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Title: Unraveling Microbial Communities Associated with Methylmercury Production in Paddy Soils

Abstract

Here, we report 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, Desulfuromonas sp. DDH964, and Desulfovibrio sp. J2, among which G. anodireducens was validated for its ability to methylate Hg. Lastly, these findings shed new light on microbialmore » community composition and major clades likely driving Hg methylation in rice paddy soils.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3]; ORCiD logo [2];  [4];  [5]; ORCiD logo [6]; ORCiD logo [7]
  1. Huazhong Agricultural University, Wuhan (China); Chinese Academy of Sciences (CAS), Beijing (China)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Chinese Academy of Sciences (CAS), Beijing (China)
  4. The University of Melbourne, Victoria (Australia)
  5. Zhejiang Univ. (China)
  6. Chinese Academy of Sciences (CAS), Beijing (China); The University of Melbourne, Victoria (Australia)
  7. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1490597
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Science and Technology
Additional Journal Information:
Journal Volume: 52; Journal Issue: 22; Journal ID: ISSN 0013-936X
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES

Citation Formats

Liu, Yu-Rong, Johs, Alexander, Bi, Li, Lu, Xia, Hu, Hang-Wei, Sun, Dan, He, Ji-Zheng, and Gu, Baohua. Unraveling Microbial Communities Associated with Methylmercury Production in Paddy Soils. United States: N. p., 2018. Web. doi:10.1021/acs.est.8b03052.
Liu, Yu-Rong, Johs, Alexander, Bi, Li, Lu, Xia, Hu, Hang-Wei, Sun, Dan, He, Ji-Zheng, & Gu, Baohua. Unraveling Microbial Communities Associated with Methylmercury Production in Paddy Soils. United States. https://doi.org/10.1021/acs.est.8b03052
Liu, Yu-Rong, Johs, Alexander, Bi, Li, Lu, Xia, Hu, Hang-Wei, Sun, Dan, He, Ji-Zheng, and Gu, Baohua. Wed . "Unraveling Microbial Communities Associated with Methylmercury Production in Paddy Soils". United States. https://doi.org/10.1021/acs.est.8b03052. https://www.osti.gov/servlets/purl/1490597.
@article{osti_1490597,
title = {Unraveling Microbial Communities Associated with Methylmercury Production in Paddy Soils},
author = {Liu, Yu-Rong and Johs, Alexander and Bi, Li and Lu, Xia and Hu, Hang-Wei and Sun, Dan and He, Ji-Zheng and Gu, Baohua},
abstractNote = {Here, we report 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, Desulfuromonas sp. DDH964, and Desulfovibrio sp. J2, among which G. anodireducens was validated for its ability to methylate Hg. Lastly, these findings shed new light on microbial community composition and major clades likely driving Hg methylation in rice paddy soils.},
doi = {10.1021/acs.est.8b03052},
journal = {Environmental Science and Technology},
number = 22,
volume = 52,
place = {United States},
year = {Wed Oct 17 00:00:00 EDT 2018},
month = {Wed Oct 17 00:00:00 EDT 2018}
}

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Figures / Tables:

Fig. 1 Fig. 1: Abundances and distribution of hgc$A$ genes from metagenomes for the selected paddy and upland soils obtained from Fenghuang (FH) and Wanshan (WS) mining areas in Southwest China; (a) Log10-transformed qPCR data for hgc$A$ gene copy number for Deltaproteobacteria and Archaea in the selected paddy soils, while qPCR formore » Firmicutes yielded no hgc$A$. (b) Relative abundance ofhgc$A$ genes (from shotgun metagenomic sequencing) normalized to metagenome size (log Gbp); (c) Assignments of hgc$A$ genes from shotgun metagenomic sequencing at the genus level. Circle size represents the relative abundance of hgc$A$sequences assigned to a specific genus in each sample. Samples FHA-U, FHB-U and WSA-U were from upland fields.« less

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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.