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Proceedings of the National Academy of Sciences of the United States of America, volume 115, issue 29, pages 7593-7598

Costs and benefits of provocation in bacterial warfare

Gonzalez Diego ^{1, 2}

Sabnis Akshay ³

Foster Kevin ¹

Mavridou Despoina A. I. ³

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Department of Zoology, University of Oxford, OX1 3PS Oxford, United Kingdom; |

Department of Fundamental Microbiology, Faculty of Biology and Medicine, University of Lausanne, 1015 Lausanne, Switzerland; |

Medical Research Council Centre for Molecular Bacteriology and Infection, Department of Life Sciences, Imperial College London, London SW7 2DD, United Kingdom |

Publication type: Journal Article

Publication date: 2018-07-02

Proceedings of the National Academy of Sciences (PNAS)

Journal: Proceedings of the National Academy of Sciences of the United States of America

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Impact factor: 11.1

ISSN: 00278424, 10916490

DOI: 10.1073/pnas.1801028115

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PubMed ID: 29967163

Multidisciplinary

Abstract

Significance Bacteria live in dense environments where competition for space and resources is fierce. For this reason, they often use diffusible toxins to eliminate closely related strains. Some toxins trigger systematic retaliation, raising the question of the role of provocation in bacterial warfare. We combine mathematical modeling and experiments to study the costs and benefits of provocation. In one-to-one encounters, provocation is costly as it leads to strong counterattacks. However, with three or more strains present, provocation can provide benefits via a “divide-and-conquer” effect, whereby a strain forces its opponents to wipe each other out. This effect could be harnessed as a targeted antibacterial approach; adding low levels of certain antibiotics to communities can promote warfare and cross-elimination between strains. Competition in animals involves a wide variety of aggressive behaviors. One of the most sophisticated strategies for a focal actor is to provoke a competitor into uncontrolled aggression toward other competitors. Like animals, bacteria rely on a broad spectrum of molecular weapons, some of which provoke potential rivals by triggering retaliation. While bacterial provocation is well documented, its potential adaptive value has received little attention. Here, we examine the costs and benefits of provocation using mathematical modeling and experiments with Escherichia coli strains encoding colicin toxins. We show that provocation is typically costly in one-to-one encounters because a provoking strain receives a strong reciprocal attack compared with nonprovoking strains. By contrast, provocation can be strongly beneficial in communities including more than two toxin-producing strains, especially when the provoker is shielded from, or resistant to, its opponents’ toxins. In these scenarios, we demonstrate that the benefit of provocation derives from a “divide-and-conquer” effect by which aggression-provoking toxin producers force their competitors into increased reciprocal aggression, leading to their cross-elimination. Furthermore, we show that this effect can be mimicked by using antibiotics that promote warfare among strains in a bacterial community, highlighting the potential of provocation as an antimicrobial approach.

By date By citations

Citations by journals

	1 2 3 4
Nature Communications	Nature Communications, 4, 9.3% Nature Communications 4 publications, 9.3%
Microorganisms	Microorganisms, 2, 4.65% Microorganisms 2 publications, 4.65%
Nature Reviews Microbiology	Nature Reviews Microbiology, 2, 4.65% Nature Reviews Microbiology 2 publications, 4.65%
Current Biology	Current Biology, 2, 4.65% Current Biology 2 publications, 4.65%
eLife	eLife, 2, 4.65% eLife 2 publications, 4.65%
International Journal of Molecular Sciences	International Journal of Molecular Sciences, 1, 2.33% International Journal of Molecular Sciences 1 publication, 2.33%
Microbiology	Microbiology, 1, 2.33% Microbiology 1 publication, 2.33%
Journal of Medical Microbiology	Journal of Medical Microbiology, 1, 2.33% Journal of Medical Microbiology 1 publication, 2.33%
Royal Society Open Science	Royal Society Open Science, 1, 2.33% Royal Society Open Science 1 publication, 2.33%
Antibiotics	Antibiotics, 1, 2.33% Antibiotics 1 publication, 2.33%
Philosophical Transactions of the Royal Society B: Biological Sciences	Philosophical Transactions of the Royal Society B: Biological Sciences, 1, 2.33% Philosophical Transactions of the Royal Society B: Biological Sciences 1 publication, 2.33%
Scientific Reports	Scientific Reports, 1, 2.33% Scientific Reports 1 publication, 2.33%
Journal of Biological Chemistry	Journal of Biological Chemistry, 1, 2.33% Journal of Biological Chemistry 1 publication, 2.33%
Biofilm	Biofilm, 1, 2.33% Biofilm 1 publication, 2.33%
Journal of Evolutionary Biology	Journal of Evolutionary Biology, 1, 2.33% Journal of Evolutionary Biology 1 publication, 2.33%
FEBS Journal	FEBS Journal, 1, 2.33% FEBS Journal 1 publication, 2.33%
Environmental Science & Technology	Environmental Science & Technology, 1, 2.33% Environmental Science & Technology 1 publication, 2.33%
Natural Product Reports	Natural Product Reports, 1, 2.33% Natural Product Reports 1 publication, 2.33%
mBio	mBio, 1, 2.33% mBio 1 publication, 2.33%
Cellular Microbiology	Cellular Microbiology, 1, 2.33% Cellular Microbiology 1 publication, 2.33%
Annual Review of Ecology, Evolution, and Systematics	Annual Review of Ecology, Evolution, and Systematics, 1, 2.33% Annual Review of Ecology, Evolution, and Systematics 1 publication, 2.33%
PLoS Pathogens	PLoS Pathogens, 1, 2.33% PLoS Pathogens 1 publication, 2.33%
Applied Microbiology and Biotechnology	Applied Microbiology and Biotechnology, 1, 2.33% Applied Microbiology and Biotechnology 1 publication, 2.33%
Advances in Microbial Physiology	Advances in Microbial Physiology, 1, 2.33% Advances in Microbial Physiology 1 publication, 2.33%
Science Translational Medicine	Science Translational Medicine, 1, 2.33% Science Translational Medicine 1 publication, 2.33%
Lab on a Chip	Lab on a Chip, 1, 2.33% Lab on a Chip 1 publication, 2.33%
	1 2 3 4

Citations by publishers

	1 2 3 4 5 6 7 8
Springer Nature	Springer Nature, 8, 18.6% Springer Nature 8 publications, 18.6%
Multidisciplinary Digital Publishing Institute (MDPI)	Multidisciplinary Digital Publishing Institute (MDPI), 4, 9.3% Multidisciplinary Digital Publishing Institute (MDPI) 4 publications, 9.3%
Elsevier	Elsevier, 4, 9.3% Elsevier 4 publications, 9.3%
Wiley	Wiley, 3, 6.98% Wiley 3 publications, 6.98%
Microbiology Society	Microbiology Society, 2, 4.65% Microbiology Society 2 publications, 4.65%
The Royal Society	The Royal Society, 2, 4.65% The Royal Society 2 publications, 4.65%
Royal Society of Chemistry (RSC)	Royal Society of Chemistry (RSC), 2, 4.65% Royal Society of Chemistry (RSC) 2 publications, 4.65%
eLife Sciences Publications	eLife Sciences Publications, 2, 4.65% eLife Sciences Publications 2 publications, 4.65%
American Society for Biochemistry and Molecular Biology	American Society for Biochemistry and Molecular Biology, 1, 2.33% American Society for Biochemistry and Molecular Biology 1 publication, 2.33%
American Chemical Society (ACS)	American Chemical Society (ACS), 1, 2.33% American Chemical Society (ACS) 1 publication, 2.33%
American Society for Microbiology	American Society for Microbiology, 1, 2.33% American Society for Microbiology 1 publication, 2.33%
Annual Reviews	Annual Reviews, 1, 2.33% Annual Reviews 1 publication, 2.33%
Public Library of Science (PLoS)	Public Library of Science (PLoS), 1, 2.33% Public Library of Science (PLoS) 1 publication, 2.33%
American Association for the Advancement of Science (AAAS)	American Association for the Advancement of Science (AAAS), 1, 2.33% American Association for the Advancement of Science (AAAS) 1 publication, 2.33%
	1 2 3 4 5 6 7 8

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Gonzalez D. et al. Costs and benefits of provocation in bacterial warfare // Proceedings of the National Academy of Sciences of the United States of America. 2018. Vol. 115. No. 29. pp. 7593-7598.

GOST all authors (up to 50) Copy

Gonzalez D., Sabnis A., Foster K., Mavridou D. A. I. Costs and benefits of provocation in bacterial warfare // Proceedings of the National Academy of Sciences of the United States of America. 2018. Vol. 115. No. 29. pp. 7593-7598.

RIS |

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RIS Copy

TY - JOUR

DO - 10.1073/pnas.1801028115

UR - https://doi.org/10.1073%2Fpnas.1801028115

TI - Costs and benefits of provocation in bacterial warfare

T2 - Proceedings of the National Academy of Sciences of the United States of America

AU - Gonzalez, Diego

AU - Sabnis, Akshay

AU - Foster, Kevin

AU - Mavridou, Despoina A. I.

PY - 2018

DA - 2018/07/02 00:00:00

PB - Proceedings of the National Academy of Sciences (PNAS)

SP - 7593-7598

IS - 29

VL - 115

PMID - 29967163

SN - 0027-8424

SN - 1091-6490

ER -

BibTex |

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BibTex Copy

@article{2018_Gonzalez,

author = {Diego Gonzalez and Akshay Sabnis and Kevin Foster and Despoina A. I. Mavridou},

title = {Costs and benefits of provocation in bacterial warfare},

journal = {Proceedings of the National Academy of Sciences of the United States of America},

year = {2018},

volume = {115},

publisher = {Proceedings of the National Academy of Sciences (PNAS)},

month = {jul},

url = {https://doi.org/10.1073%2Fpnas.1801028115},

number = {29},

pages = {7593--7598},

doi = {10.1073/pnas.1801028115}

}

MLA

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MLA Copy

Gonzalez, Diego, et al. “Costs and benefits of provocation in bacterial warfare.” Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 29, Jul. 2018, pp. 7593-7598. https://doi.org/10.1073%2Fpnas.1801028115.

Found error?

Publisher

Proceedings of the National Academy of Sciences (PNAS)

Journal

Proceedings of the National Academy of Sciences of the United States of America

Quartile SCImago

Quartile WOS

Impact factor

11.1

ISSN

00278424 (Print)
10916490 (Electronic)