Cellular uptake of inorganic divalent mercury (Hg(II)) is a key step in microbial formation of neurotoxic methylmercury (MeHg), but the mechanisms remain largely unidentified. We show that the iron reducing bacterium produces and exports appreciable amounts of low molecular mass thiol (LMM-RSH) compounds reaching concentrations of about 100 nM in the assay medium. These compounds largely control the chemical speciation and bioavailability of Hg(II) by the formation of Hg(LMM-RS) complexes (primarily with cysteine) in assays without added thiols. By characterizing these effects, we show that the thermodynamic stability of Hg(II)-complexes is a principal controlling factor for Hg(II) methylation by this bacterium such that less stable complexes with mixed ligation involving LMM-RSH, OH, and Cl are methylated at higher rates than the more stable Hg(LMM-RS) complexes. The Hg(II) methylation rate across different Hg(LMM-RS) compounds is also influenced by the chemical structure of the complexes. In contrast to the current perception of microbial uptake of Hg, our results adhere to generalized theories for metal biouptake based on metal complexation with cell surface ligands and refine the mechanistic understanding of Hg(II) availability for microbial methylation.