Advances in genetics have allowed for greater investigation into the complex microbial communities mediating mercury methylation in the environment. In wetlands in particular, dissolved organic matter (DOM) may influence methylmercury production both through direct chemical interactions with mercury and through substrate effects on the environmental microbiome. We conducted microcosm experiments in two chemically disparate wetland environments (unvegetated and vegetated sediments) to examine the impact of DOM from leachate of local vegetation and inorganic mercury loadings on microbial community membership, metagenomic potential, DOM processing, and methylmercury (MeHg) production. We show that while DOM loadings impacted the microbiome in both environment types, sediment with high organic carbon content was more resistant than oligotrophic sediment to changes in microbiomes. Oligotrophic sediments receiving DOM produced significantly more MeHg than unamended microcosms, coincident with an increase in putative chemoorganotrophic methylators within the class Clostridia. Further, metagenomic shifts toward fermentation, and secondarily iron metabolisms, in these microcosms as well as degradation of complex DOM indicated by fluorescence indices also support a possible association between rarely acknowledged microbial metabolisms and MeHg production. 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 in oligotrophic environments either 1) via direct methylation by fermenting bacteria or 2) via enhancing the bioavailability of simple carbon compounds for sulfate- and iron-reducing bacteria through breakdown of complex DOM.