Abstract
Elemental sulfur [S(0)] is a central and ecologically important intermediate in the sulfur cycle, which can be used by a wide diversity of microorganisms that gain energy from its oxidation, reduction, or disproportionation. S(0) is formed by oxidation of reduced sulfur species, which can be chemically or microbially mediated. A variety of sulfur-oxidizing bacteria can biomineralize S(0), either intracellularly or extracellularly. The details and mechanisms of extracellular S(0) formation by bacteria have been in particular understudied so far. An important question in this respect is how extracellular S(0) minerals can be formed and remain stable in the environment outside of their thermodynamic stability domain. It was recently discovered that S(0) minerals could be formed and stabilized by oxidizing sulfide in the presence of dissolved organic compounds, a process called S(0) organomineralization. S(0) particles formed through this mechanism possess specific signatures such as morphologies that differ from that of their inorganically precipitated counterparts, encapsulation within an organic envelope, and metastable crystal structures (presence of the monoclinic β- and γ-S8 allotropes). Here, we investigated S(0) formation by the chemolithoautotrophic sulfur-oxidizing and nitrate-reducing bacterium Sulfuricurvum kujiense (Epsilonproteobacteria). We performed a thorough characterization of the S(0) minerals produced extracellularly in cultures of this microorganism, and showed that they present all the specific signatures (morphology, association with organics, and crystal structures) of organomineralized S(0). Using “spent medium” experiments, we furthermore demonstrated that soluble extracellular compounds produced by S. kujiense are necessary to form and stabilize S(0) minerals outside of the cells. This study provides the first experimental evidence of the importance of organomineralization in microbial S(0) formation. The prevalence of organomineralization in extracellular S(0) precipitation by other sulfur bacteria remains to be investigated, and the biological role of this mechanism is still unclear. However, we propose that sulfur-oxidizing bacteria could use soluble organics to stabilize stores of bioavailable S(0) outside the cells.
Highlights
Elemental sulfur [S(0)] is an intermediate in the biogeochemical sulfur cycle, which can be found in many different types of environments such as marine sediments (Jørgensen and Nelson, 2004; Zopfi et al, 2004) and water columns (Findlay et al, 2014), euxinic lakes (Zerkle et al, 2010), sulfidic caves (Hamilton et al, 2015), hydrothermal vents (Taylor et al, 1999), as well as cold (Gleeson et al, 2011) or hot springs (Kamyshny et al, 2014)
Oxidation of reduced sulfur species by S. kujiense lead to the precipitation of S(0) particles after a few days when both thiosulfate and sulfide were provided (Figure 1; Supplementary Figure S1)
No S(0) was not formed in the S. kujiense culture supplemented with thiosulfate only after 5 weeks, and only Ca,Mg-phosphate particles were found (Supplementary Figure S2)
Summary
Elemental sulfur [S(0)] is an intermediate in the biogeochemical sulfur cycle, which can be found in many different types of environments such as marine sediments (Jørgensen and Nelson, 2004; Zopfi et al, 2004) and water columns (Findlay et al, 2014), euxinic lakes (Zerkle et al, 2010), sulfidic caves (Hamilton et al, 2015), hydrothermal vents (Taylor et al, 1999), as well as cold (Gleeson et al, 2011) or hot springs (Kamyshny et al, 2014). In low-temperature environments, S(0) is formed by the oxidation of more reduced sulfur species such as sulfide. This oxidation can occur chemically in the presence of oxygen or oxidized metals [e.g., Fe(III); Rickard and Luther, 2007], or it can be biologically mediated by diverse chemotrophic and phototrophic sulfur-oxidizing bacteria (SOB) and archaea (Dahl and Friedrich, 2008). The chemical oxidation of sulfide to S(0) by molecular oxygen occurs at rates that are several orders of magnitude lower than measured rates of microbial sulfide oxidation (Luther et al, 2011), and so it is usually assumed that in low-temperature environments, S(0) formation mostly results from microbial oxidation. Many different bacteria and archaea are able to biomineralize S(0) in the form of intra- or extra-cellular S(0) globules (Kleinjan et al, 2003; Dahl and Prange, 2006) or extracellular S(0) filaments (Wirsen et al, 2002; Sievert et al, 2007)
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