Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.

Horizontal gene transfer greatly facilitates rapid genetic adaptation of bacteria to shifts in environmental conditions and colonization of new niches by allowing one-step acquisition of novel functions. Conjugation is a major mechanism of horizontal gene transfer mediated by conjugative plasmids an...

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Autores principales: Mariana Gabriela Ghinet, Eric Bordeleau, Julie Beaudin, Ryszard Brzezinski, Sébastien Roy, Vincent Burrus
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spelling oai:doaj.org-article:383f342dd220447bb2fef22f0024d00a2021-11-18T07:34:03ZUncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.1932-620310.1371/journal.pone.0027846https://doaj.org/article/383f342dd220447bb2fef22f0024d00a2011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22114709/?tool=EBIhttps://doaj.org/toc/1932-6203Horizontal gene transfer greatly facilitates rapid genetic adaptation of bacteria to shifts in environmental conditions and colonization of new niches by allowing one-step acquisition of novel functions. Conjugation is a major mechanism of horizontal gene transfer mediated by conjugative plasmids and integrating conjugative elements (ICEs). While in most bacterial conjugative systems DNA translocation requires the assembly of a complex type IV secretion system (T4SS), in Actinobacteria a single DNA FtsK/SpoIIIE-like translocation protein is required. To date, the role and diversity of ICEs in Actinobacteria have received little attention. Putative ICEs were searched for in 275 genomes of Actinobacteria using HMM-profiles of proteins involved in ICE maintenance and transfer. These exhaustive analyses revealed 144 putative FtsK/SpoIIIE-type ICEs and 17 putative T4SS-type ICEs. Grouping of the ICEs based on the phylogenetic analyses of maintenance and transfer proteins revealed extensive exchanges between different sub-families of ICEs. 17 ICEs were found in Actinobacteria from the genus Frankia, globally important nitrogen-fixing microorganisms that establish root nodule symbioses with actinorhizal plants. Structural analysis of ICEs from Frankia revealed their unexpected diversity and a vast array of predicted adaptive functions. Frankia ICEs were found to excise by site-specific recombination from their host's chromosome in vitro and in planta suggesting that they are functional mobile elements whether Frankiae live as soil saprophytes or plant endosymbionts. Phylogenetic analyses of proteins involved in ICEs maintenance and transfer suggests that active exchange between ICEs cargo-borne and chromosomal genes took place within the Actinomycetales order. Functionality of Frankia ICEs in vitro as well as in planta lets us anticipate that conjugation and ICEs could allow the development of genetic manipulation tools for this challenging microorganism and for many other Actinobacteria.Mariana Gabriela GhinetEric BordeleauJulie BeaudinRyszard BrzezinskiSébastien RoyVincent BurrusPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 11, p e27846 (2011)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Mariana Gabriela Ghinet
Eric Bordeleau
Julie Beaudin
Ryszard Brzezinski
Sébastien Roy
Vincent Burrus
Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.
description Horizontal gene transfer greatly facilitates rapid genetic adaptation of bacteria to shifts in environmental conditions and colonization of new niches by allowing one-step acquisition of novel functions. Conjugation is a major mechanism of horizontal gene transfer mediated by conjugative plasmids and integrating conjugative elements (ICEs). While in most bacterial conjugative systems DNA translocation requires the assembly of a complex type IV secretion system (T4SS), in Actinobacteria a single DNA FtsK/SpoIIIE-like translocation protein is required. To date, the role and diversity of ICEs in Actinobacteria have received little attention. Putative ICEs were searched for in 275 genomes of Actinobacteria using HMM-profiles of proteins involved in ICE maintenance and transfer. These exhaustive analyses revealed 144 putative FtsK/SpoIIIE-type ICEs and 17 putative T4SS-type ICEs. Grouping of the ICEs based on the phylogenetic analyses of maintenance and transfer proteins revealed extensive exchanges between different sub-families of ICEs. 17 ICEs were found in Actinobacteria from the genus Frankia, globally important nitrogen-fixing microorganisms that establish root nodule symbioses with actinorhizal plants. Structural analysis of ICEs from Frankia revealed their unexpected diversity and a vast array of predicted adaptive functions. Frankia ICEs were found to excise by site-specific recombination from their host's chromosome in vitro and in planta suggesting that they are functional mobile elements whether Frankiae live as soil saprophytes or plant endosymbionts. Phylogenetic analyses of proteins involved in ICEs maintenance and transfer suggests that active exchange between ICEs cargo-borne and chromosomal genes took place within the Actinomycetales order. Functionality of Frankia ICEs in vitro as well as in planta lets us anticipate that conjugation and ICEs could allow the development of genetic manipulation tools for this challenging microorganism and for many other Actinobacteria.
format article
author Mariana Gabriela Ghinet
Eric Bordeleau
Julie Beaudin
Ryszard Brzezinski
Sébastien Roy
Vincent Burrus
author_facet Mariana Gabriela Ghinet
Eric Bordeleau
Julie Beaudin
Ryszard Brzezinski
Sébastien Roy
Vincent Burrus
author_sort Mariana Gabriela Ghinet
title Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.
title_short Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.
title_full Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.
title_fullStr Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.
title_full_unstemmed Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.
title_sort uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/383f342dd220447bb2fef22f0024d00a
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AT ericbordeleau uncoveringtheprevalenceanddiversityofintegratingconjugativeelementsinactinobacteria
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AT ryszardbrzezinski uncoveringtheprevalenceanddiversityofintegratingconjugativeelementsinactinobacteria
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