal and depth‐based changes of porewater carbonate chemistry to microbial community composition, in situ carbon cycling (using δ¹³C values of carbonate, dissolved inorganic carbon (DIC), and organic matter), and dominant allochems and facies. We interpret that microbial processes are a dominant control on carbon cycling within the sediment, affecting porewater DIC, aqueous carbon chemistry, and carbonate carbon and clumped isotope geochemistry. Across all seasons and sites, microbial organic matter remineralization lowers the δ¹³C of the porewater DIC. Elevated carbonate saturation states in the sediment porewaters (Ω > 3) were attributed to microbes from groups capable of sulfate reduction, which were abundant in the sediment below 5 cm depth. The nearshore carbonate sediments at Green Lake are mainly composed of microbialite intraclasts/oncoids, charophytes, larger calcite crystals, and authigenic micrite—each with a different origin. Authigenic micrite is interpreted to have precipitated in situ from the supersaturated porewaters from microbial metabolism. The stable carbon isotope values (δ¹³C_carb) and clumped isotope values (Δ₄₇) of bulk carbonate sediments from the same depth horizons and site varied depending on both the sampling season and the specific location within a site, indicating localized (μm to mm) controls on carbon and clumped isotope values. Our results suggest that biological processes are a dominant control on carbon chemistry within the sedimentary subsurface of the shorelines of Green Lake, from actively forming microbialites to pore space organic matter remineralization and micrite authigenesis. A combination of biological activity, hydrologic balance, and allochem composition of the sediments set the stable carbon, oxygen, and clumped isotope signals preserved by the Green Lake carbonate sediments. 

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5. Cryptic Methane-Cycling by Methanogens During Multi-Year Incubation of Estuarine Sediment

   https://doi.org/10.3389/fmicb.2022.847563  

   Kevorkian, Richard T.; Sipes, Katie; Winstead, Rachel; Paul, Raegan; Lloyd, Karen G. (March 2022, Frontiers in Microbiology)

   As marine sediments are buried, microbial communities transition from sulfate-reduction to methane-production after sulfate is depleted. When this biogenic methane diffuses into the overlying sulfate-rich sediments, it forms a sulfate-methane transition zone (SMTZ) because sulfate reducers deplete hydrogen concentrations and make hydrogenotrophic methanogenesis exergonic in the reverse direction, a process called the anaerobic oxidation of methane (AOM). Microbial participation in these processes is often inferred from geochemistry, genes, and gene expression changes with sediment depth, using sedimentation rates to convert depth to time. Less is known about how natural sediments transition through these geochemical states transition in real-time. We examined 16S rRNA gene amplicon libraries and metatranscriptomes in microcosms of anoxic sediment from the White Oak River estuary, NC, with three destructively sampled replicates with methane added (586-day incubations) and three re-sampled un-amended replicates (895-day incubations). Sulfate dropped to a low value (∼0.3 mM) on similar days for both experiments (312 and 320 days, respectively), followed by a peak in hydrogen, intermittent increases in methane-cycling archaea starting on days 375 and 362 (mostly Methanolinea spp. and Methanosaeta spp., and Methanococcoides sp. ANME-3), and a methane peak 1 month later. However, methane δ 13 C values only show net methanogenesis 6 months after methane-cycling archaea increase and 4 months after the methane peak, when sulfate is consistently below 0.1 mM and hydrogen increases to a stable 0.61 ± 0.13 nM (days 553–586, n = 9). Sulfate-reducing bacteria (mostly Desulfatiglans spp. and Desulfosarcina sp. SEEP-SRB1) increase in relative abundance only during this period of net methane production, suggesting syntrophy with methanogens in the absence of sulfate. The transition from sulfate reduction to methane production in marine sediments occurs through a prolonged period of methane-cycling by methanogens at low sulfate concentrations, and steady growth of sulfate reducers along with methanogens after sulfate is depleted. 

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