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

Alyssa A Carrell,Dawn M Klingeman,Grace E Schwartz,Regina L Wilpiszeski,Ann M Wymore,Scott C Brooks,Caitlin M Gionfriddo,Katherine A Muller,Melissa A Cregger,Dwayne A Elias

doi:10.3389/fmicb.2021.647861

Abstract

The conversion of mercury (Hg) to monomethylmercury (MMHg) is a critical area of concern in global Hg cycling. Periphyton biofilms may harbor significant amounts of MMHg but little is known about the Hg-methylating potential of the periphyton microbiome. Therefore, we used high-throughput amplicon sequencing of the 16S rRNA gene, ITS2 region, and Hg methylation gene pair (hgcAB) to characterize the archaea/bacteria, fungi, and Hg-methylating microorganisms in periphyton communities grown in a contaminated watershed in East Tennessee (United States). Furthermore, we examined how nutrient amendments (nitrate and/or phosphate) altered periphyton community structure and function. We found that bacterial/archaeal richness in experimental conditions decreased in summer and increased in autumn relative to control treatments, while fungal diversity generally increased in summer and decreased in autumn relative to control treatments. Interestingly, the Hg-methylating communities were dominated by Proteobacteria followed by Candidatus Atribacteria across both seasons. Surprisingly, Hg methylation potential correlated with numerous bacterial families that do not contain hgcAB, suggesting that the overall microbiome structure of periphyton communities influences rates of Hg transformation within these microbial mats. To further explore these complex community interactions, we performed a microbial network analysis and found that the nitrate-amended treatment resulted in the highest number of hub taxa that also corresponded with enhanced Hg methylation potential. This work provides insight into community interactions within the periphyton microbiome that may contribute to Hg cycling and will inform future research that will focus on establishing mixed microbial consortia to uncover mechanisms driving shifts in Hg cycling within periphyton habitats.

Highlights

The conversion of mercury (Hg) to monomethylmercury (MMHg) is a critical area of concern in global Hg cycling
Periphyton biofilms have received recent attention for their role in Hg cycling, but little is known about the structure or community interactions of this complex microbiome
We assessed the impact of nutrient amendments on the periphyton microbiome across two seasons

Summary

Introduction

The conversion of mercury (Hg) to monomethylmercury (MMHg) is a critical area of concern in global Hg cycling. Once MMHg is produced, it is bioaccumulated in organisms and biomagnifies through food webs, impacting humans through the consumption of fish with elevated levels of MMHg. 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). 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. 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). Overall MMHg production may be influenced by the interactions of the entire microbiome in the biofilm (Francoeur and Biggs, 2006; Lázaro et al, 2013, 2018)

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