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....

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Autores principales:	Ankita Kothari, Drishti Soneja, Albert Tang, Hans K. Carlson, Adam M. Deutschbauer, Aindrila Mukhopadhyay
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	plasmid mercury resistance metal resistance horizontal gene transfer natural transformation natural competence Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1ed5d692b62f45a9befb4ad055d022e0
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spelling	oai:doaj.org-article:1ed5d692b62f45a9befb4ad055d022e02021-12-02T18:39:15ZNative Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates10.1128/mSystems.00588-192379-5077https://doaj.org/article/1ed5d692b62f45a9befb4ad055d022e02019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00588-19https://doaj.org/toc/2379-5077ABSTRACT 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 in Escherichia 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. IMPORTANCE 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.Ankita KothariDrishti SonejaAlbert TangHans K. CarlsonAdam M. DeutschbauerAindrila MukhopadhyayAmerican Society for Microbiologyarticleplasmidmercury resistancemetal resistancehorizontal gene transfernatural transformationnatural competenceMicrobiologyQR1-502ENmSystems, Vol 4, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	plasmid mercury resistance metal resistance horizontal gene transfer natural transformation natural competence Microbiology QR1-502
spellingShingle	plasmid mercury resistance metal resistance horizontal gene transfer natural transformation natural competence Microbiology QR1-502 Ankita Kothari Drishti Soneja Albert Tang Hans K. Carlson Adam M. Deutschbauer Aindrila Mukhopadhyay Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates
description	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 in Escherichia 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. IMPORTANCE 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.
format	article
author	Ankita Kothari Drishti Soneja Albert Tang Hans K. Carlson Adam M. Deutschbauer Aindrila Mukhopadhyay
author_facet	Ankita Kothari Drishti Soneja Albert Tang Hans K. Carlson Adam M. Deutschbauer Aindrila Mukhopadhyay
author_sort	Ankita Kothari
title	Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates
title_short	Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates
title_full	Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates
title_fullStr	Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates
title_full_unstemmed	Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates
title_sort	native plasmid-encoded mercury resistance genes are functional and demonstrate natural transformation in environmental bacterial isolates
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/1ed5d692b62f45a9befb4ad055d022e0
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Native Plasmid-Encoded Mercury Resistance Genes Are Functional and Demonstrate Natural Transformation in Environmental Bacterial Isolates

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