Abstract
Production of sulfur globules during sulfide or thiosulfate oxidation is a characteristic feature of some sulfur bacteria. Although their generation has been reported in Acidithiobacillus ferrooxidans, its mechanism of formation and deposition, as well as the physiological significance of these globules during sulfur compounds oxidation, are currently unknown. Under oxygen-sufficient conditions (OSC), A. ferrooxidans oxidizes thiosulfate to tetrathionate, which accumulates in the culture medium. Tetrathionate is then oxidized by a tetrathionate hydrolase (TTH) generating thiosulfate, elemental sulfur, and sulfate as final products. We report here a massive production of extracellular conspicuous sulfur globules in thiosulfate-grown A. ferrooxidans cultures shifted to oxygen-limiting conditions (OLC). Concomitantly with sulfur globule deposition, the extracellular concentration of tetrathionate greatly diminished and sulfite accumulated in the culture supernatant. A. ferrooxidans cellular TTH activity was negligible in OLC-incubated cells, indicating that this enzymatic activity was not responsible for tetrathionate disappearance. On the other hand, supernatants from both OSC- and OLC-incubated cells showed extracellular TTH activity, which most likely accounted for tetrathionate consumption in the culture medium. The extracellular TTH activity described here: (i) gives experimental support to the TTH-driven model for hydrophilic sulfur globule generation, (ii) explains the extracellular location of A. ferrooxidans sulfur deposits, and (iii) strongly suggests that the generation of sulfur globules in A. ferrooxidans corresponds to an early step during its adaptation to an anaerobic lifestyle.
Highlights
IntroductionDuring oxidation of reduced inorganic sulfur compounds (RISCs), by some microaerophilic chemotrophic sulfur bacteria and by anoxygenic phototrophic microorganisms, the deposition of intracellular or extracellular conspicuous sulfur globules as an important (and sometimes obligatory) intermediary occurs
During oxidation of reduced inorganic sulfur compounds (RISCs), by some microaerophilic chemotrophic sulfur bacteria and by anoxygenic phototrophic microorganisms, the deposition of intracellular or extracellular conspicuous sulfur globules as an important intermediary occurs
Growth of A. ferrooxidans in thiosulfate as energy source As it has been previously shown (Hazeu et al, 1986) during thiosulfate oxidation by A. ferrooxidans, tetrathionate was accumulated in the culture medium, and in our experimental conditions it reached a maximum concentration of c.a. 5 mM (Figure 2A)
Summary
During oxidation of reduced inorganic sulfur compounds (RISCs), by some microaerophilic chemotrophic sulfur bacteria and by anoxygenic phototrophic microorganisms, the deposition of intracellular or extracellular conspicuous sulfur globules as an important (and sometimes obligatory) intermediary occurs. It has been proposed that production of obligated intracellular sulfur deposits, during anoxygenic sulfide and thiosulfate oxidation in photolithotrophic and facultative anaerobic chemolithotrophic bacteria, correlates with the lack of sulfur dehydrogenase (SoxCD), normally present in the thiosulfate-oxidizing multi-enzyme system (TOMES; Friedrich et al, 2005). The latter is a characteristic feature of microorganisms that oxidize RISCs by using the branched Paracoccus sulfur oxidation (PSO) pathway (Grimm et al, 2008; Ghosh and Dam, 2009, and references therein). The production of long-chain polythionates and elemental sulfur has been reported www.frontiersin.org
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