Publications by Colleges and Departments (MSU - Bozeman)
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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 Impact of mineral and non-mineral sources of iron and sulfur on the metalloproteome of Methanosarcina barkeri(American Society for Microbiology, 2024-07) Larson, James; Tokmina-Lukaszewska, Monika; Payne, Devon; Spietz, Rachel L.; Fausset, Hunter; Alam, Md Gahangir; Brekke, Brooklyn K.; Pauley, Jordan; Hasenoehrl, Ethan J.; Shepard, Eric M.; Boyd, Eric S.; Bothner, BrianMethanogens often inhabit sulfidic environments that favor the precipitation of transition metals such as iron (Fe) as metal sulfides, including mackinawite (FeS) and pyrite (FeS2). These metal sulfides have historically been considered biologically unavailable. Nonetheless, methanogens are commonly cultivated with sulfide (HS-) as a sulfur source, a condition that would be expected to favor metal precipitation and thus limit metal availability. Recent studies have shown that methanogens can access Fe and sulfur (S) from FeS and FeS2 to sustain growth. As such, medium supplied with FeS2 should lead to higher availability of transition metals when compared to medium supplied with HS-. Here, we examined how transition metal availability under sulfidic (i.e., cells provided with HS- as sole S source) versus non-sulfidic (cells provided with FeS2 as sole S source) conditions impact the metalloproteome of Methanosarcina barkeri Fusaro. To achieve this, we employed size exclusion chromatography coupled with inductively coupled plasma mass spectrometry and shotgun proteomics. Significant changes were observed in the composition and abundance of iron, cobalt, nickel, zinc, and molybdenum proteins. Among the differences were alterations in the stoichiometry and abundance of multisubunit protein complexes involved in methanogenesis and electron transport chains. Our data suggest that M. barkeri utilizes the minimal iron-sulfur cluster complex and canonical cysteine biosynthesis proteins when grown on FeS2 but uses the canonical Suf pathway in conjunction with the tRNA-Sep cysteine pathway for iron-sulfur cluster and cysteine biosynthesis under sulfidic growth conditions.Item A concept for international societally relevant microbiology education and microbiology knowledge promulgation in society(Wiley, 2024-05) Timmis, Kenneth et al.; Boyd, Eric S.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 Investigating Abiotic and Biotic Mechanisms of Pyrite Reduction(Frontiers Media SA, 2022-05) Lange Spietz, Rachel K.; Payne, Devon; Kulkarni, Gargi; Metcalf, William W.; Roden, Eric E.; Boyd, Eric S.Pyrite (FeS2) has a very low solubility and therefore has historically been considered a sink for iron (Fe) and sulfur (S) and unavailable to biology in the absence of oxygen and oxidative weathering. Anaerobic methanogens were recently shown to reduce FeS2 and assimilate Fe and S reduction products to meet nutrient demands. However, the mechanism of FeS2 mineral reduction and the forms of Fe and S assimilated by methanogens remained unclear. Thermodynamic calculations described herein indicate that H2 at aqueous concentrations as low as 10–10 M favors the reduction of FeS2, with sulfide (HS–) and pyrrhotite (Fe1–xS) as products; abiotic laboratory experiments confirmed the reduction of FeS2 with dissolved H2 concentrations greater than 1.98 × 10–4 M H2. Growth studies of Methanosarcina barkeri provided with FeS2 as the sole source of Fe and S resulted in H2 production but at concentrations too low to drive abiotic FeS2 reduction, based on abiotic laboratory experimental data. A strain of M. barkeri with deletions in all [NiFe]-hydrogenases maintained the ability to reduce FeS2 during growth, providing further evidence that extracellular electron transport (EET) to FeS2 does not involve H2 or [NiFe]-hydrogenases. Physical contact between cells and FeS2 was required for mineral reduction but was not required to obtain Fe and S from dissolution products. The addition of a synthetic electron shuttle, anthraquinone-2,6-disulfonate, allowed for biological reduction of FeS2 when physical contact between cells and FeS2 was prohibited, indicating that exogenous electron shuttles can mediate FeS2 reduction. Transcriptomics experiments revealed upregulation of several cytoplasmic oxidoreductases during growth of M. barkeri on FeS2, which may indicate involvement in provisioning low potential electrons for EET to FeS2. Collectively, the data presented herein indicate that reduction of insoluble FeS2 by M. barkeri occurred via electron transfer from the cell surface to the mineral surface resulting in the generation of soluble HS– and mineral-associated Fe1–xS. Solubilized Fe(II), but not HS–, from mineral-associated Fe1–xS reacts with aqueous HS– yielding aqueous iron sulfur clusters (FeSaq) that likely serve as the Fe and S source for methanogen growth and activity. FeSaq nucleation and subsequent precipitation on the surface of cells may result in accelerated EET to FeS2, resulting in positive feedback between cell activity and FeS2 reduction.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 Molecular Evidence for an Active Microbial Methane Cycle in Subsurface Serpentinite-Hosted Groundwaters in the Samail Ophiolite, Oman(American Society for Microbiology, 2021-01) Kraus, Emily A.; Nothaft, Daniel; Stamps, Blake W.; Rempfert, Kaitlin R.; Ellison, Eric T.; Matter, Juerg M.; Templeton, Alexis S.; Boyd, Eric S.; Spear, John R.Serpentinization can generate highly reduced fluids replete with hydrogen (H2) and methane (CH4), potent reductants capable of driving microbial methanogenesis and methanotrophy, respectively. However, CH4 in serpentinized waters is thought to be primarily abiogenic, raising key questions about the relative importance of methanogens and methanotrophs in the production and consumption of CH4 in these systems. Herein, we apply molecular approaches to examine the functional capability and activity of microbial CH4 cycling in serpentinization-impacted subsurface waters intersecting multiple rock and water types within the Samail Ophiolite of Oman. Abundant 16S rRNA genes and transcripts affiliated with the methanogenic genus Methanobacterium were recovered from the most alkaline (pH, >10), H2- and CH4-rich subsurface waters. Additionally, 16S rRNA genes and transcripts associated with the aerobic methanotrophic genus Methylococcus were detected in wells that spanned varied fluid geochemistry. Metagenomic sequencing yielded genes encoding homologs of proteins involved in the hydrogenotrophic pathway of microbial CH4 production and in microbial CH4 oxidation. Transcripts of several key genes encoding methanogenesis/methanotrophy enzymes were identified, predominantly in communities from the most hyperalkaline waters. These results indicate active methanogenic and methanotrophic populations in waters with hyperalkaline pH in the Samail Ophiolite, thereby supporting a role for biological CH4 cycling in aquifers that undergo low-temperature serpentinization.