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Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins
Horizontal gene transfer is a major driver of bacterial evolution and adaptation to environmental stresses, occurring notably via transformation of naturally competent organisms. The Deinococcus radiodurans bacterium, characterized by its extreme radioresistance, is also naturally competent. Here, w...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7314969/ https://www.ncbi.nlm.nih.gov/pubmed/32625182 http://dx.doi.org/10.3389/fmicb.2020.01253 |
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author | Ithurbide, Solenne Coste, Geneviève Lisboa, Johnny Eugénie, Nicolas Bentchikou, Esma Bouthier de la Tour, Claire Liger, Dominique Confalonieri, Fabrice Sommer, Suzanne Quevillon-Cheruel, Sophie Servant, Pascale |
author_facet | Ithurbide, Solenne Coste, Geneviève Lisboa, Johnny Eugénie, Nicolas Bentchikou, Esma Bouthier de la Tour, Claire Liger, Dominique Confalonieri, Fabrice Sommer, Suzanne Quevillon-Cheruel, Sophie Servant, Pascale |
author_sort | Ithurbide, Solenne |
collection | PubMed |
description | Horizontal gene transfer is a major driver of bacterial evolution and adaptation to environmental stresses, occurring notably via transformation of naturally competent organisms. The Deinococcus radiodurans bacterium, characterized by its extreme radioresistance, is also naturally competent. Here, we investigated the role of D. radiodurans players involved in different steps of natural transformation. First, we identified the factors (PilQ, PilD, type IV pilins, PilB, PilT, ComEC-ComEA, and ComF) involved in DNA uptake and DNA translocation across the external and cytoplasmic membranes and showed that the DNA-uptake machinery is similar to that described in the Gram negative bacterium Vibrio cholerae. Then, we studied the involvement of recombination and DNA repair proteins, RecA, RecF, RecO, DprA, and DdrB into the DNA processing steps of D. radiodurans transformation by plasmid and genomic DNA. The transformation frequency of the cells devoid of DprA, a highly conserved protein among competent species, strongly decreased but was not completely abolished whereas it was completely abolished in ΔdprA ΔrecF, ΔdprA ΔrecO, and ΔdprA ΔddrB double mutants. We propose that RecF and RecO, belonging to the recombination mediator complex, and DdrB, a specific deinococcal DNA binding protein, can replace a function played by DprA, or alternatively, act at a different step of recombination with DprA. We also demonstrated that a ΔdprA mutant is as resistant as wild type to various doses of γ-irradiation, suggesting that DprA, and potentially transformation, do not play a major role in D. radiodurans radioresistance. |
format | Online Article Text |
id | pubmed-7314969 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-73149692020-07-02 Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins Ithurbide, Solenne Coste, Geneviève Lisboa, Johnny Eugénie, Nicolas Bentchikou, Esma Bouthier de la Tour, Claire Liger, Dominique Confalonieri, Fabrice Sommer, Suzanne Quevillon-Cheruel, Sophie Servant, Pascale Front Microbiol Microbiology Horizontal gene transfer is a major driver of bacterial evolution and adaptation to environmental stresses, occurring notably via transformation of naturally competent organisms. The Deinococcus radiodurans bacterium, characterized by its extreme radioresistance, is also naturally competent. Here, we investigated the role of D. radiodurans players involved in different steps of natural transformation. First, we identified the factors (PilQ, PilD, type IV pilins, PilB, PilT, ComEC-ComEA, and ComF) involved in DNA uptake and DNA translocation across the external and cytoplasmic membranes and showed that the DNA-uptake machinery is similar to that described in the Gram negative bacterium Vibrio cholerae. Then, we studied the involvement of recombination and DNA repair proteins, RecA, RecF, RecO, DprA, and DdrB into the DNA processing steps of D. radiodurans transformation by plasmid and genomic DNA. The transformation frequency of the cells devoid of DprA, a highly conserved protein among competent species, strongly decreased but was not completely abolished whereas it was completely abolished in ΔdprA ΔrecF, ΔdprA ΔrecO, and ΔdprA ΔddrB double mutants. We propose that RecF and RecO, belonging to the recombination mediator complex, and DdrB, a specific deinococcal DNA binding protein, can replace a function played by DprA, or alternatively, act at a different step of recombination with DprA. We also demonstrated that a ΔdprA mutant is as resistant as wild type to various doses of γ-irradiation, suggesting that DprA, and potentially transformation, do not play a major role in D. radiodurans radioresistance. Frontiers Media S.A. 2020-06-18 /pmc/articles/PMC7314969/ /pubmed/32625182 http://dx.doi.org/10.3389/fmicb.2020.01253 Text en Copyright © 2020 Ithurbide, Coste, Lisboa, Eugénie, Bentchikou, Bouthier de la Tour, Liger, Confalonieri, Sommer, Quevillon-Cheruel and Servant. http://creativecommons.org/licenses/by/4.0/ 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. |
spellingShingle | Microbiology Ithurbide, Solenne Coste, Geneviève Lisboa, Johnny Eugénie, Nicolas Bentchikou, Esma Bouthier de la Tour, Claire Liger, Dominique Confalonieri, Fabrice Sommer, Suzanne Quevillon-Cheruel, Sophie Servant, Pascale Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins |
title | Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins |
title_full | Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins |
title_fullStr | Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins |
title_full_unstemmed | Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins |
title_short | Natural Transformation in Deinococcus radiodurans: A Genetic Analysis Reveals the Major Roles of DprA, DdrB, RecA, RecF, and RecO Proteins |
title_sort | natural transformation in deinococcus radiodurans: a genetic analysis reveals the major roles of dpra, ddrb, reca, recf, and reco proteins |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7314969/ https://www.ncbi.nlm.nih.gov/pubmed/32625182 http://dx.doi.org/10.3389/fmicb.2020.01253 |
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