Periphyton and Flocculent Materials Are Important Ecological Compartments Supporting Abundant and Diverse Mercury Methylator Assemblages in the Florida Everglades

Abstract

Mercury (Hg) methylation in the Florida Everglades is of great environmental concern because of its adverse effects on human and wildlife health through biomagnification in aquatic food webs. Periphyton and flocculant materials (floc) overlaying peat soil are important ecological compartments producing methylmercury (MeHg) in this ecosystem. These compartments retain higher concentrations of MeHg than did soil at study sites across nutrient and/or sulfate gradient(s). To better understand what controls Hg methylation in these compartments, the present study explored the structures and abundances of Hg methylators using genes hgcAB as biomarkers. The hgcA sequences indicated that these compartments hosted a high diversity of Hg methylators, including Deltaproteobacteria, Chloroflexi, Firmicutes, and Methanomicrobia, with community compositions that differed between these habitats. The copy numbers of hgcAB quantified by quantitative PCR revealed that floc and soil supported higher numbers of Hg methylators than periphyton in the Everglades ecosystem. The abundance of Hg methylators was strongly positively correlated with concentrations of carbon and nutrients (e.g., phosphorus and nitrogen) according to redundancy analysis. Strong correlations were also observed among numbers of sulfate reducers, methanogens, and the dominant hgcAB-carrying groups, suggesting that hgcAB would spread primarily through the growth of those assemblages. The abundances of Hg methylators were weakly negatively correlated to MeHg concentrations, suggesting that the size of this population would not solely determine the final concentrations of MeHg in the ecological compartments studied. This study extends the knowledge regarding the distribution of diverse potential mercury methylators in different environmental compartments in a wetland of national concern. IMPORTANCE Methylmercury is a potent neurotoxin that impacts the health of humans and wildlife. Most mercury in wetlands such as the Florida Everglades enters as inorganic mercury via atmospheric deposition, some of which is transformed to the more toxic methylmercury through the activities of anaerobic microorganisms. We investigated the numbers and phylogenetic diversity of hgcAB, genes that are linked to mercury methylation, in the soil, floc, and periphyton in areas of the Everglades with different sulfate and nutrient concentrations. Soil harbored relatively high numbers of cells capable of methylating mercury; however, little detectable methylmercury was present in soil. The greatest concentrations of methylmercury were found in floc and periphyton. The dominant methylators in those compartments included methanogens and Syntrophobacteriales. This work provides significant insight into the microbial processes that control methylation and form the basis for accumulation through the food chain in this important environment.

Mercury cycling in freshwater systems - An updated conceptual model

“…A wide occurrence of HgII methylating Deltaproteobacteria and Firmicutes was observed in periphyton collected in the Everglades (Bae et al, 2019). Because of the high abundance of macrophytes in shallow freshwater environments in tropical, subtropical and northern climates wetlands, macrophyte-associated periphyton were identified as contributors of MeHg production in these ecosystems (Hall et al, 2008) although their relative role in the lake Hg cycle remains largely unquantified.…”

Substratum‐associated microbiota

“…Consumption of contaminated fish esposes humans to this neurotoxin. Bae, Dierberg, and Ogram (2019) studied the distribution of mercury methylators in the Florida Everglades, United States. Jones et al (2019) used biochemical and molecular techniques to study the distribution of potential mercury methylators in two sulfate-impacted lakes on Minnesota's Mesabi Iron Range (USA).…”

Nutrient Exposure Alters Microbial Composition, Structure, and Mercury Methylating Activity in Periphyton in a Contaminated Watershed

“…The transformation of inorganic Hg into MMHg is mediated by anaerobic microorganisms ( Parks et al, 2013 ; Bravo and Cosio, 2020 ), predominantly from the Deltaproteobacteria, Methanomicrobia, and Firmicutes ( Christensen et al, 2016 , 2018 ). While significant work has examined Hg transformations in aquatic sediments ( Bae et al, 2019 ; Branfireun et al, 2020 ; Xiang et al, 2020 ), less research has focused on aquatic microbial biofilms like periphyton. Recent work demonstrates that these biofilms may harbor significant amounts of MMHg ( McDowell et al, 2020 ), but little is known about the community of microorganisms mediating Hg transformations.…”

“…Mercury methylation in periphyton has been shown in many different ecosystems and has been attributed to sulfate-reducing bacteria (SRB) and methanogenic archaea that occupy anoxic niches within the periphyton biofilm structure ( Cleckner et al, 1999 ; Achá et al, 2011 ; Hamelin et al, 2011 ). To our knowledge, there is only one study that has identified Hg-methylating microorganisms in periphyton using the Hg methylation gene cluster, hgcAB , as a biomarker ( Bae et al, 2019 ). Bae et al (2019) found that periphyton and flocculant material from the Florida Everglades contained a diverse assemblage of hgcAB -containing microorganisms, including Deltaproteobacteria, Chloroflexi, Firmicutes, and Methanomicrobia.…”

“…To our knowledge, there is only one study that has identified Hg-methylating microorganisms in periphyton using the Hg methylation gene cluster, hgcAB , as a biomarker ( Bae et al, 2019 ). Bae et al (2019) found that periphyton and flocculant material from the Florida Everglades contained a diverse assemblage of hgcAB -containing microorganisms, including Deltaproteobacteria, Chloroflexi, Firmicutes, and Methanomicrobia. In addition to harboring Hg-methylating microorganisms, periphyton consortia can produce photosynthetic by-products and organic molecules that, in some instances, increase Hg bioavailability and MMHg production ( Mangal et al, 2019a , b ; Branfireun et al, 2020 ).…”