Microbial communities associated with mercury methylation in paddy soils

Yu-Rong Liua,b*, A. Johsc, L. Bib, X. Luc, J.Z. Heb and B.H. Guc

a College of Resources and Environment, Huazhong Agricultural University, China

b Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, China

c Environmental Sciences Division, Oak Ridge National Laboratory, United States

yrliu@mail.hzau.edu.cn

Mercury (Hg) is a growing environmental concern because it can be converted to neurotoxic methylmercury (MeHg) that can bioaccumulate and biomagnify up the food chain. The consumption of foods contaminated with MeHg threatens human health globally. Seafood, especially large predatory fish, is widely considered as the primary route for human exposure to MeHg, but recent studies show that rice may constitute another important exposure route, particularly in countries where rice is a staple of the everyday diet. Although certain anaerobic microorganisms are known to convert inorganic mercury (Hg) to MeHg and the discovery of a two-gene cluster hgcAB has linked Hg methylation to several phylogenetically diverse groups of microorganisms, the prevalence and diversity of Hg methylators in microbial communities of rice paddy soils remain unclear. Here, we report the abundance and distribution of hgcAB genes using a combination of 3rd-generation PacBio sequencing, metagenomic and quantitative PCR analyses in several mine-impacted paddy soils from southwest China. We show that Hg methylating communities are diverse, with iron-reducing bacteria (i.e., Geobacter) and methanogens as the dominant taxa likely involved in Hg methylation in the soil. Phylogenetic analysis also uncovered some hgcAB sequences closely related to three novel Hg methylators, Geobacter anodireducens, Desulfuromonas sp. DDH964, and Desulfovibrio sp. J2 in these paddy soils. These findings shed new light on microbial community composition and major clades driving Hg methylation in rice paddy soils and have important implications in developing strategies for minimizing bioaccumulation of MeHg in rice grains and thus human exposure. Our findings also offer new insights into the biogeochemical factors controlling MeHg production and have the potential global implications for understanding the evolution and distribution of Hg(II) methylating microorganisms not only in paddy habitats but also other ecosystems such as wetlands.

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