Comparative proteomics reveals hydrogenase-centered steel-dependent growth and corrosion in Desulfovibrio vulgaris and Desulfovibrio ferrophilus

Abstract

Comparative proteomic analyses including ecologically distinct sulfate-reducing strains and different cellular fractions are scarce, limiting our understanding of corrosion-related mechanisms under anoxic conditions and the identification of protein signatures relevant to microbiologically influenced corrosion (MIC). To capture both freshwater and marine adaptations, we investigated the well-established SRB model strains Desulfovibrio vulgaris and Desulfovibrio ferrophilus. We compared energy metabolism, electron transport pathways, and growth patterns in both strains cultivated with lactate, H2, or steel as electron donor. Time-dependent biophysicochemical measurements, SEM/EDX, and shotgun proteomics were performed. We explored cellular proteins in planktonic and biofilm fractions, as well as potential extracellular enzymes in the supernatant. In both the strains, growth with steel revealed energy metabolisms more similar to H2-dependent metabolism instead of direct iron-to-microbe electron transfer (DIMET). Increased abundances of periplasmic hydrogenases and c-type cytochromes served as proteomic signatures supporting H2-mediated iron-to-microbe electron transfer (HIMET). Concomitant to bacterial growth and biofilm formation, mineral deposits of carbonates, phosphates and FeS were formed, the latter especially in saltwater treatments. The close association of D. ferrophilus cells with FeS particles supports the possibility of the role of FeS in electron transfer in addition to H2 as well as formate mediated electron transfer which may have contributed to the high corrosion levels with D. ferrophilus. Neither strain exhibited increased abundances of redox proteins known to be involved in extracellular electron transfer, supporting that DIMET may have not been a dominant mechanism under the given conditions. This interpretation is also in line with the observation that only a small proportion of the total cells were associated with the steel surface, and that direct cell-to-steel contact was not observed. These findings show that SRB can be metabolically flexible and that hydrogenase-based systems are sufficient for steel-dependent growth leading to corrosion. This is especially relevant in natural environments, where more than one type of electron donor is available and different modes of extracellular electron transfer exist.