Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments

ABSTRACT Swarming bacteria are challenged by the need to invade hostile environments. Swarms of the flagellated bacterium Paenibacillus vortex can collectively transport other microorganisms. Here we show that P. vortex can invade toxic environments by carrying antibiotic-degrading bacteria; this tr...

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Autores principales:	Alin Finkelshtein, Dalit Roth, Eshel Ben Jacob, Colin J. Ingham
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c3e0a18d7a0e41c192c1775da68eedb2
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spelling	oai:doaj.org-article:c3e0a18d7a0e41c192c1775da68eedb22021-11-15T15:49:03ZBacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments10.1128/mBio.00074-152150-7511https://doaj.org/article/c3e0a18d7a0e41c192c1775da68eedb22015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00074-15https://doaj.org/toc/2150-7511ABSTRACT Swarming bacteria are challenged by the need to invade hostile environments. Swarms of the flagellated bacterium Paenibacillus vortex can collectively transport other microorganisms. Here we show that P. vortex can invade toxic environments by carrying antibiotic-degrading bacteria; this transport is mediated by a specialized, phenotypic subpopulation utilizing a process not dependent on cargo motility. Swarms of beta-lactam antibiotic (BLA)-sensitive P. vortex used beta-lactamase-producing, resistant, cargo bacteria to detoxify BLAs in their path. In the presence of BLAs, both transporter and cargo bacteria gained from this temporary cooperation; there was a positive correlation between BLA resistance and dispersal. P. vortex transported only the most beneficial antibiotic-resistant cargo (including environmental and clinical isolates) in a sustained way. P. vortex displayed a bet-hedging strategy that promoted the colonization of nontoxic niches by P. vortex alone; when detoxifying cargo bacteria were not needed, they were lost. This work has relevance for the dispersal of antibiotic-resistant microorganisms and for strategies for asymmetric cooperation with agricultural and medical implications. IMPORTANCE Antibiotic resistance is a major health threat. We show a novel mechanism for the local spread of antibiotic resistance. This involves interactions between different bacteria: one species provides an enzyme that detoxifies the antibiotic (a sessile cargo bacterium carrying a resistance gene), while the other (Paenibacillus vortex) moves itself and transports the cargo. P. vortex used a bet-hedging strategy, colonizing new environments alone when the cargo added no benefit, but cooperating when the cargo was needed. This work is of interest in an evolutionary context and sheds light on fundamental questions, such as how environmental antibiotic resistance may lead to clinical resistance and also microbial social organization, as well as the costs, benefits, and risks of dispersal in the environment.Alin FinkelshteinDalit RothEshel Ben JacobColin J. InghamAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Alin Finkelshtein Dalit Roth Eshel Ben Jacob Colin J. Ingham Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments
description	ABSTRACT Swarming bacteria are challenged by the need to invade hostile environments. Swarms of the flagellated bacterium Paenibacillus vortex can collectively transport other microorganisms. Here we show that P. vortex can invade toxic environments by carrying antibiotic-degrading bacteria; this transport is mediated by a specialized, phenotypic subpopulation utilizing a process not dependent on cargo motility. Swarms of beta-lactam antibiotic (BLA)-sensitive P. vortex used beta-lactamase-producing, resistant, cargo bacteria to detoxify BLAs in their path. In the presence of BLAs, both transporter and cargo bacteria gained from this temporary cooperation; there was a positive correlation between BLA resistance and dispersal. P. vortex transported only the most beneficial antibiotic-resistant cargo (including environmental and clinical isolates) in a sustained way. P. vortex displayed a bet-hedging strategy that promoted the colonization of nontoxic niches by P. vortex alone; when detoxifying cargo bacteria were not needed, they were lost. This work has relevance for the dispersal of antibiotic-resistant microorganisms and for strategies for asymmetric cooperation with agricultural and medical implications. IMPORTANCE Antibiotic resistance is a major health threat. We show a novel mechanism for the local spread of antibiotic resistance. This involves interactions between different bacteria: one species provides an enzyme that detoxifies the antibiotic (a sessile cargo bacterium carrying a resistance gene), while the other (Paenibacillus vortex) moves itself and transports the cargo. P. vortex used a bet-hedging strategy, colonizing new environments alone when the cargo added no benefit, but cooperating when the cargo was needed. This work is of interest in an evolutionary context and sheds light on fundamental questions, such as how environmental antibiotic resistance may lead to clinical resistance and also microbial social organization, as well as the costs, benefits, and risks of dispersal in the environment.
format	article
author	Alin Finkelshtein Dalit Roth Eshel Ben Jacob Colin J. Ingham
author_facet	Alin Finkelshtein Dalit Roth Eshel Ben Jacob Colin J. Ingham
author_sort	Alin Finkelshtein
title	Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments
title_short	Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments
title_full	Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments
title_fullStr	Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments
title_full_unstemmed	Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments
title_sort	bacterial swarms recruit cargo bacteria to pave the way in toxic environments
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/c3e0a18d7a0e41c192c1775da68eedb2
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Bacterial Swarms Recruit Cargo Bacteria To Pave the Way in Toxic Environments

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