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 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 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 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.