Recent advances have allowed for greater investigation into microbial regulation of mercury toxicity in the environment. In wetlands in particular, dissolved organic matter (DOM) may influence methylmercury (MeHg) production both through chemical interactions and through substrate effects on microbiomes. We conducted microcosm experiments in two disparate wetland environments (unvegetated and vegetated sediments) to examine the impacts of plant leachate and inorganic mercury loadings on microbiomes, DOM cycling, and MeHg production. We show that while leachate influenced the microbiome in both environment types, sediment with high organic carbon content was more resistant to change than oligotrophic sediment. Oligotrophic unvegetated sediments receiving leachate produced more MeHg than unamended microcosms, coincident with an increase in putative chemoorganotrophic methylators belonging to Clostridia. Further, metagenomic shifts toward fermentation, and secondarily iron metabolisms, in these microcosms as well as degradation of complex DOM also support a possible association between rarely acknowledged microorganisms and MeHg. Our research provides a basis for future investigation into the role of fermenting organisms in mercury toxicity and generates a new hypothesis that DOM can stimulate mercury methylation either 1) via direct methylation by fermenting bacteria or 2) via enhancing carbon bioavailability for sulfate- and iron-reducing bacteria through breakdown of complex DOM.