Abstract 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 S80disproportionating enzyme attributed to S80oxidation. 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 S80during 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 S80oxidation in the SOR‐encoding strain. This is attributed to the generation of hydrogen sulfide (H2S) from S80disproportionation that can diffuse out of the cell to solubilise bulk S80to form soluble polysulfides (Sx2−) and/or S80nanoparticles 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 S80inhibited 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. 
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                            Sulfide oxidation by members of the Sulfolobales
                        
                    
    
            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. 
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                            - Award ID(s):
- 1820658
- PAR ID:
- 10549608
- Editor(s):
- Fukami, Tadashi
- Publisher / Repository:
- PNAS Nexus
- Date Published:
- Journal Name:
- PNAS Nexus
- Volume:
- 3
- Issue:
- 6
- ISSN:
- 2752-6542
- Page Range / eLocation ID:
- pgae201
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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