Lateral Gene Transfer in a Heavy Metal-Contaminated-Groundwater Microbial Community

Authors

Christopher L. Hemme, University of Rhode IslandFollow
Stefan J. Green
Lavanya Rishishwar
Om Prakash
Angelica Pettenato
Romy Chakraborty
Adam M. Deutschbauer
Joy D. Van Nostrand
Liyou Wu
Zhili He
I. King Jordan
Terry C. Hazen
Adam P. Arkin
Joel E. Kostka
Jizhong Zhou

Document Type

Article

Date of Original Version

2016

Department

Biomedical and Pharmaceutical Sciences

Abstract

Unraveling the drivers controlling the response and adaptation of biological communities to environmental change, especially anthropogenic activities, is a central but poorly understood issue in ecology and evolution. Comparative genomics studies suggest that lateral gene transfer (LGT) is a major force driving microbial genome evolution, but its role in the evolution of microbial communities remains elusive. To delineate the importance of LGT in mediating the response of a groundwater microbial community to heavy metal contamination, representative Rhodanobacter reference genomes were sequenced and compared to shotgun metagenome sequences. 16S rRNA gene-based amplicon sequence analysis indicated that Rhodanobacter populations were highly abundant in contaminated wells with low pHs and high levels of nitrate and heavy metals but remained rare in the uncontaminated wells. Sequence comparisons revealed that multiple geochemically important genes, including genes encoding Fe²⁺/Pb²⁺ permeases, most denitrification enzymes, and cytochrome c₅₅₃, were native to Rhodanobacter and not subjected to LGT. In contrast, the Rhodanobacter pangenome contained a recombinational hot spot in which numerous metal resistance genes were subjected to LGT and/or duplication. In particular, Co²⁺/Zn²⁺/Cd²⁺ efflux and mercuric resistance operon genes appeared to be highly mobile within Rhodanobacter populations. Evidence of multiple duplications of a mercuric resistance operon common to most Rhodanobacter strains was also observed. Collectively, our analyses indicated the importance of LGT during the evolution of groundwater microbial communities in response to heavy metal contamination, and a conceptual model was developed to display such adaptive evolutionary processes for explaining the extreme dominance of Rhodanobacter populations in the contaminated groundwater microbiome.

Citation/Publisher Attribution

Hemme CL, Green SJ, Rishishwar L, Prakash O, Pettenato A, Chakraborty R, Deutschbauer AM, Van Nostrand JD, Wu L, He Z, Jordan IK, Hazen TC, Arkin AP, Kostka JE, Zhou J. 2016. Lateral gene transfer in a heavy metal-contaminated-groundwater microbial community. mBio 7(2):e02234-15. doi: 10.1128/mBio.02234-15.

Available at: http://dx.doi.org/10.1128/mBio.02234-15

Creative Commons License

This work is licensed under a Creative Commons Attribution-Noncommercial-Share Alike 3.0 License.