CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction

ABSTRACT A powerful contributor to prokaryotic evolution is horizontal gene transfer (HGT) through transformation, conjugation, and transduction, which can be advantageous, neutral, or detrimental to fitness. Bacteria and archaea control HGT and phage infection through CRISPR-Cas (clustered regularl...

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Autores principales:	Bridget N. J. Watson, Raymond H. J. Staals, Peter C. Fineran
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	CRISPR-Cas bacteriophages genomic islands horizontal gene transfer plasmids transduction Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b1081660118546c791dce1a0a6a6135e
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spelling	oai:doaj.org-article:b1081660118546c791dce1a0a6a6135e2021-11-15T15:53:26ZCRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction10.1128/mBio.02406-172150-7511https://doaj.org/article/b1081660118546c791dce1a0a6a6135e2018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02406-17https://doaj.org/toc/2150-7511ABSTRACT A powerful contributor to prokaryotic evolution is horizontal gene transfer (HGT) through transformation, conjugation, and transduction, which can be advantageous, neutral, or detrimental to fitness. Bacteria and archaea control HGT and phage infection through CRISPR-Cas (clustered regularly interspaced short palindromic repeats–CRISPR-associated proteins) adaptive immunity. Although the benefits of resisting phage infection are evident, this can come at a cost of inhibiting the acquisition of other beneficial genes through HGT. Despite the ability of CRISPR-Cas to limit HGT through conjugation and transformation, its role in transduction is largely overlooked. Transduction is the phage-mediated transfer of bacterial DNA between cells and arguably has the greatest impact on HGT. We demonstrate that in Pectobacterium atrosepticum, CRISPR-Cas can inhibit the transduction of plasmids and chromosomal loci. In addition, we detected phage-mediated transfer of a large plant pathogenicity genomic island and show that CRISPR-Cas can inhibit its transduction. Despite these inhibitory effects of CRISPR-Cas on transduction, its more common role in phage resistance promotes rather than diminishes HGT via transduction by protecting bacteria from phage infection. This protective effect can also increase transduction of phage-sensitive members of mixed populations. CRISPR-Cas systems themselves display evidence of HGT, but little is known about their lateral dissemination between bacteria and whether transduction can contribute. We show that, through transduction, bacteria can acquire an entire chromosomal CRISPR-Cas system, including cas genes and phage-targeting spacers. We propose that the positive effect of CRISPR-Cas phage immunity on enhancing transduction surpasses the rarer cases where gene flow by transduction is restricted. IMPORTANCE The generation of genetic diversity through acquisition of DNA is a powerful contributor to microbial evolution and occurs through transformation, conjugation, and transduction. Of these, transduction, the phage-mediated transfer of bacterial DNA, is arguably the major route for genetic exchange. CRISPR-Cas adaptive immune systems control gene transfer by conjugation and transformation, but transduction has been mostly overlooked. Our results indicate that CRISPR-Cas can impede, but typically enhances the transduction of plasmids, chromosomal genes, and pathogenicity islands. By limiting wild-type phage replication, CRISPR-Cas immunity increases transduction in both phage-resistant and -sensitive members of mixed populations. Furthermore, we demonstrate mobilization of a chromosomal CRISPR-Cas system containing phage-targeting spacers by generalized transduction, which might partly account for the uneven distribution of these systems in nature. Overall, the ability of CRISPR-Cas to promote transduction reveals an unexpected impact of adaptive immunity on horizontal gene transfer, with broader implications for microbial evolution.Bridget N. J. WatsonRaymond H. J. StaalsPeter C. FineranAmerican Society for MicrobiologyarticleCRISPR-Casbacteriophagesgenomic islandshorizontal gene transferplasmidstransductionMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	CRISPR-Cas bacteriophages genomic islands horizontal gene transfer plasmids transduction Microbiology QR1-502
spellingShingle	CRISPR-Cas bacteriophages genomic islands horizontal gene transfer plasmids transduction Microbiology QR1-502 Bridget N. J. Watson Raymond H. J. Staals Peter C. Fineran CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction
description	ABSTRACT A powerful contributor to prokaryotic evolution is horizontal gene transfer (HGT) through transformation, conjugation, and transduction, which can be advantageous, neutral, or detrimental to fitness. Bacteria and archaea control HGT and phage infection through CRISPR-Cas (clustered regularly interspaced short palindromic repeats–CRISPR-associated proteins) adaptive immunity. Although the benefits of resisting phage infection are evident, this can come at a cost of inhibiting the acquisition of other beneficial genes through HGT. Despite the ability of CRISPR-Cas to limit HGT through conjugation and transformation, its role in transduction is largely overlooked. Transduction is the phage-mediated transfer of bacterial DNA between cells and arguably has the greatest impact on HGT. We demonstrate that in Pectobacterium atrosepticum, CRISPR-Cas can inhibit the transduction of plasmids and chromosomal loci. In addition, we detected phage-mediated transfer of a large plant pathogenicity genomic island and show that CRISPR-Cas can inhibit its transduction. Despite these inhibitory effects of CRISPR-Cas on transduction, its more common role in phage resistance promotes rather than diminishes HGT via transduction by protecting bacteria from phage infection. This protective effect can also increase transduction of phage-sensitive members of mixed populations. CRISPR-Cas systems themselves display evidence of HGT, but little is known about their lateral dissemination between bacteria and whether transduction can contribute. We show that, through transduction, bacteria can acquire an entire chromosomal CRISPR-Cas system, including cas genes and phage-targeting spacers. We propose that the positive effect of CRISPR-Cas phage immunity on enhancing transduction surpasses the rarer cases where gene flow by transduction is restricted. IMPORTANCE The generation of genetic diversity through acquisition of DNA is a powerful contributor to microbial evolution and occurs through transformation, conjugation, and transduction. Of these, transduction, the phage-mediated transfer of bacterial DNA, is arguably the major route for genetic exchange. CRISPR-Cas adaptive immune systems control gene transfer by conjugation and transformation, but transduction has been mostly overlooked. Our results indicate that CRISPR-Cas can impede, but typically enhances the transduction of plasmids, chromosomal genes, and pathogenicity islands. By limiting wild-type phage replication, CRISPR-Cas immunity increases transduction in both phage-resistant and -sensitive members of mixed populations. Furthermore, we demonstrate mobilization of a chromosomal CRISPR-Cas system containing phage-targeting spacers by generalized transduction, which might partly account for the uneven distribution of these systems in nature. Overall, the ability of CRISPR-Cas to promote transduction reveals an unexpected impact of adaptive immunity on horizontal gene transfer, with broader implications for microbial evolution.
format	article
author	Bridget N. J. Watson Raymond H. J. Staals Peter C. Fineran
author_facet	Bridget N. J. Watson Raymond H. J. Staals Peter C. Fineran
author_sort	Bridget N. J. Watson
title	CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction
title_short	CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction
title_full	CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction
title_fullStr	CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction
title_full_unstemmed	CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction
title_sort	crispr-cas-mediated phage resistance enhances horizontal gene transfer by transduction
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/b1081660118546c791dce1a0a6a6135e
work_keys_str_mv	AT bridgetnjwatson crisprcasmediatedphageresistanceenhanceshorizontalgenetransferbytransduction AT raymondhjstaals crisprcasmediatedphageresistanceenhanceshorizontalgenetransferbytransduction AT petercfineran crisprcasmediatedphageresistanceenhanceshorizontalgenetransferbytransduction
_version_	1718427297430634496

CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction

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