Efficient Gene Transfer in Bacterial Cell Chains

ABSTRACT Horizontal gene transfer contributes to evolution and the acquisition of new traits. In bacteria, horizontal gene transfer is often mediated by conjugative genetic elements that transfer directly from cell to cell. Integrative and conjugative elements (ICEs; also known as conjugative transp...

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Autores principales:	Ana Babic, Melanie B. Berkmen, Catherine A. Lee, Alan D. Grossman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9bae9689ba5c464f9581cf5453c1230d
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spelling	oai:doaj.org-article:9bae9689ba5c464f9581cf5453c1230d2021-11-15T15:39:07ZEfficient Gene Transfer in Bacterial Cell Chains10.1128/mBio.00027-112150-7511https://doaj.org/article/9bae9689ba5c464f9581cf5453c1230d2011-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00027-11https://doaj.org/toc/2150-7511ABSTRACT Horizontal gene transfer contributes to evolution and the acquisition of new traits. In bacteria, horizontal gene transfer is often mediated by conjugative genetic elements that transfer directly from cell to cell. Integrative and conjugative elements (ICEs; also known as conjugative transposons) are mobile genetic elements that reside within a host genome but can excise to form a circle and transfer by conjugation to recipient cells. ICEs contribute to the spread of genes involved in pathogenesis, symbiosis, metabolism, and antibiotic resistance. Despite its importance, little is known about the mechanisms of conjugation in Gram-positive bacteria or how quickly or frequently transconjugants become donors. We visualized the transfer of the integrative and conjugative element ICEBs1 from a Bacillus subtilis donor to recipient cells in real time using fluorescence microscopy. We found that transfer of DNA from a donor to a recipient appeared to occur at a cell pole or along the lateral cell surface of either cell. Most importantly, we found that when acquired by 1 cell in a chain, ICEBs1 spread rapidly from cell to cell within the chain by additional sequential conjugation events. This intrachain conjugation is inherently more efficient than conjugation that is due to chance encounters between individual cells. Many bacterial species, including pathogenic, commensal, symbiotic, and nitrogen-fixing organisms, harbor ICEs and grow in chains, often as parts of microbial communities. It is likely that efficient intrachain spreading is a general feature of conjugative DNA transfer and serves to amplify the number of cells that acquire conjugative mobile genetic elements. IMPORTANCE Conjugative elements contribute to horizontal gene transfer and the acquisition of new traits. They are largely responsible for spreading antibiotic resistance in bacterial communities. To study the cell biology of conjugation, we visualized conjugative DNA transfer between Bacillus subtilis cells in real time using fluorescence microscopy. In contrast to previous predictions that transfer would occur preferentially from the donor cell pole, we found that transfer of DNA from a donor to a recipient appeared to occur at a cell pole or along the lateral cell surface of either cell. Most importantly, we found that when acquired by 1 cell in a chain, the conjugative DNA spread rapidly from cell to cell within the chain through sequential conjugation events. Since many bacterial species grow naturally in chains, this intrachain transfer is likely a common mechanism for accelerating the spread of conjugative elements within microbial communities.Ana BabicMelanie B. BerkmenCatherine A. LeeAlan D. GrossmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 2 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Ana Babic Melanie B. Berkmen Catherine A. Lee Alan D. Grossman Efficient Gene Transfer in Bacterial Cell Chains
description	ABSTRACT Horizontal gene transfer contributes to evolution and the acquisition of new traits. In bacteria, horizontal gene transfer is often mediated by conjugative genetic elements that transfer directly from cell to cell. Integrative and conjugative elements (ICEs; also known as conjugative transposons) are mobile genetic elements that reside within a host genome but can excise to form a circle and transfer by conjugation to recipient cells. ICEs contribute to the spread of genes involved in pathogenesis, symbiosis, metabolism, and antibiotic resistance. Despite its importance, little is known about the mechanisms of conjugation in Gram-positive bacteria or how quickly or frequently transconjugants become donors. We visualized the transfer of the integrative and conjugative element ICEBs1 from a Bacillus subtilis donor to recipient cells in real time using fluorescence microscopy. We found that transfer of DNA from a donor to a recipient appeared to occur at a cell pole or along the lateral cell surface of either cell. Most importantly, we found that when acquired by 1 cell in a chain, ICEBs1 spread rapidly from cell to cell within the chain by additional sequential conjugation events. This intrachain conjugation is inherently more efficient than conjugation that is due to chance encounters between individual cells. Many bacterial species, including pathogenic, commensal, symbiotic, and nitrogen-fixing organisms, harbor ICEs and grow in chains, often as parts of microbial communities. It is likely that efficient intrachain spreading is a general feature of conjugative DNA transfer and serves to amplify the number of cells that acquire conjugative mobile genetic elements. IMPORTANCE Conjugative elements contribute to horizontal gene transfer and the acquisition of new traits. They are largely responsible for spreading antibiotic resistance in bacterial communities. To study the cell biology of conjugation, we visualized conjugative DNA transfer between Bacillus subtilis cells in real time using fluorescence microscopy. In contrast to previous predictions that transfer would occur preferentially from the donor cell pole, we found that transfer of DNA from a donor to a recipient appeared to occur at a cell pole or along the lateral cell surface of either cell. Most importantly, we found that when acquired by 1 cell in a chain, the conjugative DNA spread rapidly from cell to cell within the chain through sequential conjugation events. Since many bacterial species grow naturally in chains, this intrachain transfer is likely a common mechanism for accelerating the spread of conjugative elements within microbial communities.
format	article
author	Ana Babic Melanie B. Berkmen Catherine A. Lee Alan D. Grossman
author_facet	Ana Babic Melanie B. Berkmen Catherine A. Lee Alan D. Grossman
author_sort	Ana Babic
title	Efficient Gene Transfer in Bacterial Cell Chains
title_short	Efficient Gene Transfer in Bacterial Cell Chains
title_full	Efficient Gene Transfer in Bacterial Cell Chains
title_fullStr	Efficient Gene Transfer in Bacterial Cell Chains
title_full_unstemmed	Efficient Gene Transfer in Bacterial Cell Chains
title_sort	efficient gene transfer in bacterial cell chains
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/9bae9689ba5c464f9581cf5453c1230d
work_keys_str_mv	AT anababic efficientgenetransferinbacterialcellchains AT melaniebberkmen efficientgenetransferinbacterialcellchains AT catherinealee efficientgenetransferinbacterialcellchains AT alandgrossman efficientgenetransferinbacterialcellchains
_version_	1718427782083510272

Efficient Gene Transfer in Bacterial Cell Chains

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