skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 10:00 PM ET on Friday, February 6 until 10:00 AM ET on Saturday, February 7 due to maintenance. We apologize for the inconvenience.


Title: Acquisition of elemental sulfur by sulfur‐oxidising Sulfolobales
Elemental sulfur (S80‐oxidising Sulfolobales (Archaea) dominate high‐temperature acidic hot springs (>80°C, pH <4). However, genomic analyses of S8 oxidising members of the Sulfolobales reveal a patchy distribution of genes encoding sulfur oxygenase reductase (SOR), an S8 disproportionating enzyme attributed to S80oxidation. Here, we report the S8‐dependent growth of two Sulfolobales strains previously isolated from acidic hot springs in Yellowstone National Park, one of which associated with bulk S8 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 S8 oxidation in the SOR‐encoding strain. This is attributed to the generation of hydrogen sulfide (H2S) from S8 disproportionation that can diffuse out of the cell to solubilise bulk S8 to form soluble polysulfides (Sx2-) and/or S8 nanoparticles that readily diffuse across dialysis membranes. The Sulfolobales strain lacking SOR required direct contact to oxidise S8, which could be overcome by the addition of H2S. High concentrations of S8 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.  more » « less
Award ID(s):
1820658
PAR ID:
10549610
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Environmental Microbiology
Date Published:
Journal Name:
Environmental Microbiology
Volume:
26
Issue:
9
ISSN:
1462-2912
Page Range / eLocation ID:
e16691
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Fukami, Tadashi (Ed.)
    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. 
    more » « less
  2. Abstract Despite over a century of study, it is unknown if continental hydrothermal fields support high-temperature subsurface biospheres. Cinder Pool is among the deepest hot springs in Yellowstone and is widely studied due to unique sulfur geochemistry that is attributed to hydrolysis of molten elemental sulfur at ∼18 m depth that promotes several chemical reactions that maintain low sulfide, low oxygen, and a moderate pH of ∼4.0. Following ∼100 years of stability, Cinder Pool underwent extreme visual and chemical change (acidification) in 2018. Here, we show that depth-resolved geochemical and metagenomic-based microbial community analyses pre- (2016) and post-acidification (2020) indicate the changes are likely attributable to feedbacks between geological/geochemical processes, sulfur oxidation by subsurface Sulfolobales Archaea, and the disappearance of molten sulfur at depth. These findings underscore the dynamic and rapid feedback between the geosphere and biosphere in continental hydrothermal fields and suggest subsurface biospheres to be more prevalent in these systems than previously recognized. 
    more » « less
  3. Spear, John R (Ed.)
    ABSTRACT Microorganisms are important catalysts for the oxidation of reduced inorganic sulfur compounds. One environmentally important source of reduced sulfur is metal sulfide minerals that occur in economic mineral deposits and mine waste. Previous research found thatSulfuriferulaspp. were abundant and active in long-term weathering experiments with simulated waste rock and tailings from the Duluth Complex, Northern Minnesota. We, therefore, isolated several strains ofSulfuriferulaspp. from these long-term experiments and characterized their metabolic and genomic properties to provide insight into microbe-mineral interactions and the microbial biogeochemistry in these and other moderately acidic to circumneutral environments. TheSulfuriferulastrains are all obligate chemolithoautotrophs capable of oxidizing inorganic sulfur compounds and ferrous iron. The strains grew over different pH ranges, but all grew between pH 4.5 and 7, matching the weathering conditions of the Duluth Complex rocks. All strains grew on the iron-sulfide mineral pyrrhotite (Fe1 −xS, 0 <x< 0.125) as the sole energy source, as well as hydrogen sulfide and thiosulfate, which are products of sulfide mineral breakdown. Despite their metabolic similarities, each strain encodes a distinct pathway for the oxidation of reduced inorganic sulfur compounds as well as differences in nitrogen metabolism that reveal diverse genomic capabilities among the group. Our results show thatSulfuriferulaspp. are primary producers that likely play a role in sulfide mineral breakdown in moderately acidic to circumneutral mine waste, and the metabolic diversity within the genus may explain their success in sulfide mineral-rich and other sulfidic environments. IMPORTANCEMetal sulfide minerals, such as pyrite and pyrrhotite, are one of the main sources of reduced sulfur in the global sulfur cycle. The chemolithotrophic microorganisms that break down these minerals in natural and engineered settings are catalysts for biogeochemical sulfur cycling and have important applications in biotechnological processes such as biomining and bioremediation.Sulfuriferulais a recently described genus of sulfur-oxidizing bacteria that are abundant primary producers in diverse terrestrial environments, including waste rock and tailings from metal mining operations. In this study, we explored the genomic and metabolic properties of new isolates from this genus, and the implications for their ecophysiology and biotechnological potential in ore and waste from economic mineral deposits. 
    more » « less
  4. 1,4-naphthoquinones (NQs) catalytically oxidize H2S to per- and polysufides and sulfoxides, reduce oxygen to superoxide and hydrogen peroxide, and can form NQ-SH adducts through Michael addition. Here, we measured oxygen consumption and used sulfur-specific fluorophores, liquid chromatography tandem mass spectrometry (LC-MS/MS), and UV-Vis spectrometry to examine H2S oxidation by NQs with various substituent groups. In general, the order of H2S oxidization was DCNQ ~ juglone > 1,4-NQ > plumbagin >DMNQ ~ 2-MNQ > menadione, although this order varied somewhat depending on the experimental conditions. DMNQ does not form adducts with GSH or cysteine (Cys), yet it readily oxidizes H2S to polysulfides and sulfoxides. This suggests that H2S oxidation occurs at the carbonyl moiety and not at the quinoid 2 or 3 carbons, although the latter cannot be ruled out. We found little evidence from oxygen consumption studies or LC-MS/MS that NQs directly oxidize H2S2–4, and we propose that apparent reactions of NQs with inorganic polysulfides are due to H2S impurities in the polysulfides or an equilibrium between H2S and H2Sn. Collectively, NQ oxidation of H2S forms a variety of products that include hydropersulfides, hydropolysulfides, sulfenylpolysulfides, sulfite, and thiosulfate, and some of these reactions may proceed until an insoluble S8 colloid is formed. 
    more » « less
  5. null (Ed.)
    ABSTRACT Thermoacidophilic archaea belonging to the order Sulfolobales thrive in extreme biotopes, such as sulfuric hot springs and ore deposits. These microorganisms have been model systems for understanding life in extreme environments, as well as for probing the evolution of both molecular genetic processes and central metabolic pathways. Thermoacidophiles, such as the Sulfolobales, use typical microbial responses to persist in hot acid (e.g. motility, stress response, biofilm formation), albeit with some unusual twists. They also exhibit unique physiological features, including iron and sulfur chemolithoautotrophy, that differentiate them from much of the microbial world. Although first discovered >50 years ago, it was not until recently that genome sequence data and facile genetic tools have been developed for species in the Sulfolobales. These advances have not only opened up ways to further probe novel features of these microbes but also paved the way for their potential biotechnological applications. Discussed here are the nuances of the thermoacidophilic lifestyle of the Sulfolobales, including their evolutionary placement, cell biology, survival strategies, genetic tools, metabolic processes and physiological attributes together with how these characteristics make thermoacidophiles ideal platforms for specialized industrial processes. 
    more » « less