Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis

Abstract Background The crAss-like phages are ubiquitous and highly abundant members of the human gut virome that infect commensal bacteria of the order Bacteroidales. Although incapable of lysogeny, these viruses demonstrate long-term persistence in the human gut microbiome, dominating the virome i...

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Main Authors: Andrey N. Shkoporov, Ekaterina V. Khokhlova, Niamh Stephens, Cara Hueston, Samuel Seymour, Andrew J. Hryckowian, Dimitri Scholz, R. Paul Ross, Colin Hill
Format: Article
Language:English
Published: BMC 2021-08-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-021-01084-3
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spelling doaj-ff11d5a8f013466aacf9249cc8cb1acd2021-08-22T11:47:25ZengBMCBMC Biology1741-70072021-08-0119111610.1186/s12915-021-01084-3Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalisAndrey N. Shkoporov0Ekaterina V. Khokhlova1Niamh Stephens2Cara Hueston3Samuel Seymour4Andrew J. Hryckowian5Dimitri Scholz6R. Paul Ross7Colin Hill8School of Microbiology, University College CorkAPC Microbiome Ireland, University College CorkConway Institute of Biomolecular and Biomedical Research, University College DublinAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkDepartment of Medicine, University of Wisconsin School of Medicine and Public HealthConway Institute of Biomolecular and Biomedical Research, University College DublinSchool of Microbiology, University College CorkSchool of Microbiology, University College CorkAbstract Background The crAss-like phages are ubiquitous and highly abundant members of the human gut virome that infect commensal bacteria of the order Bacteroidales. Although incapable of lysogeny, these viruses demonstrate long-term persistence in the human gut microbiome, dominating the virome in some individuals. Results Here we show that rapid phase variation of alternate capsular polysaccharides in Bacteroides intestinalis cultures plays an important role in a dynamic equilibrium between phage sensitivity and resistance, allowing phage and bacteria to multiply in parallel. The data also suggests the role of a concomitant phage persistence mechanism associated with delayed lysis of infected cells, similar to carrier state infection. From an ecological and evolutionary standpoint, this type of phage-host interaction is consistent with the Piggyback-the-Winner model, which suggests a preference towards lysogenic or other “benign” forms of phage infection when the host is stably present at high abundance. Conclusion Long-term persistence of bacteriophage and host could result from mutually beneficial mechanisms driving bacterial strain-level diversity and phage survival in complex environments.https://doi.org/10.1186/s12915-021-01084-3crAss-like phagescrAssphageHuman gut microbiomeHuman viromePhase variationCapsular polysaccharides
collection DOAJ
language English
format Article
sources DOAJ
author Andrey N. Shkoporov
Ekaterina V. Khokhlova
Niamh Stephens
Cara Hueston
Samuel Seymour
Andrew J. Hryckowian
Dimitri Scholz
R. Paul Ross
Colin Hill
spellingShingle Andrey N. Shkoporov
Ekaterina V. Khokhlova
Niamh Stephens
Cara Hueston
Samuel Seymour
Andrew J. Hryckowian
Dimitri Scholz
R. Paul Ross
Colin Hill
Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis
BMC Biology
crAss-like phages
crAssphage
Human gut microbiome
Human virome
Phase variation
Capsular polysaccharides
author_facet Andrey N. Shkoporov
Ekaterina V. Khokhlova
Niamh Stephens
Cara Hueston
Samuel Seymour
Andrew J. Hryckowian
Dimitri Scholz
R. Paul Ross
Colin Hill
author_sort Andrey N. Shkoporov
title Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis
title_short Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis
title_full Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis
title_fullStr Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis
title_full_unstemmed Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis
title_sort long-term persistence of crass-like phage crass001 is associated with phase variation in bacteroides intestinalis
publisher BMC
series BMC Biology
issn 1741-7007
publishDate 2021-08-01
description Abstract Background The crAss-like phages are ubiquitous and highly abundant members of the human gut virome that infect commensal bacteria of the order Bacteroidales. Although incapable of lysogeny, these viruses demonstrate long-term persistence in the human gut microbiome, dominating the virome in some individuals. Results Here we show that rapid phase variation of alternate capsular polysaccharides in Bacteroides intestinalis cultures plays an important role in a dynamic equilibrium between phage sensitivity and resistance, allowing phage and bacteria to multiply in parallel. The data also suggests the role of a concomitant phage persistence mechanism associated with delayed lysis of infected cells, similar to carrier state infection. From an ecological and evolutionary standpoint, this type of phage-host interaction is consistent with the Piggyback-the-Winner model, which suggests a preference towards lysogenic or other “benign” forms of phage infection when the host is stably present at high abundance. Conclusion Long-term persistence of bacteriophage and host could result from mutually beneficial mechanisms driving bacterial strain-level diversity and phage survival in complex environments.
topic crAss-like phages
crAssphage
Human gut microbiome
Human virome
Phase variation
Capsular polysaccharides
url https://doi.org/10.1186/s12915-021-01084-3
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