Identification of a Novel Conjugative Plasmid in Mycobacteria That Requires Both Type IV and Type VII Secretion

Handle URI:
http://hdl.handle.net/10754/334952
Title:
Identification of a Novel Conjugative Plasmid in Mycobacteria That Requires Both Type IV and Type VII Secretion
Authors:
Ummels, R.; Abdallah, A. M.; Kuiper, V.; Aajoud, A.; Sparrius, M.; Naeem, R.; Spaink, H. P.; van Soolingen, D.; Pain, Arnab ( 0000-0002-1755-2819 ) ; Bitter, W.
Abstract:
Conjugative plasmids have been identified in a wide variety of different bacteria, ranging from proteobacteria to firmicutes, and conjugation is one of the most efficient routes for horizontal gene transfer. The most widespread mechanism of plasmid conjugation relies on different variants of the type IV secretion pathway. Here, we describe the identification of a novel type of conjugative plasmid that seems to be unique for mycobacteria. Interestingly, while this plasmid is efficiently exchanged between different species of slow-growing mycobacteria, including Mycobacterium tuberculosis, it could not be transferred to any of the fast-growing mycobacteria tested. Genetic analysis of the conjugative plasmid showed the presence of a locus containing homologues of three type IV secretion system components and a relaxase. In addition, a new type VII secretion locus was present. Using transposon insertion mutagenesis, we show that in fact both these secretion systems are essential for conjugation, indicating that this plasmid represents a new class of conjugative plasmids requiring two secretion machineries. This plasmid could form a useful new tool to exchange or introduce DNA in slow-growing mycobacteria. IMPORTANCE: Conjugative plasmids play an important role in horizontal gene transfer between different bacteria and, as such, in their adaptation and evolution. This effect is most obvious in the spread of antibiotic resistance genes. Thus far, conjugation of natural plasmids has been described only rarely for mycobacterial species. In fact, it is generally accepted that M. tuberculosis does not show any recent sign of horizontal gene transfer. In this study, we describe the identification of a new widespread conjugative plasmid that can also be efficiently transferred to M. tuberculosis. This plasmid therefore poses both a threat and an opportunity. The threat is that, through the acquisition of antibiotic resistance markers, this plasmid could start a rapid spread of antibiotic resistance genes between pathogenic mycobacteria. The opportunity is that we could use this plasmid to generate new tools for the efficient introduction of foreign DNA in slow-growing mycobacteria.
KAUST Department:
Pathogen Genomics Laboratory; Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
Ummels R, Abdallah AM, Kuiper V, Aâjoud A, Sparrius M, Naeem R, Spaink HP, van Soolingen D, Pain A, Bitter W. 2014. Identification of a novel conjugative plasmid in mycobacteria that requires both type IV and type VII secretion. mBio 5(5):e01744-14. doi:10.1128/mBio.01744-14.
Publisher:
American Society for Microbiology
Journal:
mBio
Issue Date:
23-Sep-2014
DOI:
10.1128/mBio.01744-14
PubMed ID:
25249284
PubMed Central ID:
PMC4173767
Type:
Article
ISSN:
2150-7511
Additional Links:
http://mbio.asm.org/cgi/doi/10.1128/mBio.01744-14
Appears in Collections:
Articles; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorUmmels, R.en
dc.contributor.authorAbdallah, A. M.en
dc.contributor.authorKuiper, V.en
dc.contributor.authorAajoud, A.en
dc.contributor.authorSparrius, M.en
dc.contributor.authorNaeem, R.en
dc.contributor.authorSpaink, H. P.en
dc.contributor.authorvan Soolingen, D.en
dc.contributor.authorPain, Arnaben
dc.contributor.authorBitter, W.en
dc.date.accessioned2014-11-16T12:15:00Z-
dc.date.available2014-11-16T12:15:00Z-
dc.date.issued2014-09-23en
dc.identifier.citationUmmels R, Abdallah AM, Kuiper V, Aâjoud A, Sparrius M, Naeem R, Spaink HP, van Soolingen D, Pain A, Bitter W. 2014. Identification of a novel conjugative plasmid in mycobacteria that requires both type IV and type VII secretion. mBio 5(5):e01744-14. doi:10.1128/mBio.01744-14.en
dc.identifier.issn2150-7511en
dc.identifier.pmid25249284en
dc.identifier.doi10.1128/mBio.01744-14en
dc.identifier.urihttp://hdl.handle.net/10754/334952en
dc.description.abstractConjugative plasmids have been identified in a wide variety of different bacteria, ranging from proteobacteria to firmicutes, and conjugation is one of the most efficient routes for horizontal gene transfer. The most widespread mechanism of plasmid conjugation relies on different variants of the type IV secretion pathway. Here, we describe the identification of a novel type of conjugative plasmid that seems to be unique for mycobacteria. Interestingly, while this plasmid is efficiently exchanged between different species of slow-growing mycobacteria, including Mycobacterium tuberculosis, it could not be transferred to any of the fast-growing mycobacteria tested. Genetic analysis of the conjugative plasmid showed the presence of a locus containing homologues of three type IV secretion system components and a relaxase. In addition, a new type VII secretion locus was present. Using transposon insertion mutagenesis, we show that in fact both these secretion systems are essential for conjugation, indicating that this plasmid represents a new class of conjugative plasmids requiring two secretion machineries. This plasmid could form a useful new tool to exchange or introduce DNA in slow-growing mycobacteria. IMPORTANCE: Conjugative plasmids play an important role in horizontal gene transfer between different bacteria and, as such, in their adaptation and evolution. This effect is most obvious in the spread of antibiotic resistance genes. Thus far, conjugation of natural plasmids has been described only rarely for mycobacterial species. In fact, it is generally accepted that M. tuberculosis does not show any recent sign of horizontal gene transfer. In this study, we describe the identification of a new widespread conjugative plasmid that can also be efficiently transferred to M. tuberculosis. This plasmid therefore poses both a threat and an opportunity. The threat is that, through the acquisition of antibiotic resistance markers, this plasmid could start a rapid spread of antibiotic resistance genes between pathogenic mycobacteria. The opportunity is that we could use this plasmid to generate new tools for the efficient introduction of foreign DNA in slow-growing mycobacteria.en
dc.language.isoenen
dc.publisherAmerican Society for Microbiologyen
dc.relation.urlhttp://mbio.asm.org/cgi/doi/10.1128/mBio.01744-14en
dc.rightshttp://creativecommons.org/licenses/by-nc-sa/3.0/en
dc.rights.urihttp://creativecommons.org/licenses/by-nc-sa/3.0/en
dc.titleIdentification of a Novel Conjugative Plasmid in Mycobacteria That Requires Both Type IV and Type VII Secretionen
dc.typeArticleen
dc.contributor.departmentPathogen Genomics Laboratoryen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalmBioen
dc.identifier.pmcidPMC4173767en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionDepartment of Medical Microbiology and Infection Control, VU University Medical Center, Amsterdam, The Netherlandsen
dc.contributor.institutionInstitute of Biology, Leiden University, Leiden, Amsterdam, The Netherlandsen
dc.contributor.institutionNational Mycobacteria Reference Laboratory, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlandsen
dc.contributor.institutionSection Molecular Microbiology, VU University Amsterdam, Amsterdam, The Netherlandsen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorNaeem, Raeeceen
kaust.authorPain, Arnaben
kaust.authorAbdallah, Abdallahen

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