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Title: Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates

Abstract

Plasmid-mediated horizontal gene transfer (HGT) is a major driver of genetic diversity in bacteria. We experimentally validated the function of a putative mercury resistance operon present on an abundant 8-kbp native plasmid found in groundwater samples without detectable levels of mercury. Phylogenetic analyses of the plasmid-encoded mercury reductases from the studied groundwater site show them to be distinct from those reported in proximal metal-contaminated sites. We synthesized the entire native plasmid and demonstrated that the plasmid was sufficient to confer functional mercury resistance inEscherichia coli. Given the possibility that natural transformation is a prevalent HGT mechanism in the low-cell-density environments of groundwaters, we also assayed bacterial strains from this environment for competence. We used the native plasmid-encoded metal resistance to design a screen and identified 17 strains positive for natural transformation. We selected 2 of the positive strains along with a model bacterium to fully confirm HGT via natural transformation. From an ecological perspective, the role of the native plasmid population in providing advantageous traits combined with the microbiome’s capacity to take up environmental DNA enables rapid adaptation to environmental stresses. Horizontal transfer of mobile genetic elements via natural transformation has been poorly understood in environmental microbes. Here, we confirmmore » the functionality of a native plasmid-encoded mercury resistance operon in a model microbe and then query for the dissemination of this resistance trait via natural transformation into environmental bacterial isolates. We identified 17 strains including Gram-positive and Gram-negative bacteria to be naturally competent. These strains were able to successfully take up the plasmid DNA and obtain a clear growth advantage in the presence of mercury. Our study provides important insights into gene dissemination via natural transformation enabling rapid adaptation to dynamic stresses in groundwater environments.« less

Authors:
ORCiD logo [1];  [1];  [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1];  [4]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States)
  3. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Vanderbilt Univ., Nashville, TN (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1591854
Grant/Contract Number:  
[AC02-05CH11231]
Resource Type:
Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
[ Journal Volume: 4; Journal Issue: 6]; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; plasmid; mercury resistance; metal resistance; horizontal gene transfer; natural transformation; natural competence; mercury tolerance

Citation Formats

Kothari, Ankita, Soneja, Drishti, Tang, Albert, Carlson, Hans K., Deutschbauer, Adam M., Mukhopadhyay, Aindrila, and Bordenstein, Seth. Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates. United States: N. p., 2019. Web. doi:10.1128/mSystems.00588-19.
Kothari, Ankita, Soneja, Drishti, Tang, Albert, Carlson, Hans K., Deutschbauer, Adam M., Mukhopadhyay, Aindrila, & Bordenstein, Seth. Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates. United States. doi:10.1128/mSystems.00588-19.
Kothari, Ankita, Soneja, Drishti, Tang, Albert, Carlson, Hans K., Deutschbauer, Adam M., Mukhopadhyay, Aindrila, and Bordenstein, Seth. Tue . "Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates". United States. doi:10.1128/mSystems.00588-19. https://www.osti.gov/servlets/purl/1591854.
@article{osti_1591854,
title = {Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates},
author = {Kothari, Ankita and Soneja, Drishti and Tang, Albert and Carlson, Hans K. and Deutschbauer, Adam M. and Mukhopadhyay, Aindrila and Bordenstein, Seth},
abstractNote = {Plasmid-mediated horizontal gene transfer (HGT) is a major driver of genetic diversity in bacteria. We experimentally validated the function of a putative mercury resistance operon present on an abundant 8-kbp native plasmid found in groundwater samples without detectable levels of mercury. Phylogenetic analyses of the plasmid-encoded mercury reductases from the studied groundwater site show them to be distinct from those reported in proximal metal-contaminated sites. We synthesized the entire native plasmid and demonstrated that the plasmid was sufficient to confer functional mercury resistance inEscherichia coli. Given the possibility that natural transformation is a prevalent HGT mechanism in the low-cell-density environments of groundwaters, we also assayed bacterial strains from this environment for competence. We used the native plasmid-encoded metal resistance to design a screen and identified 17 strains positive for natural transformation. We selected 2 of the positive strains along with a model bacterium to fully confirm HGT via natural transformation. From an ecological perspective, the role of the native plasmid population in providing advantageous traits combined with the microbiome’s capacity to take up environmental DNA enables rapid adaptation to environmental stresses. Horizontal transfer of mobile genetic elements via natural transformation has been poorly understood in environmental microbes. Here, we confirm the functionality of a native plasmid-encoded mercury resistance operon in a model microbe and then query for the dissemination of this resistance trait via natural transformation into environmental bacterial isolates. We identified 17 strains including Gram-positive and Gram-negative bacteria to be naturally competent. These strains were able to successfully take up the plasmid DNA and obtain a clear growth advantage in the presence of mercury. Our study provides important insights into gene dissemination via natural transformation enabling rapid adaptation to dynamic stresses in groundwater environments.},
doi = {10.1128/mSystems.00588-19},
journal = {mSystems},
number = [6],
volume = [4],
place = {United States},
year = {2019},
month = {12}
}

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Works referenced in this record:

Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Lateral Gene Transfer in a Heavy Metal-Contaminated-Groundwater Microbial Community
journal, April 2016

  • Hemme, Christopher L.; Green, Stefan J.; Rishishwar, Lavanya
  • mBio, Vol. 7, Issue 2
  • DOI: 10.1128/mBio.02234-15

NMR Structure Determination of a Membrane Protein with Two Transmembrane Helices in Micelles:  MerF of the Bacterial Mercury Detoxification System ,
journal, April 2005

  • Howell, Stanley C.; Mesleh, Michael F.; Opella, Stanley J.
  • Biochemistry, Vol. 44, Issue 13
  • DOI: 10.1021/bi048095v

PaperBLAST: Text Mining Papers for Information about Homologs
journal, August 2017


The rapid generation of mutation data matrices from protein sequences
journal, January 1992


Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids
journal, October 2014

  • Millan, A. San; Peña-Miller, R.; Toll-Riera, M.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6208

Confidence Limits on Phylogenies: an Approach Using the Bootstrap
journal, July 1985


Natural Competence and the Evolution of DNA Uptake Specificity
journal, January 2014

  • Mell, J. C.; Redfield, R. J.
  • Journal of Bacteriology, Vol. 196, Issue 8
  • DOI: 10.1128/JB.01293-13

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

The prokaryotic tree of life: past, present…and future?
journal, May 2008

  • McInerney, James O.; Cotton, James A.; Pisani, Davide
  • Trends in Ecology & Evolution, Vol. 23, Issue 5
  • DOI: 10.1016/j.tree.2008.01.008

The Mercury Resistance Operon: From an Origin in a Geothermal Environment to an Efficient Detoxification Machine
journal, January 2012


The neighbor-joining method: a new method for reconstructing phylogenetic trees.
journal, July 1987


Prospects for inferring very large phylogenies by using the neighbor-joining method
journal, July 2004

  • Tamura, K.; Nei, M.; Kumar, S.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 30
  • DOI: 10.1073/pnas.0404206101

SPOCTOPUS: a combined predictor of signal peptides and membrane protein topology
journal, October 2008


Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community
journal, February 2010

  • Hemme, Christopher L.; Deng, Ye; Gentry, Terry J.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.154

Comparative metagenomics reveals impact of contaminants on groundwater microbiomes
journal, October 2015