Acidithiobacillus ferrooxidans oxidizes ferrous iron before sulfur likely through transcriptional regulation by the global redox responding RegBA signal transducing system

The mechanisms of ferrous iron (Fe(II)) and reduced inorganic sulfur compounds (RISC) oxidation under oxic conditions of the bioleaching bacterium Acidithiobacillus ferrooxidans have been deciphered. The genes involved in these pathways are more transcribed in the presence than in the absence of the corresponding electron donor, i.e. the genes involved in Fe(II) oxidation are expressed preferentially in the presence of Fe(II) than sulfur (S0) and those involved in RISC oxidation are more transcribed in S0- than in Fe(II)-grown cells. In this study, oxidation of Fe(II) and S0 and expression of the main genes involved in these pathways have been followed when both electron donors are present in the medium. The results obtained clearly indicate that (i) S0 oxidation takes place only when iron is totally oxidized and (ii) the genes involved in Fe(II) are expressed before those involved in RISC oxidation, even in the presence of S0. Therefore, a transcriptional regulator is likely inducing the genes involved in Fe(II) oxidation and repressing those involved in RISC oxidation when Fe(II) is present. Data presented in this paper suggest that the redox sensing sensor/regulator two-component signal transducing system RegBA could be responsible for this regulation since (i) the redox potential increases during Fe(II) oxidation but remains stable during S0 oxidation and (ii) the regulator RegA is able to bind to the regulatory region of a number of genes/operons of which the expression is regulated by Fe(II). The understanding of how RegBA controls the energetic pathways depending on the overall redox state of the cell is of primordial importance since it could help in controlling the dynamics of Fe(II) and RISC oxidation during bioleaching processes.