Elemental Sulfur Formation by Sulfuricurvum kujiense Is Mediated by Extracellular Organic Compounds

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.

Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas

“…Furthermore, the structures of extracellular S 0 produced by NW10 T were mainly in the form of crystalline bars with clear edges composed of α-S 8 , which was significantly different from the sulfur globules usually resulting from most chemotrophic and phototrophic bacteria activity (Dahl and Prange, 2006;Jiang et al, 2017;Cron et al, 2019). α-S 8 is the thermodynamically most stable form of elemental sulfur at ambient temperature and pressure, and has been found in very diverse environments, such as marine sediments, water columns, euxinic lakes, sulfidic caves, hydrothermal vents, as well as cold or hot springs (Roy and Trudinger, 1970;Taylor et al, 1999;Steudel, 2000;Gleeson et al, 2012;Findlay et al, 2014;Hamilton et al, 2015).…”

“…So far, a large number of studies focused on the analysis of chemical form and structure of microbial extra-and intracellular S 0 (Pickering et al, 2001;George et al, 2008;Berg et al, 2014). To our knowledge, the enzymes catalyzing the oxidation of sulfide or thiosulfate to S 0 are usually located in the bacterial periplasm, but sulfur globules are observed outside of the cells, and sometimes even keeping the cells at a distance (Gregersen et al, 2011;Marnocha et al, 2016;Cron et al, 2019). Therefore, it has been proposed that reduced sulfur compounds could be initially oxidized to soluble polysulfide intermediates in the periplasm, and then be transported outside the cells to form sulfur globules.…”

“…Therefore, it has been proposed that reduced sulfur compounds could be initially oxidized to soluble polysulfide intermediates in the periplasm, and then be transported outside the cells to form sulfur globules. It is still not clear how extracellular S 0 can accumulate outside of the cells (Cron et al, 2019). Recently, increasing number of studies indicate that SOB could excrete soluble organics to help form and stabilize S 0 in the environment (Cosmidis et al, 2019;Cron et al, 2019;Marnocha et al, 2019).…”

“…It is still not clear how extracellular S 0 can accumulate outside of the cells (Cron et al, 2019). Recently, increasing number of studies indicate that SOB could excrete soluble organics to help form and stabilize S 0 in the environment (Cosmidis et al, 2019;Cron et al, 2019;Marnocha et al, 2019). This could explain many of the puzzling fact observed in microbial extracellular S 0 , such as coated by organics on the surface, and growing extracellularly at a distance from the cells (Hanson et al, 2016;Marnocha et al, 2016Marnocha et al, , 2019.…”

Benefits at the nanoscale: a review of nanoparticle‐enabled processes favouring microbial growth and functionality

“…This may form larger minerals that are more easily 'shed' from the cell walls compared to nanoparticles. However, the recent finding that soluble organics harvested from E. coli are just as potent at inducing extracellular S 0 formation compared to organics from the S‐oxidizing bacteria Sulfuricurvum kujiense (Cron et al ., 2019) indicates a non‐specific role of organic molecules in directing mineralization. The delicate balance between nanoparticle (trans)formation and microbial responses needs to be understood in order to better determine the extent of regulation that microbes have in directing extracellular biomineralization.…”