Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection

Bacteriophages, the viruses infecting bacteria, hold great potential for the treatment of multidrug-resistant bacterial infections and other applications due to their unparalleled diversity and recent breakthroughs in their genetic engineering. However, fundamental knowledge of the molecular mechani...

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Autores principales:	Enea Maffei, Aisylu Shaidullina, Marco Burkolter, Yannik Heyer, Fabienne Estermann, Valentin Druelle, Patrick Sauer, Luc Willi, Sarah Michaelis, Hubert Hilbi, David S. Thaler, Alexander Harms
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/25cbfa218379460eb89244b3f155a834
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spelling	oai:doaj.org-article:25cbfa218379460eb89244b3f155a8342021-11-25T05:33:14ZSystematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection1544-91731545-7885https://doaj.org/article/25cbfa218379460eb89244b3f155a8342021-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8594841/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Bacteriophages, the viruses infecting bacteria, hold great potential for the treatment of multidrug-resistant bacterial infections and other applications due to their unparalleled diversity and recent breakthroughs in their genetic engineering. However, fundamental knowledge of the molecular mechanisms underlying phage–host interactions is mostly confined to a few traditional model systems and did not keep pace with the recent massive expansion of the field. The true potential of molecular biology encoded by these viruses has therefore remained largely untapped, and phages for therapy or other applications are often still selected empirically. We therefore sought to promote a systematic exploration of phage–host interactions by composing a well-assorted library of 68 newly isolated phages infecting the model organism Escherichia coli that we share with the community as the BASEL (BActeriophage SElection for your Laboratory) collection. This collection is largely representative of natural E. coli phage diversity and was intensively characterized phenotypically and genomically alongside 10 well-studied traditional model phages. We experimentally determined essential host receptors of all phages, quantified their sensitivity to 11 defense systems across different layers of bacterial immunity, and matched these results to the phages’ host range across a panel of pathogenic enterobacterial strains. Clear patterns in the distribution of phage phenotypes and genomic features highlighted systematic differences in the potency of different immunity systems and suggested the molecular basis of receptor specificity in several phage groups. Our results also indicate strong trade-offs between fitness traits like broad host recognition and resistance to bacterial immunity that might drive the divergent adaptation of different phage groups to specific ecological niches. We envision that the BASEL collection will inspire future work exploring the biology of bacteriophages and their hosts by facilitating the discovery of underlying molecular mechanisms as the basis for an effective translation into biotechnology or therapeutic applications. This study presents the BASEL collection of phages that infect the model bacterium Escherichia coli; this resource for the community is representative of natural E. coli phage diversity and has been extensively characterized phenotypically and genomically.Enea MaffeiAisylu ShaidullinaMarco BurkolterYannik HeyerFabienne EstermannValentin DruellePatrick SauerLuc WilliSarah MichaelisHubert HilbiDavid S. ThalerAlexander HarmsPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 11 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Enea Maffei Aisylu Shaidullina Marco Burkolter Yannik Heyer Fabienne Estermann Valentin Druelle Patrick Sauer Luc Willi Sarah Michaelis Hubert Hilbi David S. Thaler Alexander Harms Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection
description	Bacteriophages, the viruses infecting bacteria, hold great potential for the treatment of multidrug-resistant bacterial infections and other applications due to their unparalleled diversity and recent breakthroughs in their genetic engineering. However, fundamental knowledge of the molecular mechanisms underlying phage–host interactions is mostly confined to a few traditional model systems and did not keep pace with the recent massive expansion of the field. The true potential of molecular biology encoded by these viruses has therefore remained largely untapped, and phages for therapy or other applications are often still selected empirically. We therefore sought to promote a systematic exploration of phage–host interactions by composing a well-assorted library of 68 newly isolated phages infecting the model organism Escherichia coli that we share with the community as the BASEL (BActeriophage SElection for your Laboratory) collection. This collection is largely representative of natural E. coli phage diversity and was intensively characterized phenotypically and genomically alongside 10 well-studied traditional model phages. We experimentally determined essential host receptors of all phages, quantified their sensitivity to 11 defense systems across different layers of bacterial immunity, and matched these results to the phages’ host range across a panel of pathogenic enterobacterial strains. Clear patterns in the distribution of phage phenotypes and genomic features highlighted systematic differences in the potency of different immunity systems and suggested the molecular basis of receptor specificity in several phage groups. Our results also indicate strong trade-offs between fitness traits like broad host recognition and resistance to bacterial immunity that might drive the divergent adaptation of different phage groups to specific ecological niches. We envision that the BASEL collection will inspire future work exploring the biology of bacteriophages and their hosts by facilitating the discovery of underlying molecular mechanisms as the basis for an effective translation into biotechnology or therapeutic applications. This study presents the BASEL collection of phages that infect the model bacterium Escherichia coli; this resource for the community is representative of natural E. coli phage diversity and has been extensively characterized phenotypically and genomically.
format	article
author	Enea Maffei Aisylu Shaidullina Marco Burkolter Yannik Heyer Fabienne Estermann Valentin Druelle Patrick Sauer Luc Willi Sarah Michaelis Hubert Hilbi David S. Thaler Alexander Harms
author_facet	Enea Maffei Aisylu Shaidullina Marco Burkolter Yannik Heyer Fabienne Estermann Valentin Druelle Patrick Sauer Luc Willi Sarah Michaelis Hubert Hilbi David S. Thaler Alexander Harms
author_sort	Enea Maffei
title	Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection
title_short	Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection
title_full	Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection
title_fullStr	Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection
title_full_unstemmed	Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection
title_sort	systematic exploration of escherichia coli phage–host interactions with the basel phage collection
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/25cbfa218379460eb89244b3f155a834
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Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection

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