The specialized secretory apparatus ESX‐1 is essential for DNA transfer in Mycobacterium smegmatis

Coros, Abbie; Callahan, Brian; Battaglioli, Eric; Derbyshire, Keith M.

doi:10.1111/j.1365-2958.2008.06299.x

Cited by 137Tuberculosis Research and EpidemiologyBacterial Genetics and BiotechnologyMycobacterium research and diagnosis

The specialized secretory apparatus ESX‐1 is essential for DNA transfer in Mycobacterium smegmatis

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Coros, Abbie, Callahan, Brian, Battaglioli, Eric, Derbyshire, Keith M.·2008·Molecular Microbiology

DOI 10.1111/j.1365-2958.2008.06299.xPMC PMC2562793

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Abstract

Summary: Conjugal DNA transfer in Mycobacterium smegmatis occurs by a mechanism distinct from plasmid‐mediated DNA transfer. Previously, we had shown that the secretory apparatus, ESX‐1, negatively regulated DNA transfer from the donor strain; ESX‐1 donor mutants are hyper‐conjugative. Here, we describe a genome‐wide transposon mutagenesis screen to isolate recipient mutants. Surprisingly, we find that a majority of insertions map within the esx‐1 locus, which encodes the secretory apparatus. Thus, in contrast to its role in donor function, ESX‐1 is essential for recipient function; recipient ESX‐1 mutants are hypo‐conjugative. In addition to esx‐1 genes, our screen identifies novel non‐esx‐1 loci in the M. smegmatis genome that are required for both DNA transfer and ESX‐1 activity. DNA transfer therefore provides a simple molecular genetic assay to characterize ESX‐1, which, in Mycobacterium tuberculosis, is necessary for full virulence. These findings reinforce the functional intertwining of DNA transfer and ESX‐1 secretion, first described in the M. smegmatis donor. Moreover, our observation that ESX‐1 has such diametrically opposed effects on transfer in the donor and recipient, forces us to consider how proteins secreted by the ESX‐1 apparatus can function so as to modulate two seemingly disparate processes, M. smegmatis DNA transfer and M. tuberculosis virulence.

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The ESX-1 system is required for distributive conjugal transfer (DCT) of chromosomal DNA from donor into recipient strains of M. smegmatis.
“For example, the ESX-1 system, which is present in fast-and slow-growing mycobacterial species, is required for distributive conjugal transfer (DCT) of chromosomal DNA from donor into recipient strains of M. smegmatis (51,52).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [51]

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Authors: Coros, A., Callahan, B., Battaglioli, E., & Derbyshire, K. M.
Affiliations: New York State Department of Health (US)
Corresponding author: Derbyshire, Keith M.
ORCID: Callahan, Brian
Battaglioli, Eric
Derbyshire, Keith M.
Venue: Molecular Microbiology
Publisher: Wiley
Published: 2008-07-23
Volume: 69
Issue: 4
Pages: 794-808
ISSN: 0950-382X (ISSN-L)
1365-2958
DOI: 10.1111/j.1365-2958.2008.06299.x
PMC: PMC2562793
OpenAlex: W2155383369
Cited by: 137
References: 52
Citations by year: 2026: 1 · 2025: 2 · 2024: 4 · 2023: 5 · 2022: 5 · 2021: 8 · 2020: 10 · 2019: 11 · 2018: 5 · 2017: 7 · 2016: 16 · 2015: 7 · 2014: 14 · 2013: 13 · 2012: 11
FWCI: 3.86
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Molecular Microbiology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Centers for Disease Control and Prevention
National Institute of General Medical Sciences (GM-27099)
National Institute of Allergy and Infectious Diseases (T32AI055429, R21AI070666, R01AI042308)
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
Keywords: ESX-1, Mycobacterium smegmatis, conjugation, transposon mutagenesis screen, plasmid transfer
MeSH terms: Bacterial Proteins, Base Sequence, Biological Transport, Conjugation, Genetic, DNA, Genes, Bacterial, Operon, Mutagenesis, Insertional, Mycobacterium smegmatis

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The specialized secretory apparatus ESX‐1 is essential for DNA transfer in Mycobacterium smegmatis

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