Plasmid-like replication of a minimal streptococcal integrative and conjugative element

International audience Integrative and conjugative elements (ICEs) are mobile genetic elements encoding their own excision from a replicon of their bacterial host, transfer by conjugation to a recipient bacterium and reintegration for maintenance. The conjugation, recombination and regulation module...

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Published in:Microbiology
Main Authors: Carraro, Nicolas, Libante, Virginie, Charron-Bourgoin, Florence, Guédon, Gérard, Morel, Catherine, Leblond, Pierre
Other Authors: Dynamique des Génomes et Adaptation Microbienne (DynAMic), Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2016
Subjects:
Online Access:https://hal.univ-lorraine.fr/hal-01476043
https://doi.org/10.1099/mic.0.000219
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spelling ftunilorrainehal:oai:HAL:hal-01476043v1 2023-07-30T04:04:10+02:00 Plasmid-like replication of a minimal streptococcal integrative and conjugative element Carraro, Nicolas Libante, Virginie Charron-Bourgoin, Florence Guédon, Gérard Morel, Catherine Leblond, Pierre Dynamique des Génomes et Adaptation Microbienne (DynAMic) Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL) 2016-04-01 https://hal.univ-lorraine.fr/hal-01476043 https://doi.org/10.1099/mic.0.000219 en eng HAL CCSD Microbiology Society info:eu-repo/semantics/altIdentifier/doi/10.1099/mic.0.000219 info:eu-repo/semantics/altIdentifier/pmid/26825653 hal-01476043 https://hal.univ-lorraine.fr/hal-01476043 doi:10.1099/mic.0.000219 PRODINRA: 346177 PUBMED: 26825653 WOS: 000377847000003 ISSN: 1350-0872 EISSN: 1465-2080 Microbiology https://hal.univ-lorraine.fr/hal-01476043 Microbiology, 2016, 162 (4), pp.622 - 632. ⟨10.1099/mic.0.000219⟩ http://mic.microbiologyresearch.org/content/journal/micro/10.1099/mic.0.000219#tab2 Mobilizable genomic islands Rolling circle replication Horizontal gene-transfer IV secretion Gram-positive bacteria Lactis subsp lactis Cis-mobilization Escherichia-coli Antibiotic-resistance Thermophilus [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2016 ftunilorrainehal https://doi.org/10.1099/mic.0.00021910.1099/mic.0.000219#tab2 2023-07-17T01:31:13Z International audience Integrative and conjugative elements (ICEs) are mobile genetic elements encoding their own excision from a replicon of their bacterial host, transfer by conjugation to a recipient bacterium and reintegration for maintenance. The conjugation, recombination and regulation modules of ICEs of the ICESt3 family are grouped together in a region called the ICE 'core region'. In addition to this core region, elements belonging to this family carry a highly variable region including cargo genes that could be involved in bacterial adaptation or in the maintenance of the element. Although ICEs are a major class of mobile elements through bacterial genomes, the functionality of an element encoding only its excision, transfer, integration and regulation has never been demonstrated experimentally. We engineered MiniICESt3, an artificial ICE derived from ICESt3, devoid of its cargo genes and thus only harbouring the core region. The functionality of this minimal element was assessed. MiniICESt3 was found to be able to excise at a rate of 3.1 %, transfer with a frequency of 1.0 x 10(-5) transconjugants per donor cell and stably maintain by site-specific integration into the 3' end of the fda gene, the same as ICESt3. Furthermore, MiniICESt3 was found in similar to 10 copies per chromosome, this multicopy state likely contributing to its stability for >100 generations even in the absence of selection. Therefore, although ICEs were primarily assumed to only replicate along with the chromosome, our results uncovered extrachromosomal rolling-circle replicating plasmid-like forms of MiniICESt3. Article in Journal/Newspaper ice core Université de Lorraine: HAL Microbiology 162 4 622 632
institution Open Polar
collection Université de Lorraine: HAL
op_collection_id ftunilorrainehal
language English
topic Mobilizable genomic islands
Rolling circle replication
Horizontal gene-transfer
IV secretion
Gram-positive bacteria
Lactis subsp lactis
Cis-mobilization
Escherichia-coli
Antibiotic-resistance
Thermophilus
[SDV]Life Sciences [q-bio]
spellingShingle Mobilizable genomic islands
Rolling circle replication
Horizontal gene-transfer
IV secretion
Gram-positive bacteria
Lactis subsp lactis
Cis-mobilization
Escherichia-coli
Antibiotic-resistance
Thermophilus
[SDV]Life Sciences [q-bio]
Carraro, Nicolas
Libante, Virginie
Charron-Bourgoin, Florence
Guédon, Gérard
Morel, Catherine
Leblond, Pierre
Plasmid-like replication of a minimal streptococcal integrative and conjugative element
topic_facet Mobilizable genomic islands
Rolling circle replication
Horizontal gene-transfer
IV secretion
Gram-positive bacteria
Lactis subsp lactis
Cis-mobilization
Escherichia-coli
Antibiotic-resistance
Thermophilus
[SDV]Life Sciences [q-bio]
description International audience Integrative and conjugative elements (ICEs) are mobile genetic elements encoding their own excision from a replicon of their bacterial host, transfer by conjugation to a recipient bacterium and reintegration for maintenance. The conjugation, recombination and regulation modules of ICEs of the ICESt3 family are grouped together in a region called the ICE 'core region'. In addition to this core region, elements belonging to this family carry a highly variable region including cargo genes that could be involved in bacterial adaptation or in the maintenance of the element. Although ICEs are a major class of mobile elements through bacterial genomes, the functionality of an element encoding only its excision, transfer, integration and regulation has never been demonstrated experimentally. We engineered MiniICESt3, an artificial ICE derived from ICESt3, devoid of its cargo genes and thus only harbouring the core region. The functionality of this minimal element was assessed. MiniICESt3 was found to be able to excise at a rate of 3.1 %, transfer with a frequency of 1.0 x 10(-5) transconjugants per donor cell and stably maintain by site-specific integration into the 3' end of the fda gene, the same as ICESt3. Furthermore, MiniICESt3 was found in similar to 10 copies per chromosome, this multicopy state likely contributing to its stability for >100 generations even in the absence of selection. Therefore, although ICEs were primarily assumed to only replicate along with the chromosome, our results uncovered extrachromosomal rolling-circle replicating plasmid-like forms of MiniICESt3.
author2 Dynamique des Génomes et Adaptation Microbienne (DynAMic)
Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL)
format Article in Journal/Newspaper
author Carraro, Nicolas
Libante, Virginie
Charron-Bourgoin, Florence
Guédon, Gérard
Morel, Catherine
Leblond, Pierre
author_facet Carraro, Nicolas
Libante, Virginie
Charron-Bourgoin, Florence
Guédon, Gérard
Morel, Catherine
Leblond, Pierre
author_sort Carraro, Nicolas
title Plasmid-like replication of a minimal streptococcal integrative and conjugative element
title_short Plasmid-like replication of a minimal streptococcal integrative and conjugative element
title_full Plasmid-like replication of a minimal streptococcal integrative and conjugative element
title_fullStr Plasmid-like replication of a minimal streptococcal integrative and conjugative element
title_full_unstemmed Plasmid-like replication of a minimal streptococcal integrative and conjugative element
title_sort plasmid-like replication of a minimal streptococcal integrative and conjugative element
publisher HAL CCSD
publishDate 2016
url https://hal.univ-lorraine.fr/hal-01476043
https://doi.org/10.1099/mic.0.000219
genre ice core
genre_facet ice core
op_source ISSN: 1350-0872
EISSN: 1465-2080
Microbiology
https://hal.univ-lorraine.fr/hal-01476043
Microbiology, 2016, 162 (4), pp.622 - 632. ⟨10.1099/mic.0.000219⟩
http://mic.microbiologyresearch.org/content/journal/micro/10.1099/mic.0.000219#tab2
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1099/mic.0.000219
info:eu-repo/semantics/altIdentifier/pmid/26825653
hal-01476043
https://hal.univ-lorraine.fr/hal-01476043
doi:10.1099/mic.0.000219
PRODINRA: 346177
PUBMED: 26825653
WOS: 000377847000003
op_doi https://doi.org/10.1099/mic.0.00021910.1099/mic.0.000219#tab2
container_title Microbiology
container_volume 162
container_issue 4
container_start_page 622
op_container_end_page 632
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