Cited by 75Tuberculosis Research and EpidemiologyBacterial Genetics and BiotechnologyGenomics and Phylogenetic Studies

Distributive Conjugal Transfer: New Insights into Horizontal Gene Transfer and Genetic Exchange in Mycobacteria

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Derbyshire, Keith M., Gray, Todd A.·2014·Microbiology Spectrum

Abstract

The past decade has seen an explosion in the application of genomic tools across all biological disciplines. This is also true for mycobacteria, where whole-genome sequences are now available for pathogens and nonpathogens alike. Genomes within the Mycobacterium tuberculosis complex (MTBC) bear the hallmarks of horizontal gene transfer (HGT). Conjugation is the form of HGT with the highest potential capacity and evolutionary influence. Donor and recipient strains of Mycobacterium smegmatis actively conjugate upon coculturing in biofilms and on solid media. Whole-genome sequencing of the transconjugant progeny demonstrated the incredible scale and range of genomic variation that conjugation generates. Transconjugant genomes are complex mosaics of the parental strains. Some transconjugant genomes are up to one-quarter donor-derived, distributed over 30 segments. Transferred segments range from ∼50 bp to ∼225,000 bp in length and are exchanged with their recipient orthologs all around the genome. This unpredictable genome-wide infusion of DNA sequences is called distributive conjugal transfer (DCT), to distinguish it from traditional oriT -based conjugation. The mosaicism generated in a single transfer event resembles that seen from meiotic recombination in sexually reproducing organisms and contrasts with traditional models of HGT. This similarity allowed the application of a genome-wide association study approach to map the donor genes that confer a donor mating identity phenotype. The mating identity genes map to the esx1 locus, expanding the central role of ESX-1 function in conjugation. The potential for DCT to instantaneously blend genomes will affect how we view mycobacterial evolution and provide new tools for the facile manipulation of mycobacterial genomes.

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  • Comparative analysis of multiple genome sequences of Mycobacterium canettii revealed thousands of SNPs, and the striking similarity to experimentally produced mosaic genomes of M. smegmatis provided the first indication that HGT had occurred in the MTBC.

    “That concept was challenged when the comparative analysis of multiple genome sequences of Mycobacterium canettii (a smooth colony outlier of the MTBC) revealed thousands of SNPs: the striking similarity to the experimentally produced mosaic genomes of M. smegmatis provided the first indication that HGT had occurred in the MTBC (48–51).”

    From Mycobacterium smegmatis: The Vanguard of Mycobacterial Research (2023) · cites this paper as [51]

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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).”

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  1. [27]Crawford JT Falkinham JO McFadden J Plasmids of the Mycobacterium avium complex Molecular Biology of the Mycobacteria 1990 San Diego Academic Press Inc. 97 120

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Authors
Derbyshire, K. M., & Gray, T. A.
Affiliations
New York State Department of Health (US)
Venue
Microbiology Spectrum
Published
2014-01-17
Volume
2
Issue
1
Pages
MGM2-0022
ISSN
2165-0497 (ISSN-L)
OpenAlex
W2064043452
Cited by
75
References
72
Citations by year
2026: 2 · 2025: 4 · 2024: 3 · 2023: 8 · 2022: 6 · 2021: 3 · 2020: 9 · 2019: 15 · 2018: 8 · 2017: 11 · 2016: 6
FWCI
3.98
Type
journal article
Language
en
Open access
Locations
  • Microbiology Spectrum (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Allergy and Infectious Diseases (R56AI080694, R01AI042308)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
horizontal gene transfer, Mycobacterium smegmatis, Mycobacterium tuberculosis complex, conjugation, genome mosaicism, ESX-1

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