Cargando…

Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration

Vibrio cholerae, the bacterial pathogen responsible for the diarrheal disease cholera, resides in the aquatic environment between outbreaks. For bacteria, genetic variation by lateral gene transfer (LGT) is important for survival and adaptation. In the aquatic environment, V. cholerae is predominant...

Descripción completa

Detalles Bibliográficos
Autores principales: Rahman, Md Hafizur, Mahbub, Khandaker Rayhan, Espinoza-Vergara, Gustavo, Ritchie, Angus, Hoque, M. Mozammel, Noorian, Parisa, Cole, Louise, McDougald, Diane, Labbate, Maurizio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9296650/
https://www.ncbi.nlm.nih.gov/pubmed/35577916
http://dx.doi.org/10.1038/s41396-022-01249-0
_version_ 1784750312399044608
author Rahman, Md Hafizur
Mahbub, Khandaker Rayhan
Espinoza-Vergara, Gustavo
Ritchie, Angus
Hoque, M. Mozammel
Noorian, Parisa
Cole, Louise
McDougald, Diane
Labbate, Maurizio
author_facet Rahman, Md Hafizur
Mahbub, Khandaker Rayhan
Espinoza-Vergara, Gustavo
Ritchie, Angus
Hoque, M. Mozammel
Noorian, Parisa
Cole, Louise
McDougald, Diane
Labbate, Maurizio
author_sort Rahman, Md Hafizur
collection PubMed
description Vibrio cholerae, the bacterial pathogen responsible for the diarrheal disease cholera, resides in the aquatic environment between outbreaks. For bacteria, genetic variation by lateral gene transfer (LGT) is important for survival and adaptation. In the aquatic environment, V. cholerae is predominantly found in biofilms associated with chitinous organisms or with chitin “rain”. Chitin induces competency in V. cholerae, which can lead to LGT. In the environment, V. cholerae is also subjected to predation pressure by protist. Here we investigated whether protozoal predation affected LGT using the integron as a model. Integrons facilitate the integration of mobile DNA (gene cassettes) into the bacterial chromosome. We report that protozoal predation enhances transformation of a gene cassette by as much as 405-fold. We show that oxidative radicals produced in the protozoal phagosome induces the universal SOS response, which in turn upregulates the integron-integrase, the recombinase that facilitates cassette integration. Additionally, we show that during predation, V. cholerae requires the type VI secretion system to acquire the gene cassette from Escherichia coli. These results show that protozoal predation enhances LGT thus producing genetic variants that may have increased capacity to survive grazing. Additionally, the conditions in the food vacuole may make it a “hot spot” for LGT by accumulating diverse bacteria and inducing the SOS response helping drive genetic diversification and evolution.
format Online
Article
Text
id pubmed-9296650
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-92966502022-07-21 Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration Rahman, Md Hafizur Mahbub, Khandaker Rayhan Espinoza-Vergara, Gustavo Ritchie, Angus Hoque, M. Mozammel Noorian, Parisa Cole, Louise McDougald, Diane Labbate, Maurizio ISME J Article Vibrio cholerae, the bacterial pathogen responsible for the diarrheal disease cholera, resides in the aquatic environment between outbreaks. For bacteria, genetic variation by lateral gene transfer (LGT) is important for survival and adaptation. In the aquatic environment, V. cholerae is predominantly found in biofilms associated with chitinous organisms or with chitin “rain”. Chitin induces competency in V. cholerae, which can lead to LGT. In the environment, V. cholerae is also subjected to predation pressure by protist. Here we investigated whether protozoal predation affected LGT using the integron as a model. Integrons facilitate the integration of mobile DNA (gene cassettes) into the bacterial chromosome. We report that protozoal predation enhances transformation of a gene cassette by as much as 405-fold. We show that oxidative radicals produced in the protozoal phagosome induces the universal SOS response, which in turn upregulates the integron-integrase, the recombinase that facilitates cassette integration. Additionally, we show that during predation, V. cholerae requires the type VI secretion system to acquire the gene cassette from Escherichia coli. These results show that protozoal predation enhances LGT thus producing genetic variants that may have increased capacity to survive grazing. Additionally, the conditions in the food vacuole may make it a “hot spot” for LGT by accumulating diverse bacteria and inducing the SOS response helping drive genetic diversification and evolution. Nature Publishing Group UK 2022-05-16 2022-08 /pmc/articles/PMC9296650/ /pubmed/35577916 http://dx.doi.org/10.1038/s41396-022-01249-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Rahman, Md Hafizur
Mahbub, Khandaker Rayhan
Espinoza-Vergara, Gustavo
Ritchie, Angus
Hoque, M. Mozammel
Noorian, Parisa
Cole, Louise
McDougald, Diane
Labbate, Maurizio
Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration
title Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration
title_full Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration
title_fullStr Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration
title_full_unstemmed Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration
title_short Protozoal food vacuoles enhance transformation in Vibrio cholerae through SOS-regulated DNA integration
title_sort protozoal food vacuoles enhance transformation in vibrio cholerae through sos-regulated dna integration
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9296650/
https://www.ncbi.nlm.nih.gov/pubmed/35577916
http://dx.doi.org/10.1038/s41396-022-01249-0
work_keys_str_mv AT rahmanmdhafizur protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT mahbubkhandakerrayhan protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT espinozavergaragustavo protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT ritchieangus protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT hoquemmozammel protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT noorianparisa protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT colelouise protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT mcdougalddiane protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration
AT labbatemaurizio protozoalfoodvacuolesenhancetransformationinvibriocholeraethroughsosregulateddnaintegration