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Item Acquisition of elemental sulfur by sulfur-oxidising Sulfolobales(Wiley, 2024-08) Fernandes-Martins, Maria C.; Springer, Carli; Colman, Daniel R.; Boyd, Eric S.Elemental sulfur (S80)-oxidising Sulfolobales (Archaea) dominate high-temperature acidic hot springs (>80°C, pH <4). However, genomic analyses of S80-oxidising members of the Sulfolobales reveal a patchy distribution of genes encoding sulfur oxygenase reductase (SOR), an S80 disproportionating enzyme attributed to S80 oxidation. Here, we report the S80-dependent growth of two Sulfolobales strains previously isolated from acidic hot springs in Yellowstone National Park, one of which associated with bulk S80 during growth and one that did not. The genomes of each strain encoded different sulfur metabolism enzymes, with only one encoding SOR. Dialysis membrane experiments showed that direct contact is not required for S80 oxidation in the SOR-encoding strain. This is attributed to the generation of hydrogen sulfide (H2S) from S80 disproportionation that can diffuse out of the cell to solubilise bulk S80 to form soluble polysulfides (Sx2−) and/or S80 nanoparticles that readily diffuse across dialysis membranes. The Sulfolobales strain lacking SOR required direct contact to oxidise S80, which could be overcome by the addition of H2S. High concentrations of S80 inhibited the growth of both strains. These results implicate alternative strategies to acquire and metabolise sulfur in Sulfolobales and have implications for their distribution and ecology in their hot spring habitats.Item Covariation of hot spring geochemistry with microbial genomic diversity, function, and evolution(Springer Science and Business Media LLC, 2024-08) Colman, Daniel R.; Keller, Lisa M.; Arteaga-Pozo, Emilia; Andrade-Barahona, Eva; St. Clair, Brian; Shoemaker, Anna; Cox, Alysia; Boyd, Eric S.The geosphere and the microbial biosphere have co-evolved for ~3.8 Ga, with many lines of evidence suggesting a hydrothermal habitat for life’s origin. However, the extent that contemporary thermophiles and their hydrothermal habitats reflect those that likely existed on early Earth remains unknown. To address this knowledge gap, 64 geochemical analytes were measured and 1022 metagenome-assembled-genomes (MAGs) were generated from 34 chemosynthetic high-temperature springs in Yellowstone National Park and analysed alongside 444 MAGs from 35 published metagenomes. We used these data to evaluate co-variation in MAG taxonomy, metabolism, and phylogeny as a function of hot spring geochemistry. We found that cohorts of MAGs and their functions are discretely distributed across pH gradients that reflect different geochemical provinces. Acidic or circumneutral/alkaline springs harbor MAGs that branched later and are enriched in sulfur- and arsenic-based O2-dependent metabolic pathways that are inconsistent with early Earth conditions. In contrast, moderately acidic springs sourced by volcanic gas harbor earlier-branching MAGs that are enriched in anaerobic, gas-dependent metabolisms (e.g. H2, CO2, CH4 metabolism) that have been hypothesized to support early microbial life. Our results provide insight into the influence of redox state in the eco-evolutionary feedbacks between thermophiles and their habitats and suggest moderately acidic springs as early Earth analogs.Item Wood–Ljungdahl pathway encoding anaerobes facilitate low-cost primary production in hypersaline sediments at Great Salt Lake, Utah(Oxford University Press, 2024-07) Shoemaker, Anna; Maritan, Andrew; Cosar, Su; Nupp, Sylvia; Menchaca, Ana; Jackson, Thomas; Dang, Aria; Baxter, Bonnie K.; Colman, Daniel R.; Dunham, Eric C.; Boyd, Eric S.Little is known of primary production in dark hypersaline ecosystems despite the prevalence of such environments on Earth today and throughout its geologic history. Here, we generated and analyzed metagenome-assembled genomes (MAGs) organized as operational taxonomic units (OTUs) from three depth intervals along a 30-cm sediment core from the north arm of Great Salt Lake, Utah. The sediments and associated porewaters were saturated with NaCl, exhibited redox gradients with depth, and harbored nitrogen-depleted organic carbon. Metabolic predictions of MAGs representing 36 total OTUs recovered from the core indicated that communities transitioned from aerobic and heterotrophic at the surface to anaerobic and autotrophic at depth. Dark CO2 fixation was detected in sediments and the primary mode of autotrophy was predicted to be via the Wood–Ljungdahl pathway. This included novel hydrogenotrophic acetogens affiliated with the bacterial class Candidatus Bipolaricaulia. Minor populations were dependent on the Calvin cycle and the reverse tricarboxylic acid cycle, including in a novel Thermoplasmatota MAG. These results are interpreted to reflect the favorability of and selectability for populations that operate the lowest energy requiring CO2-fixation pathway known, the Wood–Ljungdahl pathway, in anoxic and hypersaline conditions that together impart a higher energy demand on cells.Item Sulfide oxidation by members of the Sulfolobales(Oxford University Press, 2024-05) Fernandes-Martins, Maria C.; Colman, Daniel R.; Boyd, Eric S.The oxidation of sulfur compounds drives the acidification of geothermal waters. At high temperatures (>80°C) and in acidic conditions (pH <6.0), oxidation of sulfide has historically been considered an abiotic process that generates elemental sulfur (S0) that, in turn, is oxidized by thermoacidophiles of the model archaeal order Sulfolobales to generate sulfuric acid (i.e. sulfate and protons). Here, we describe five new aerobic and autotrophic strains of Sulfolobales comprising two species that were isolated from acidic hot springs in Yellowstone National Park (YNP) and that can use sulfide as an electron donor. These strains significantly accelerated the rate and extent of sulfide oxidation to sulfate relative to abiotic controls, concomitant with production of cells. Yields of sulfide-grown cultures were ∼2-fold greater than those of S0-grown cultures, consistent with thermodynamic calculations indicating more available energy in the former condition than the latter. Homologs of sulfide:quinone oxidoreductase (Sqr) were identified in nearly all Sulfolobales genomes from YNP metagenomes as well as those from other reference Sulfolobales, suggesting a widespread ability to accelerate sulfide oxidation. These observations expand the role of Sulfolobales in the oxidative sulfur cycle, the geobiological feedbacks that drive the formation of acidic hot springs, and landscape evolution.Item Relationships between fluid mixing, biodiversity, and chemosynthetic primary productivity in Yellowstone hot springs(Wiley, 2023-01) Fernandes‐Martins, Maria C.; Colman, Daniel R.; Boyd, Eric S.The factors that influence biodiversity and productivity of hydrothermal ecosystems are not well understood. Here we investigate the relationship between fluid mixing, biodiversity, and chemosynthetic primary productivity in three co-localized hot springs (RSW, RSN, and RSE) in Yellowstone National Park that have different geochemistry. All three springs are sourced by reduced hydrothermal fluid, but RSE and RSN receive input of vapour phase gas and oxidized groundwaters, with input of both being substantially higher in RSN. Metagenomic sequencing revealed that communities in RSN were more biodiverse than those of RSE and RSW in all dimensions evaluated. Microcosm activity assays indicate that rates of dissolved inorganic carbon (DIC) uptake were also higher in RSN than in RSE and RSW. Together, these results suggest that increased mixing of reduced volcanic fluid with oxidized fluids generates additional niche space capable of supporting increasingly biodiverse communities that are more productive. These results provide insight into the factors that generate and maintain chemosynthetic biodiversity in hydrothermal systems and that influence the distribution, abundance, and diversity of microbial life in communities supported by chemosynthesis. These factors may also extend to other ecosystems not supported by photosynthesis, including the vast subterranean biosphere and biospheres beneath ice sheets and glaciers.Item Ecological dichotomies arise in microbial communities due to mixing of deep hydrothermal waters and atmospheric gas in a circumneutral hot spring.(American Society for Microbiology, 2021-09) 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.; Boyd, Eric S.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.Item Diversification of methanogens into hyperalkaline serpentinizing environments through adaptations to minimize oxidant limitation(Springer Science and Business Media LLC, 2020-11) Fones, Elizabeth M.; Colman, Daniel R.; Kraus, Emily A.; Stepanauskas, Ramunas; Templetin, Alexis S.; Spear, John R.; Boyd, Eric S.Metagenome assembled genomes (MAGs) and single amplified genomes (SAGs) affiliated with two distinct Methanobacterium lineages were recovered from subsurface fracture waters of the Samail Ophiolite, Sultanate of Oman. Lineage Type I was abundant in waters with circumneutral pH, whereas lineage Type II was abundant in hydrogen rich, hyperalkaline waters. Type I encoded proteins to couple hydrogen oxidation to CO2 reduction, typical of hydrogenotrophic methanogens. Surprisingly, Type II, which branched from the Type I lineage, lacked homologs of two key oxidative [NiFe]-hydrogenases. These functions were presumably replaced by formate dehydrogenases that oxidize formate to yield reductant and cytoplasmic CO2 via a pathway that was unique among characterized Methanobacteria, allowing cells to overcome CO2/oxidant limitation in high pH waters. This prediction was supported by microcosm-based radiotracer experiments that showed significant biological methane generation from formate, but not bicarbonate, in waters where the Type II lineage was detected in highest relative abundance. Phylogenetic analyses and variability in gene content suggested that recent and ongoing diversification of the Type II lineage was enabled by gene transfer, loss, and transposition. These data indicate that selection imposed by CO2/oxidant availability drove recent methanogen diversification into hyperalkaline waters that are heavily impacted by serpentinization.Item Pathways of Iron and Sulfur Acquisition, Cofactor Assembly, Destination, and Storage in Diverse Archaeal Methanogens and Alkanotrophs(2021-08) Johnson, Christina; England, Alexis; Munro-Ehrlich, Mason; Colman, Daniel R.; DuBois, Jennifer L.; Boyd, Eric S.Archaeal methanogens, methanotrophs, and alkanotrophs have a high demand for iron (Fe) and sulfur (S); however, little is known of how they acquire, traffic, deploy, and store these elements. Here, we examined the distribution of homologs of proteins mediating key steps in Fe/S metabolism in model microorganisms, including iron(II) sensing/uptake (FeoAB), sulfide extraction from cysteine (SufS), and the biosynthesis of iron-sulfur [Fe-S] clusters (SufBCDE), siroheme (Pch2 dehydrogenase), protoheme (AhbABCD), cytochrome c (Cyt c) (CcmCF), and iron storage/detoxification (Bfr, FtrA, and IssA), among 326 publicly available, complete or metagenome-assembled genomes of archaeal methanogens/methanotrophs/alkanotrophs. The results indicate several prevalent but nonuniversal features, including FeoB, SufBC, and the biosynthetic apparatus for the basic tetrapyrrole scaffold, as well as its siroheme (and F430) derivatives. However, several early-diverging genomes lacked SufS and pathways to synthesize and deploy heme. Genomes encoding complete versus incomplete heme biosynthetic pathways exhibited equivalent prevalences of [Fe-S] cluster binding proteins, suggesting an expansion of catalytic capabilities rather than substitution of heme for [Fe-S] in the former group. Several strains with heme binding proteins lacked heme biosynthesis capabilities, while other strains with siroheme biosynthesis capability lacked homologs of known siroheme binding proteins, indicating heme auxotrophy and unknown siroheme biochemistry, respectively. While ferritin proteins involved in ferric oxide storage were widespread, those involved in storing Fe as thioferrate were unevenly distributed. Collectively, the results suggest that differences in the mechanisms of Fe and S acquisition, deployment, and storage have accompanied the diversification of methanogens/methanotrophs/alkanotrophs, possibly in response to differential availability of these elements as these organisms evolved.Item Roadmap for naming uncultivated Archaea and Bacteria(2020-08) Murray, Alison E.; Freudenstein, John; Gribaldo, Simonetta; Hatzenpichler, Roland; Hugenholtz, Philip; Kampfer, Peter; Konstantinidis, Konstantinos T.; Lane, Christopher E.; Papke, R. Thane; Parks, Donovan H.; Rossello-Mora, Ramon; Stott, Matthew B.; Sutcliffe, Iain C.; Thrash, J. Cameron; Venter, Stephanus N.; Whitman, William B.; Acinas, Silvia G.; Amann, Rudolf I.; Anantharaman, Karthik; Armengaud, Jean; Baker, Brett J.; Barco, Roman A.; Bode, Helge B.; Boyd, Eric S.; Brady, Carrie L.; Carini, Paul; Chain, Patrick S. G.; Colman, Daniel R.; DeAngelis, Kristen M.; Asuncion de los Rios, Maria; Estrada-de los Santos, Paulina; Dunlap, Christopher A.; Eisen, Jonathan A.; Emerson, David; Ettema, Thisjs J. G.; Eveillard, Damien R.; Girguis, Peter R.; Hentschel, Ute; Hollibaugh, James T.; Hug, Laura A.; Inskeep, William P.; Ivanova, Elena P.; Klenk, Hans-Peter; Li, Wen-Jun; Lloyd, Karen G.; Loffler, Frank E.; Makhalanyane, Thulani P.; Moser, Duane P.; Nunoura, Takuro; Palmer, Marike; Parro, Victor; Pedros-Alio, Carlos; Probst, Alexander J.; Smits, Theo H. M.; Steen, Andrew D.; Steenkamp, Emma T.; Spang, Anja; Stewart, Frank J.; Tiedje, James M.; Vandamme, Peter; Wagner, Michael; Wang, Feng-Ping; Yarza, Pablo; Hedlund, Brian P.; Reysenbach, Anna-LouiseThe assembly of single-amplified genomes (SAGs) and metagenome-assembled genomes (MAGs) has led to a surge in genome-based discoveries of members affiliated with Archaea and Bacteria, bringing with it a need to develop guidelines for nomenclature of uncultivated microorganisms. The International Code of Nomenclature of Prokaryotes (ICNP) only recognizes cultures as ‘type material’, thereby preventing the naming of uncultivated organisms. In this Consensus Statement, we propose two potential paths to solve this nomenclatural conundrum. One option is the adoption of previously proposed modifications to the ICNP to recognize DNA sequences as acceptable type material; the other option creates a nomenclatural code for uncultivated Archaea and Bacteria that could eventually be merged with the ICNP in the future. Regardless of the path taken, we believe that action is needed now within the scientific community to develop consistent rules for nomenclature of uncultivated taxa in order to provide clarity and stability, and to effectively communicate microbial diversity.Item Phylogenomic analysis of novel Diaforarchaea is consistent with sulfite but not sulfate reduction in volcanic environments on early Earth(2020-02) Colman, Daniel R.; Lindsay, Melody R.; Amenabar, Maximiliano J.; Fernandes-Martins, Maria C.; Roden, Eric R.; Boyd, Eric S.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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