Distributive Conjugal Transfer in Mycobacteria Generates Progeny with Meiotic-Like Genome-Wide Mosaicism, Allowing Mapping of a Mating Identity Locus

Gray, Todd A.; Krywy, Janet A.; Harold, Jessica; Palumbo, Michael J.; Derbyshire, Keith M.

doi:10.1371/journal.pbio.1001602

Cited by 87 publications

(113 citation statements)

References 42 publications

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“…S2). Overall, our results with M. smegmatis strains mc 2 155 and mc 2 874 confirm previous observations (16), but also suggest putative alternative mechanisms of plasmid transfer. Importantly, the results validated the used fluorescence/antibiotic markers in the experimental setup for use in HGT experiments on M. canettii and MTBC strains.…”

Section: Resultssupporting

confidence: 91%

“…DCT was originally described as a mechanism of DNA transfer between M. smegmatis donor and recipient trains that generated genome-wide mosaicism in the transconjugants (16). For the initial setup of our experimental mating assay, we thus rendered M. smegmatis strains mc 2 155 (NC_008596), known to be an efficient donor (16), GFP fluorescent, and hygromycin resistant (Hyg r ) by using the pYUB412-derived integrating cosmid F10 (19,20). In parallel, red colonies of strain mc 2 874 (NZ_AOCJ01000000), known to be a good recipient (16), were obtained by transformation with a replicative, nonmobilizable plasmid, carrying a kanamycin resistance (Km r ) cassette and a gene encoding DsRed.…”

Section: Resultsmentioning

confidence: 99%

“…For the initial setup of our experimental mating assay, we thus rendered M. smegmatis strains mc 2 155 (NC_008596), known to be an efficient donor (16), GFP fluorescent, and hygromycin resistant (Hyg r ) by using the pYUB412-derived integrating cosmid F10 (19,20). In parallel, red colonies of strain mc 2 874 (NZ_AOCJ01000000), known to be a good recipient (16), were obtained by transformation with a replicative, nonmobilizable plasmid, carrying a kanamycin resistance (Km r ) cassette and a gene encoding DsRed. After incubation on filter plates as previously described (12), potential recombinants were identified on Km/Hyg agar plates by using orange colony appearance as selection criterion.…”

Section: Resultsmentioning

confidence: 99%

“…M. smegmatis transconjugants typically display highly mosaic genomes reminiscent of products of eukaryotic meiosis, composed of multiple donor-derived sequence segments that are distributed without apparent regional bias across the genome. Consequently, this type of HGT was termed distributive conjugal transfer (DCT) (16). Detection of mosaic sequence arrangements in M. canettii genomes (10,11,17,18) raised the issue whether similar molecular mechanisms might be active in tuberculosis-causing mycobacteria and/or in mycobacteria, in general.…”

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confidence: 99%

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Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria

Boritsch

Khanna

Pawlik

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Horizontal gene transfer (HGT) is a major driving force of bacterial diversification and evolution. For tuberculosis-causing mycobacteria, the impact of HGT in the emergence and distribution of dominant lineages remains a matter of debate. Here, by using fluorescenceassisted mating assays and whole genome sequencing, we present unique experimental evidence of chromosomal DNA transfer between tubercle bacilli of the early-branching Mycobacterium canettii clade. We found that the obtained recombinants had received multiple donor-derived DNA fragments in the size range of 100 bp to 118 kbp, fragments large enough to contain whole operons. Although the transfer frequency between M. canettii strains was low and no transfer could be observed among classical Mycobacterium tuberculosis complex (MTBC) strains, our study provides the proof of concept for genetic exchange in tubercle bacilli. This outstanding, now experimentally validated phenomenon presumably played a key role in the early evolution of the MTBC toward pathogenicity. Moreover, our findings also provide important information for the risk evaluation of potential transfer of drug resistance and fitness mutations among clinically relevant mycobacterial strains.recombination | DNA transfer | tuberculosis | Mycobacterium canettii | evolution

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Section: Resultssupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria

Boritsch

Khanna

Pawlik

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…ESX-1 allows cytosolic contact and mediates vacuoles rupture [47]; the protein intervenes in host cell lysis in a contact dependent way, producing gross membrane disruptions [48]. DNA transfer through conjugation is also a function of ESX-1 system [49]; a phenomenon called "distributive conjugal transfer" that describes a genetic exchange between recipient and donor is dependent of ESX-1 in M. smegmatis [50]. espB gene located in the RD1 region has been related with cytotoxicity and their presence in the surface of apoptotic cells for clearance by macrophages through efferocytosis [51].…”

Section: Esx-1mentioning

confidence: 99%

Virulence Factors and Pathogenicity of Mycobacterium

Echeverría-Valencia¹,

Flores-Villalva²,

Espitia³

2018

Mycobacterium - Research and Development

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Virulence, is referred as the ability of a pathogen to cause disease, and for mycobacteria it depends on their ability to reside within host cells and evade the microbicidal mechanisms of macrophages. The outcome of tuberculosis (TB) infection is highly variable and it seems that the closest relationship between the Mycobacterium genre and humans has shaped the mycobacterial genome to encode bacterial factors that reflects a highly evolved and coordinated program of immune evasion strategies that interfere with both innate and adaptive immunity causing disease even in fully immunocompetent host. Although Mycobacterium tuberculosis (MTB) does not have classical virulence factors, it has described many virulence-associated genes and virulence lifestyle genes from Mycobacterium tuberculosis complex (MTBC). In this chapter, we describe the most important gene/molecule involved in the host defense modulation response, also the plethora of strategies to evade immune mechanisms of macrophage. We review the main genes whose inactivation in the mycobacterial genome leads to a measurable loss in virulence in the different validated TB models.

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Type VII Secretion Systems in Gram-Positive Bacteria

Bottai

Gröschel

Brosch

2015

Current Topics in Microbiology and Immunology

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Bacterial secretion systems are sophisticated molecular machines that fulfil a wide range of important functions, which reach from export/secretion of essential proteins or virulence factors to the implication in conjugation processes. In contrast to the widely distributed Sec and Twin Arginine Translocation (TAT) systems, the recently identified ESX/type VII systems show a more restricted distribution and are typical for mycobacteria and other high-GC Actinobacteria. Similarly, type VII-like secretion systems have been described in low-GC Gram-positive bacteria belonging to the phylum Firmicutes. While the most complex organization of type VII secretion systems currently known is found in slow-growing mycobacteria, which harbour up to 5 chromosomal-encoded systems (ESX-1 to ESX-5), much simpler organization is reported for type VII-like systems in Firmicutes. In this chapter, we describe common and divergent features of type VII- and type VII-like secretion pathways and also comment on their biological key roles, many of which are related to species-/genus-specific host-pathogen interactions and/or virulence mechanisms.

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Distributive Conjugal Transfer in Mycobacteria Generates Progeny with Meiotic-Like Genome-Wide Mosaicism, Allowing Mapping of a Mating Identity Locus

Abstract: We find that genome-wide DNA transfer by conjugation in mycobacteria affords bacteria that reproduce by binary fission the same advantages of sexual reproduction, and may explain the genomic evolution of Mycobacterium tuberculosis.

Cited by 87 publications

References 42 publications

Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria

Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria

Virulence Factors and Pathogenicity of Mycobacterium

Type VII Secretion Systems in Gram-Positive Bacteria

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