Rice consumption is now recognized as an important pathway of human exposure to the neurotoxin methylmercury (MeHg), particularly in countries where rice is a staple food. Although the discovery of a two-gene cluster hgcAB has linked Hg methylation to several phylogenetically diverse groups of anaerobic microorganisms converting inorganic mercury (Hg) to MeHg, the prevalence and diversity of Hg methylators in microbial communities of rice paddy soils remain unclear. We characterized the abundance and distribution of hgcAB genes using third-generation PacBio long-read sequencing and Illumina short-read metagenomic sequencing, in combination with quantitative PCR analyses in several mine-impacted paddy soils from southwest China. Both Illumina and PacBio sequencing analyses revealed that Hg methylating communities were dominated by iron-reducing bacteria (i.e., Geobacter) and methanogens, with a relatively low abundance of hgcA + sulfate-reducing bacteria in the soil. A positive correlation was observed between the MeHg content in soil and the relative abundance of Geobacter carrying the hgcA gene. Phylogenetic analysis also uncovered some hgcAB sequences closely related to three novel Hg methylators, Geobacter anodireducens, Desulf uromonas sp. DDH964, and Desulfovibrio sp. J2, among which G. anodireducens was validated for its ability to methylate Hg. These findings shed new light on microbial community composition and major clades likely driving Hg methylation in rice paddy soils.

BackgroundThe ecological consequences of mercury (Hg) pollution—one of the major pollutants worldwide—on microbial taxonomic and functional attributes remain poorly understood and largely unexplored. Using soils from two typical Hg-impacted regions across China, here, we evaluated the role of Hg pollution in regulating bacterial abundance, diversity, and co-occurrence network. We also investigated the associations between Hg contents and the relative abundance of microbial functional genes by analyzing the soil metagenomes from a subset of those sites.ResultsWe found that soil Hg largely influenced the taxonomic and functional attributes of microbial communities in the two studied regions. In general, Hg pollution was negatively related to bacterial abundance, but positively related to the diversity of bacteria in two separate regions. We also found some consistent associations between soil Hg contents and the community composition of bacteria. For example, soil total Hg content was positively related to the relative abundance of Firmicutes and Bacteroidetes in both paddy and upland soils. In contrast, the methylmercury (MeHg) concentration was negatively correlated to the relative abundance of Nitrospirae in the two types of soils. Increases in soil Hg pollution correlated with drastic changes in the relative abundance of ecological clusters within the co-occurrence network of bacterial communities for the two regions. Using metagenomic data, we were also able to detect the effect of Hg pollution on multiple functional genes relevant to key soil processes such as element cycles and Hg transformations (e.g., methylation and reduction).ConclusionsTogether, our study provides solid evidence that Hg pollution has predictable and significant effects on multiple taxonomic and functional attributes including bacterial abundance, diversity, and the relative abundance of ecological clusters and functional genes. Our results suggest an increase in soil Hg pollution linked to human activities will lead to predictable shifts in the taxonomic and functional attributes in the Hg-impacted areas, with potential implications for sustainable management of agricultural ecosystems and elsewhere.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0572-7) contains supplementary material, which is available to authorized users.

Summary Viruses can affect microbial dynamics, metabolism and biogeochemical cycles in aquatic ecosystems. However, viral diversity and functions in agricultural soils are poorly known, especially in the rhizosphere. We used virome analysis of eight rhizosphere and bulk soils to study viral diversity and potential biogeochemical impacts in an agro‐ecosystem. The order Caudovirales was the predominant viral type in agricultural soils, with Siphoviridae being the most abundant family. Phylogenetic analysis of the terminase large subunit of Caudovirales identified high viral diversity and three novel groups. Viral community composition differed significantly between bulk and rhizosphere soils. Soil pH was the main environmental driver of the viral community structure. Remarkably, abundant auxiliary carbohydrate‐active enzyme (CAZyme) genes were detected in viromes, including glycoside hydrolases, carbohydrate esterases and carbohydrate‐binding modules. These results demonstrate that virus‐encoded putative auxiliary metabolic genes or metabolic genes that may change bacterial metabolism and indirectly contribute to biogeochemical cycling, especially carbon cycling, in agricultural soil.