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

Abstract

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, representativeRhodanobacterreference genomes were sequenced and compared to shotgun metagenome sequences. 16S rRNA gene-based amplicon sequence analysis indicated thatRhodanobacterpopulations 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 cytochromec₅₅₃, were native toRhodanobacterand not subjected to LGT. In contrast, theRhodanobacterpangenome 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 withinRhodanobacterpopulations. Evidence of multiple duplications of a mercuric resistance operon common to mostRhodanobacterstrains was also observed. Collectively, our analyses indicated the importance of LGT duringmore » 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 ofRhodanobacterpopulations in the contaminated groundwater microbiome. IMPORTANCELateral gene transfer (LGT), along with positive selection and gene duplication, are the three main mechanisms that drive adaptive evolution of microbial genomes and communities, but their relative importance is unclear. Some recent studies suggested that LGT is a major adaptive mechanism for microbial populations in response to changing environments, and hence, it could also be critical in shaping microbial community structure. However, direct evidence of LGT and its rates in extant natural microbial communities in response to changing environments is still lacking. Our results presented in this study provide explicit evidence that LGT played a crucial role in driving the evolution of a groundwater microbial community in response to extreme heavy metal contamination. It appears that acquisition of genes critical for survival, growth, and reproduction via LGT is the most rapid and effective way to enable microorganisms and associated microbial communities to quickly adapt to abrupt harsh environmental stresses.« less

Authors:

Hemme, Christopher L. ^[1]; Green, Stefan J. ^[2]; Rishishwar, Lavanya ^[3]; Prakash, Om ^[4]; Pettenato, Angelica ^[5]; Chakraborty, Romy ^[5]; Deutschbauer, Adam M. ^[6]; Van Nostrand, Joy D. ^[7]; Wu, Liyou ^[7]; He, Zhili ^[7]; Jordan, I. King ^[8]; Hazen, Terry C.  ^[9];

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• Search DOE PAGES for ORCID "0000-0002-2536-9993"

Arkin, Adam P. ^[10]; Kostka, Joel E. ^[3]; Zhou, Jizhong ^[11]; Huffnagle, ed., Gary B.

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+ Show Author Affiliations

1. Institute for Environmental Genomics, Department of Microbiology and Plant Sciences, University of Oklahoma, Norman, Oklahoma, USA, Ostrow School of Dentistry, University of Southern California, Los Angeles, California, USA
2. Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois, USA, DNA Services Facility, University of Illinois at Chicago, Chicago, Illinois, USA
3. School of Biology and Earth &, Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
4. National Centre for Cell Science, Ganeshkhind, Pune, Maharashtra, India
5. Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA
6. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA
7. Institute for Environmental Genomics, Department of Microbiology and Plant Sciences, University of Oklahoma, Norman, Oklahoma, USA
8. School of Biology and Earth &, Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA, PanAmerican Bioinformatics Institute, Santa Marta, Magdalena, Colombia
9. Department of Civil &, Environmental Engineering, University of Tennessee, Knoxville, Tennessee, USA, Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, Tennessee, USA, Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA, Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
10. Department of Bioengineering, Lawrence Berkeley National Laboratory, Berkeley, California, USA
11. Institute for Environmental Genomics, Department of Microbiology and Plant Sciences, University of Oklahoma, Norman, Oklahoma, USA, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA, State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China

Publication Date:

Wed May 04 00:00:00 EDT 2016

Research Org.:

Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:

1784829

Alternate Identifier(s):

OSTI ID: 1327748; OSTI ID: 1379276

Grant/Contract Number:  

AC02-05CH11231; FG02-07ER64398; AC05-00OR22725

Resource Type:

Published Article

Journal Name:

mBio

Additional Journal Information:

Journal Name: mBio Journal Volume: 7 Journal Issue: 2; Journal ID: ISSN 2161-2129

Publisher:

American Society for Microbiology

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES