Prophage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation

ABSTRACT Natural transformation is a broadly conserved mechanism of horizontal gene transfer (HGT) in bacteria that can shape their evolution through the acquisition of genes that promote virulence, antibiotic resistance, and other traits. Recent work has established that neighbor predation via type...

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Autores principales: Roberto C. Molina-Quiroz, Triana N. Dalia, Andrew Camilli, Ankur B. Dalia, Cecilia A. Silva-Valenzuela
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Lenguaje:EN
Publicado: American Society for Microbiology 2020
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HGT
Acceso en línea:https://doaj.org/article/f3adafb05b0b4fa78a51d6e7bd7819aa
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spelling oai:doaj.org-article:f3adafb05b0b4fa78a51d6e7bd7819aa2021-11-15T15:31:13ZProphage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation10.1128/mSphere.00975-202379-5042https://doaj.org/article/f3adafb05b0b4fa78a51d6e7bd7819aa2020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00975-20https://doaj.org/toc/2379-5042ABSTRACT Natural transformation is a broadly conserved mechanism of horizontal gene transfer (HGT) in bacteria that can shape their evolution through the acquisition of genes that promote virulence, antibiotic resistance, and other traits. Recent work has established that neighbor predation via type VI secretion systems, bacteriocins, and virulent phages plays an important role in promoting HGT. Here, we demonstrate that in chitin estuary microcosms, Vibrio cholerae K139 lysogens exhibit prophage-dependent neighbor predation of nonlysogens to enhance HGT. Through predation of nonlysogens, K139 lysogens also have a fitness advantage under these microcosm conditions. The ecological strategy revealed by our work provides a better understanding of the evolutionary mechanisms used by bacteria to adapt in their natural setting and contributes to our understanding of the selective pressures that may drive prophage maintenance in bacterial genomes. IMPORTANCE Prophages are nearly ubiquitous in bacterial species. These integrated phage elements have previously been implicated in horizontal gene transfer (HGT) largely through their ability to carry out transduction (generalized or specialized). Here, we show that prophage-encoded viral particles promote neighbor predation leading to enhanced HGT by natural transformation in the waterborne pathogen Vibrio cholerae. Our findings contribute to a comprehensive understanding of the dynamic forces involved in prophage maintenance which ultimately drive the evolution of naturally competent bacteria in their natural environment.Roberto C. Molina-QuirozTriana N. DaliaAndrew CamilliAnkur B. DaliaCecilia A. Silva-ValenzuelaAmerican Society for MicrobiologyarticleHGTVibrio choleraebacteriophageschitinnatural transformationneighbor predationMicrobiologyQR1-502ENmSphere, Vol 5, Iss 6 (2020)
institution DOAJ
collection DOAJ
language EN
topic HGT
Vibrio cholerae
bacteriophages
chitin
natural transformation
neighbor predation
Microbiology
QR1-502
spellingShingle HGT
Vibrio cholerae
bacteriophages
chitin
natural transformation
neighbor predation
Microbiology
QR1-502
Roberto C. Molina-Quiroz
Triana N. Dalia
Andrew Camilli
Ankur B. Dalia
Cecilia A. Silva-Valenzuela
Prophage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation
description ABSTRACT Natural transformation is a broadly conserved mechanism of horizontal gene transfer (HGT) in bacteria that can shape their evolution through the acquisition of genes that promote virulence, antibiotic resistance, and other traits. Recent work has established that neighbor predation via type VI secretion systems, bacteriocins, and virulent phages plays an important role in promoting HGT. Here, we demonstrate that in chitin estuary microcosms, Vibrio cholerae K139 lysogens exhibit prophage-dependent neighbor predation of nonlysogens to enhance HGT. Through predation of nonlysogens, K139 lysogens also have a fitness advantage under these microcosm conditions. The ecological strategy revealed by our work provides a better understanding of the evolutionary mechanisms used by bacteria to adapt in their natural setting and contributes to our understanding of the selective pressures that may drive prophage maintenance in bacterial genomes. IMPORTANCE Prophages are nearly ubiquitous in bacterial species. These integrated phage elements have previously been implicated in horizontal gene transfer (HGT) largely through their ability to carry out transduction (generalized or specialized). Here, we show that prophage-encoded viral particles promote neighbor predation leading to enhanced HGT by natural transformation in the waterborne pathogen Vibrio cholerae. Our findings contribute to a comprehensive understanding of the dynamic forces involved in prophage maintenance which ultimately drive the evolution of naturally competent bacteria in their natural environment.
format article
author Roberto C. Molina-Quiroz
Triana N. Dalia
Andrew Camilli
Ankur B. Dalia
Cecilia A. Silva-Valenzuela
author_facet Roberto C. Molina-Quiroz
Triana N. Dalia
Andrew Camilli
Ankur B. Dalia
Cecilia A. Silva-Valenzuela
author_sort Roberto C. Molina-Quiroz
title Prophage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation
title_short Prophage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation
title_full Prophage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation
title_fullStr Prophage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation
title_full_unstemmed Prophage-Dependent Neighbor Predation Fosters Horizontal Gene Transfer by Natural Transformation
title_sort prophage-dependent neighbor predation fosters horizontal gene transfer by natural transformation
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/f3adafb05b0b4fa78a51d6e7bd7819aa
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