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Multiple phase-variable mechanisms, including capsular polysaccharides, modify bacteriophage susceptibility in Bacteroides thetaiotaomicron

Nathan T. Porter, Andrew J. Hryckowian, Bryan D. Merrill, Jaime J. Fuentes, Jackson O. Gardner, Robert W. P. Glowacki, Shaleni Singh, Ryan D. Crawford, Evan S. Snitkin, Justin L. Sonnenburg, Eric C. Martens
doi: https://doi.org/10.1101/521070
Nathan T. Porter
1Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA
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Andrew J. Hryckowian
2Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305
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  • For correspondence: andrew.hryckowian@gmail.com emartens@umich.edu
Bryan D. Merrill
2Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305
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Jaime J. Fuentes
1Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA
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Jackson O. Gardner
2Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305
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Robert W. P. Glowacki
1Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA
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Shaleni Singh
1Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA
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Ryan D. Crawford
3Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48109, USA
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Evan S. Snitkin
1Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA
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Justin L. Sonnenburg
2Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305
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Eric C. Martens
1Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA
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  • For correspondence: andrew.hryckowian@gmail.com emartens@umich.edu
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Abstract

A variety of cell surface structures, including capsular polysaccharides (CPS), dictate interactions between bacteria and their environment including their viruses (bacteriophages). Members of the prominent human gut Bacteroidetes characteristically produce several phase-variable CPS, but their contributions to bacteriophage interactions are unknown. We used engineered strains of the human symbiont Bacteroides thetaiotaomicron, which differ only in the CPS they express, to isolate bacteriophages from two locations in the United States. Testing each of 71 bacteriophages against a panel of strains that express wild-type phase-variable CPS, one of eight different single CPS, or no CPS at all, revealed that each phage infects only a subset of otherwise isogenic strains. Deletion of infection-permissive CPS from B. thetaiotaomicron was sufficient to abolish infection for several individual bacteriophages, while infection of wild-type B. thetaiotaomicron with either of two different bacteriophages rapidly selected for expression of non-permissive CPS. Surprisingly, acapsular B. thetaiotaomicron also escapes complete killing by these bacteriophages, but surviving bacteria exhibit increased expression of 8 distinct phase-variable lipoproteins. When constitutively expressed, one of these lipoproteins promotes resistance to multiple bacteriophages. Finally, both wild-type and acapsular B. thetaiotaomicron were able to separately co-exist with one bacteriophage for over two months in the mouse gut, suggesting that phase-variation promotes resistance but also generates sufficient numbers of susceptible revertants to allow bacteriophage persistence. Our results reveal important roles for Bacteroides CPS and other cell surface structures that allow these bacteria to persist despite bacteriophage predation and hold important implications for using bacteriophages therapeutically to target gut symbionts.

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Posted March 26, 2020.
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Multiple phase-variable mechanisms, including capsular polysaccharides, modify bacteriophage susceptibility in Bacteroides thetaiotaomicron
Nathan T. Porter, Andrew J. Hryckowian, Bryan D. Merrill, Jaime J. Fuentes, Jackson O. Gardner, Robert W. P. Glowacki, Shaleni Singh, Ryan D. Crawford, Evan S. Snitkin, Justin L. Sonnenburg, Eric C. Martens
bioRxiv 521070; doi: https://doi.org/10.1101/521070
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Multiple phase-variable mechanisms, including capsular polysaccharides, modify bacteriophage susceptibility in Bacteroides thetaiotaomicron
Nathan T. Porter, Andrew J. Hryckowian, Bryan D. Merrill, Jaime J. Fuentes, Jackson O. Gardner, Robert W. P. Glowacki, Shaleni Singh, Ryan D. Crawford, Evan S. Snitkin, Justin L. Sonnenburg, Eric C. Martens
bioRxiv 521070; doi: https://doi.org/10.1101/521070

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