Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation

ABSTRACT Bacteriophages infect an estimated 1023 to 1025 bacterial cells each second, many of which carry physiologically relevant plasmids (e.g., those encoding antibiotic resistance). However, even though phage-plasmid interactions occur on a massive scale and have potentially significant evolutio...

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Autores principales:	Eric C. Keen, Valery V. Bliskovsky, Francisco Malagon, James D. Baker, Jeffrey S. Prince, James S. Klaus, Sankar L. Adhya
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Publicado:	American Society for Microbiology 2017
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/11327bd25c1f41288e42688ec9446787
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spelling	oai:doaj.org-article:11327bd25c1f41288e42688ec94467872021-11-15T15:51:07ZNovel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation10.1128/mBio.02115-162150-7511https://doaj.org/article/11327bd25c1f41288e42688ec94467872017-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02115-16https://doaj.org/toc/2150-7511ABSTRACT Bacteriophages infect an estimated 1023 to 1025 bacterial cells each second, many of which carry physiologically relevant plasmids (e.g., those encoding antibiotic resistance). However, even though phage-plasmid interactions occur on a massive scale and have potentially significant evolutionary, ecological, and biomedical implications, plasmid fate upon phage infection and lysis has not been investigated to date. Here we show that a subset of the natural lytic phage population, which we dub “superspreaders,” releases substantial amounts of intact, transformable plasmid DNA upon lysis, thereby promoting horizontal gene transfer by transformation. Two novel Escherichia coli phage superspreaders, SUSP1 and SUSP2, liberated four evolutionarily distinct plasmids with equal efficiency, including two close relatives of prominent antibiotic resistance vectors in natural environments. SUSP2 also mediated the extensive lateral transfer of antibiotic resistance in unbiased communities of soil bacteria from Maryland and Wyoming. Furthermore, the addition of SUSP2 to cocultures of kanamycin-resistant E. coli and kanamycin-sensitive Bacillus sp. bacteria resulted in roughly 1,000-fold more kanamycin-resistant Bacillus sp. bacteria than arose in phage-free controls. Unlike many other lytic phages, neither SUSP1 nor SUSP2 encodes homologs to known hydrolytic endonucleases, suggesting a simple potential mechanism underlying the superspreading phenotype. Consistent with this model, the deletion of endonuclease IV and the nucleoid-disrupting protein ndd from coliphage T4, a phage known to extensively degrade chromosomal DNA, significantly increased its ability to promote plasmid transformation. Taken together, our results suggest that phage superspreaders may play key roles in microbial evolution and ecology but should be avoided in phage therapy and other medical applications. IMPORTANCE Bacteriophages (phages), viruses that infect bacteria, are the planet’s most numerous biological entities and kill vast numbers of bacteria in natural environments. Many of these bacteria carry plasmids, extrachromosomal DNA elements that frequently encode antibiotic resistance. However, it is largely unknown whether plasmids are destroyed during phage infection or released intact upon phage lysis, whereupon their encoded resistance could be acquired and manifested by other bacteria (transformation). Because phages are being developed to combat antibiotic-resistant bacteria and because transformation is a principal form of horizontal gene transfer, this question has important implications for biomedicine and microbial evolution alike. Here we report the isolation and characterization of two novel Escherichia coli phages, dubbed “superspreaders,” that promote extensive plasmid transformation and efficiently disperse antibiotic resistance genes. Our work suggests that phage superspreaders are not suitable for use in medicine but may help drive bacterial evolution in natural environments.Eric C. KeenValery V. BliskovskyFrancisco MalagonJames D. BakerJeffrey S. PrinceJames S. KlausSankar L. AdhyaAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 1 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Eric C. Keen Valery V. Bliskovsky Francisco Malagon James D. Baker Jeffrey S. Prince James S. Klaus Sankar L. Adhya Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation
description	ABSTRACT Bacteriophages infect an estimated 1023 to 1025 bacterial cells each second, many of which carry physiologically relevant plasmids (e.g., those encoding antibiotic resistance). However, even though phage-plasmid interactions occur on a massive scale and have potentially significant evolutionary, ecological, and biomedical implications, plasmid fate upon phage infection and lysis has not been investigated to date. Here we show that a subset of the natural lytic phage population, which we dub “superspreaders,” releases substantial amounts of intact, transformable plasmid DNA upon lysis, thereby promoting horizontal gene transfer by transformation. Two novel Escherichia coli phage superspreaders, SUSP1 and SUSP2, liberated four evolutionarily distinct plasmids with equal efficiency, including two close relatives of prominent antibiotic resistance vectors in natural environments. SUSP2 also mediated the extensive lateral transfer of antibiotic resistance in unbiased communities of soil bacteria from Maryland and Wyoming. Furthermore, the addition of SUSP2 to cocultures of kanamycin-resistant E. coli and kanamycin-sensitive Bacillus sp. bacteria resulted in roughly 1,000-fold more kanamycin-resistant Bacillus sp. bacteria than arose in phage-free controls. Unlike many other lytic phages, neither SUSP1 nor SUSP2 encodes homologs to known hydrolytic endonucleases, suggesting a simple potential mechanism underlying the superspreading phenotype. Consistent with this model, the deletion of endonuclease IV and the nucleoid-disrupting protein ndd from coliphage T4, a phage known to extensively degrade chromosomal DNA, significantly increased its ability to promote plasmid transformation. Taken together, our results suggest that phage superspreaders may play key roles in microbial evolution and ecology but should be avoided in phage therapy and other medical applications. IMPORTANCE Bacteriophages (phages), viruses that infect bacteria, are the planet’s most numerous biological entities and kill vast numbers of bacteria in natural environments. Many of these bacteria carry plasmids, extrachromosomal DNA elements that frequently encode antibiotic resistance. However, it is largely unknown whether plasmids are destroyed during phage infection or released intact upon phage lysis, whereupon their encoded resistance could be acquired and manifested by other bacteria (transformation). Because phages are being developed to combat antibiotic-resistant bacteria and because transformation is a principal form of horizontal gene transfer, this question has important implications for biomedicine and microbial evolution alike. Here we report the isolation and characterization of two novel Escherichia coli phages, dubbed “superspreaders,” that promote extensive plasmid transformation and efficiently disperse antibiotic resistance genes. Our work suggests that phage superspreaders are not suitable for use in medicine but may help drive bacterial evolution in natural environments.
format	article
author	Eric C. Keen Valery V. Bliskovsky Francisco Malagon James D. Baker Jeffrey S. Prince James S. Klaus Sankar L. Adhya
author_facet	Eric C. Keen Valery V. Bliskovsky Francisco Malagon James D. Baker Jeffrey S. Prince James S. Klaus Sankar L. Adhya
author_sort	Eric C. Keen
title	Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation
title_short	Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation
title_full	Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation
title_fullStr	Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation
title_full_unstemmed	Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation
title_sort	novel “superspreader” bacteriophages promote horizontal gene transfer by transformation
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/11327bd25c1f41288e42688ec9446787
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Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation

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