Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species

ABSTRACT Bacteria that express contact-dependent growth inhibition (CDI) systems outcompete siblings that lack immunity, suggesting that CDI mediates intercellular competition. To further explore the role of CDI in competition, we determined the target cell range of the CDIEC93 system from Escherich...

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Autores principales:	Zachary C. Ruhe, Adam B. Wallace, David A. Low, Christopher S. Hayes
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1f7009aec0804475bfbffc76c460ec7e
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spelling	oai:doaj.org-article:1f7009aec0804475bfbffc76c460ec7e2021-11-15T15:43:09ZReceptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species10.1128/mBio.00480-132150-7511https://doaj.org/article/1f7009aec0804475bfbffc76c460ec7e2013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00480-13https://doaj.org/toc/2150-7511ABSTRACT Bacteria that express contact-dependent growth inhibition (CDI) systems outcompete siblings that lack immunity, suggesting that CDI mediates intercellular competition. To further explore the role of CDI in competition, we determined the target cell range of the CDIEC93 system from Escherichia coli EC93. The CdiAEC93 effector protein recognizes the widely conserved BamA protein as a receptor, yet E. coli EC93 does not inhibit other enterobacterial species. The predicted membrane topology of BamA indicates that three of its extracellular loops vary considerably between species, suggesting that loop heterogeneity may control CDI specificity. Consistent with this hypothesis, other enterobacteria are sensitized to CDIEC93 upon the expression of E. coli bamA and E. coli cells become CDIEC93 resistant when bamA is replaced with alleles from other species. Our data indicate that BamA loops 6 and 7 form the CdiAEC93-binding epitope and their variation between species restricts CDIEC93 target cell selection. Although BamA loops 6 and 7 vary dramatically between species, these regions are identical in hundreds of E. coli strains, suggesting that BamAEcoli and CdiAEC93 play a role in self-nonself discrimination. IMPORTANCE Contact-dependent growth inhibition (CDI) systems are widespread among Gram-negative bacteria, enabling them to bind to neighboring bacterial cells and deliver protein toxins that inhibit cell growth. In this study, we tested the role of CDI in interspecies competition using intestinal isolate Escherichia coli EC93 as an inhibitor cell model. Although E. coli EC93 inhibits different E. coli strains, other bacterial species from the intestine are completely resistant to CDI. We show that resistance is due to small variations in the CDI receptor that prevent other species from being recognized as target cells. CDI receptor interactions thus provide a mechanism by which bacteria can distinguish siblings and other close relatives (self) from more distant relatives or other species of bacteria (nonself). Our results provide a possible means by which antimicrobials could be directed to one or only a few related bacterial pathogens by using a specific receptor “zip code.”Zachary C. RuheAdam B. WallaceDavid A. LowChristopher S. HayesAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 4 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Zachary C. Ruhe Adam B. Wallace David A. Low Christopher S. Hayes Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species
description	ABSTRACT Bacteria that express contact-dependent growth inhibition (CDI) systems outcompete siblings that lack immunity, suggesting that CDI mediates intercellular competition. To further explore the role of CDI in competition, we determined the target cell range of the CDIEC93 system from Escherichia coli EC93. The CdiAEC93 effector protein recognizes the widely conserved BamA protein as a receptor, yet E. coli EC93 does not inhibit other enterobacterial species. The predicted membrane topology of BamA indicates that three of its extracellular loops vary considerably between species, suggesting that loop heterogeneity may control CDI specificity. Consistent with this hypothesis, other enterobacteria are sensitized to CDIEC93 upon the expression of E. coli bamA and E. coli cells become CDIEC93 resistant when bamA is replaced with alleles from other species. Our data indicate that BamA loops 6 and 7 form the CdiAEC93-binding epitope and their variation between species restricts CDIEC93 target cell selection. Although BamA loops 6 and 7 vary dramatically between species, these regions are identical in hundreds of E. coli strains, suggesting that BamAEcoli and CdiAEC93 play a role in self-nonself discrimination. IMPORTANCE Contact-dependent growth inhibition (CDI) systems are widespread among Gram-negative bacteria, enabling them to bind to neighboring bacterial cells and deliver protein toxins that inhibit cell growth. In this study, we tested the role of CDI in interspecies competition using intestinal isolate Escherichia coli EC93 as an inhibitor cell model. Although E. coli EC93 inhibits different E. coli strains, other bacterial species from the intestine are completely resistant to CDI. We show that resistance is due to small variations in the CDI receptor that prevent other species from being recognized as target cells. CDI receptor interactions thus provide a mechanism by which bacteria can distinguish siblings and other close relatives (self) from more distant relatives or other species of bacteria (nonself). Our results provide a possible means by which antimicrobials could be directed to one or only a few related bacterial pathogens by using a specific receptor “zip code.”
format	article
author	Zachary C. Ruhe Adam B. Wallace David A. Low Christopher S. Hayes
author_facet	Zachary C. Ruhe Adam B. Wallace David A. Low Christopher S. Hayes
author_sort	Zachary C. Ruhe
title	Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species
title_short	Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species
title_full	Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species
title_fullStr	Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species
title_full_unstemmed	Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species
title_sort	receptor polymorphism restricts contact-dependent growth inhibition to members of the same species
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/1f7009aec0804475bfbffc76c460ec7e
work_keys_str_mv	AT zacharycruhe receptorpolymorphismrestrictscontactdependentgrowthinhibitiontomembersofthesamespecies AT adambwallace receptorpolymorphismrestrictscontactdependentgrowthinhibitiontomembersofthesamespecies AT davidalow receptorpolymorphismrestrictscontactdependentgrowthinhibitiontomembersofthesamespecies AT christophershayes receptorpolymorphismrestrictscontactdependentgrowthinhibitiontomembersofthesamespecies
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Receptor Polymorphism Restricts Contact-Dependent Growth Inhibition to Members of the Same Species

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