Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population

The type VI secretion system (T6SS) operons of Vibrio cholerae contain extraordinarily diverse arrays of toxic effector and cognate immunity genes, which are thought to play an important role in the environmental lifestyle and adaptation of this human pathogen. Through the T6SS, proteinaceous “spear...

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Main Authors: Hussain, Nora A. S., Kirchberger, Paul C., Case, Rebecca J., Boucher, Yann F.
Other Authors: School of Biological Sciences
Format: Article
Language:English
Published: 2021
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Online Access:https://hdl.handle.net/10356/151777
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spelling sg-ntu-dr.10356-1517772021-07-17T20:11:37Z Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population Hussain, Nora A. S. Kirchberger, Paul C. Case, Rebecca J. Boucher, Yann F. School of Biological Sciences Singapore Centre for Environmental Life Sciences and Engineering Science::Biological sciences Vibrio Cholerae Type VI Secretion System The type VI secretion system (T6SS) operons of Vibrio cholerae contain extraordinarily diverse arrays of toxic effector and cognate immunity genes, which are thought to play an important role in the environmental lifestyle and adaptation of this human pathogen. Through the T6SS, proteinaceous “spears” tipped with antibacterial effectors are injected into adjacent cells, killing those not possessing immunity proteins to these effectors. Here, we investigate the T6SS-mediated dynamics of bacterial competition within a single environmental population of V. cholerae. We show that numerous members of a North American V. cholerae population possess strain-specific repertoires of cytotoxic T6SS effector and immunity genes. Using pairwise competition assays, we demonstrate that the vast majority of T6SS-mediated duels end in stalemates between strains with different T6SS repertoires. However, horizontally acquired effector and immunity genes can significantly alter the outcome of these competitions. Frequently observed horizontal gene transfer events can both increase or reduce competition between distantly related strains by homogenizing or diversifying the T6SS repertoire. Our results also suggest temperature-dependent outcomes in T6SS competition, with environmental isolates faring better against a pathogenic strain under native conditions than under those resembling a host-associated environment. Taken altogether, these interactions produce density-dependent fitness effects and a constant T6SS-mediated arms race in individual V. cholerae populations, which could ultimately preserve intraspecies diversity. Since T6SSs are widespread, we expect within-population diversity in T6SS repertoires and the resulting competitive dynamics to be a common theme in bacterial species harboring this machinery. Published version This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) grant numbers RGPIN-2020-04422 (to YB) and RGPIN-2018-05706 (to RC) and the Integrated Microbial Biodiversity program of the Canadian Institute for Advanced Research (to YB), as well as graduate student scholarships from Alberta Innovates–Technology Futures (to PK), the Department of Biological Sciences at the University of Alberta (to NH), Alberta Advanced Education (to NH), and the Faculty of Graduate Studies and Research at the University of Alberta (to NH). The funding bodies had no role in study design, data collection and interpretation, and or the decision to submit the work for publication. 2021-07-16T10:16:27Z 2021-07-16T10:16:27Z 2021 Journal Article Hussain, N. A. S., Kirchberger, P. C., Case, R. J. & Boucher, Y. F. (2021). Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population. Frontiers in Microbiology, 12, 671092-. https://dx.doi.org/10.3389/fmicb.2021.671092 1664-302X https://hdl.handle.net/10356/151777 10.3389/fmicb.2021.671092 34122386 2-s2.0-85107632032 12 671092 en Frontiers in Microbiology © 2021 Hussain, Kirchberger, Case and Boucher. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
Vibrio Cholerae
Type VI Secretion System
spellingShingle Science::Biological sciences
Vibrio Cholerae
Type VI Secretion System
Hussain, Nora A. S.
Kirchberger, Paul C.
Case, Rebecca J.
Boucher, Yann F.
Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population
description The type VI secretion system (T6SS) operons of Vibrio cholerae contain extraordinarily diverse arrays of toxic effector and cognate immunity genes, which are thought to play an important role in the environmental lifestyle and adaptation of this human pathogen. Through the T6SS, proteinaceous “spears” tipped with antibacterial effectors are injected into adjacent cells, killing those not possessing immunity proteins to these effectors. Here, we investigate the T6SS-mediated dynamics of bacterial competition within a single environmental population of V. cholerae. We show that numerous members of a North American V. cholerae population possess strain-specific repertoires of cytotoxic T6SS effector and immunity genes. Using pairwise competition assays, we demonstrate that the vast majority of T6SS-mediated duels end in stalemates between strains with different T6SS repertoires. However, horizontally acquired effector and immunity genes can significantly alter the outcome of these competitions. Frequently observed horizontal gene transfer events can both increase or reduce competition between distantly related strains by homogenizing or diversifying the T6SS repertoire. Our results also suggest temperature-dependent outcomes in T6SS competition, with environmental isolates faring better against a pathogenic strain under native conditions than under those resembling a host-associated environment. Taken altogether, these interactions produce density-dependent fitness effects and a constant T6SS-mediated arms race in individual V. cholerae populations, which could ultimately preserve intraspecies diversity. Since T6SSs are widespread, we expect within-population diversity in T6SS repertoires and the resulting competitive dynamics to be a common theme in bacterial species harboring this machinery.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Hussain, Nora A. S.
Kirchberger, Paul C.
Case, Rebecca J.
Boucher, Yann F.
format Article
author Hussain, Nora A. S.
Kirchberger, Paul C.
Case, Rebecca J.
Boucher, Yann F.
author_sort Hussain, Nora A. S.
title Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population
title_short Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population
title_full Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population
title_fullStr Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population
title_full_unstemmed Modular molecular weaponry plays a key role in competition within an environmental Vibrio cholerae population
title_sort modular molecular weaponry plays a key role in competition within an environmental vibrio cholerae population
publishDate 2021
url https://hdl.handle.net/10356/151777
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