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Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus

BACKGROUND: Lateral Gene Transfer (LGT) is a major contributor to bacterial evolution and up to 25% of a bacterium's genome may have been acquired by this process over evolutionary periods of time. Successful LGT requires both the physical transfer of DNA and its successful incorporation into t...

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Autores principales: Labbate, Maurizio, Boucher, Yan, Chowdhury, Piklu Roy, Stokes, Hatch W
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3262767/
https://www.ncbi.nlm.nih.gov/pubmed/22093957
http://dx.doi.org/10.1186/1471-2180-11-253
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author Labbate, Maurizio
Boucher, Yan
Chowdhury, Piklu Roy
Stokes, Hatch W
author_facet Labbate, Maurizio
Boucher, Yan
Chowdhury, Piklu Roy
Stokes, Hatch W
author_sort Labbate, Maurizio
collection PubMed
description BACKGROUND: Lateral Gene Transfer (LGT) is a major contributor to bacterial evolution and up to 25% of a bacterium's genome may have been acquired by this process over evolutionary periods of time. Successful LGT requires both the physical transfer of DNA and its successful incorporation into the host cell. One system that contributes to this latter step by site-specific recombination is the integron. Integrons are found in many diverse bacterial Genera and is a genetic system ubiquitous in vibrios that captures mobile DNA at a dedicated site. The presence of integron-associated genes, contained within units of mobile DNA called gene cassettes makes up a substantial component of the vibrio genome (1-3%). Little is known about the role of this system since the vast majority of genes in vibrio arrays are highly novel and functions cannot be ascribed. It is generally regarded that strain-specific mobile genes cannot be readily integrated into the cellular machinery since any perturbation of core metabolism is likely to result in a loss of fitness. RESULTS: In this study, at least one mobile gene contained within the Vibrio rotiferianus strain DAT722, but lacking close relatives elsewhere, is shown to greatly reduce host fitness when deleted and tested in growth assays. The precise role of the mobile gene product is unknown but impacts on the regulation of outermembrane porins. This demonstrates that strain specific laterally acquired mobile DNA can be integrated rapidly into bacterial networks such that it becomes advantageous for survival and adaptation in changing environments. CONCLUSIONS: Mobile genes that are highly strain specific are generally believed to act in isolation. This is because perturbation of existing cell machinery by the acquisition of a new gene by LGT is highly likely to lower fitness. In contrast, we show here that at least one mobile gene, apparently unique to a strain, encodes a product that has integrated into central cellular metabolic processes such that it greatly lowers fitness when lost under those conditions likely to be commonly encountered for the free living cell. This has ramifications for our understanding of the role mobile gene encoded products play in the cell from a systems biology perspective.
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spelling pubmed-32627672012-01-21 Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus Labbate, Maurizio Boucher, Yan Chowdhury, Piklu Roy Stokes, Hatch W BMC Microbiol Research Article BACKGROUND: Lateral Gene Transfer (LGT) is a major contributor to bacterial evolution and up to 25% of a bacterium's genome may have been acquired by this process over evolutionary periods of time. Successful LGT requires both the physical transfer of DNA and its successful incorporation into the host cell. One system that contributes to this latter step by site-specific recombination is the integron. Integrons are found in many diverse bacterial Genera and is a genetic system ubiquitous in vibrios that captures mobile DNA at a dedicated site. The presence of integron-associated genes, contained within units of mobile DNA called gene cassettes makes up a substantial component of the vibrio genome (1-3%). Little is known about the role of this system since the vast majority of genes in vibrio arrays are highly novel and functions cannot be ascribed. It is generally regarded that strain-specific mobile genes cannot be readily integrated into the cellular machinery since any perturbation of core metabolism is likely to result in a loss of fitness. RESULTS: In this study, at least one mobile gene contained within the Vibrio rotiferianus strain DAT722, but lacking close relatives elsewhere, is shown to greatly reduce host fitness when deleted and tested in growth assays. The precise role of the mobile gene product is unknown but impacts on the regulation of outermembrane porins. This demonstrates that strain specific laterally acquired mobile DNA can be integrated rapidly into bacterial networks such that it becomes advantageous for survival and adaptation in changing environments. CONCLUSIONS: Mobile genes that are highly strain specific are generally believed to act in isolation. This is because perturbation of existing cell machinery by the acquisition of a new gene by LGT is highly likely to lower fitness. In contrast, we show here that at least one mobile gene, apparently unique to a strain, encodes a product that has integrated into central cellular metabolic processes such that it greatly lowers fitness when lost under those conditions likely to be commonly encountered for the free living cell. This has ramifications for our understanding of the role mobile gene encoded products play in the cell from a systems biology perspective. BioMed Central 2011-11-18 /pmc/articles/PMC3262767/ /pubmed/22093957 http://dx.doi.org/10.1186/1471-2180-11-253 Text en Copyright ©2011 Labbate et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Labbate, Maurizio
Boucher, Yan
Chowdhury, Piklu Roy
Stokes, Hatch W
Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus
title Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus
title_full Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus
title_fullStr Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus
title_full_unstemmed Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus
title_short Integration of a laterally acquired gene into a cell network important for growth in a strain of Vibrio rotiferianus
title_sort integration of a laterally acquired gene into a cell network important for growth in a strain of vibrio rotiferianus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3262767/
https://www.ncbi.nlm.nih.gov/pubmed/22093957
http://dx.doi.org/10.1186/1471-2180-11-253
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