Conjugal plasmid transfer in<i>Streptomyces</i>resembles bacterial chromosome segregation by FtsK/SpoIIIE

Vogelmann, Jutta; Ammelburg, Moritz; Finger, Constanze; Guezguez, Jamil; Linke, Dirk; Flötenmeyer, Matthias; Stierhof, York‐Dieter; Wohlleben, Wolfgang; Muth, Günther

doi:10.1038/emboj.2011.121

Cited by 67 publications

(128 citation statements)

References 49 publications

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“…This is probably mediated by pVAPN_0320, encoding a TraB-like plasmid translocase, also present in pNSL1. TraB translocases are evolutionarily related to the septal FtsK/SpoIIE family proteins involved in chromosome segregation (51) and mediate a novel relaxase/T4SS-independent mechanism of conjugation in Streptomyces linear replicons (53). They all share a similar structural arrangement, with an AAA ϩ motor ATPase domain with characteristic Walker A and B boxes, a transmembrane domain, and a C-terminal DNA-binding winged helix-turn-helix motif (53).…”

Section: Resultsmentioning

confidence: 99%

“…TraB translocases are evolutionarily related to the septal FtsK/SpoIIE family proteins involved in chromosome segregation (51) and mediate a novel relaxase/T4SS-independent mechanism of conjugation in Streptomyces linear replicons (53). They all share a similar structural arrangement, with an AAA ϩ motor ATPase domain with characteristic Walker A and B boxes, a transmembrane domain, and a C-terminal DNA-binding winged helix-turn-helix motif (53). In translocase-mediated conjugation, TraB binds to plasmid dsDNA and forms a transmembrane DNA-conducting hexameric channel through which the plasmid is transferred to the recipient bacterium in an ATP-dependent manner.…”

Section: Resultsmentioning

confidence: 99%

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An Invertron-Like Linear Plasmid Mediates Intracellular Survival and Virulence in Bovine Isolates of Rhodococcus equi

et al. 2015

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dWe report a novel host-associated virulence plasmid in Rhodococcus equi, pVAPN, carried by bovine isolates of this facultative intracellular pathogenic actinomycete. Surprisingly, pVAPN is a 120-kb invertron-like linear replicon unrelated to the circular virulence plasmids associated with equine (pVAPA) and porcine (pVAPB variant) R. equi isolates. pVAPN is similar to the linear plasmid pNSL1 from Rhodococcus sp. NS1 and harbors six new vap multigene family members (vapN to vapS) in a vap pathogenicity locus presumably acquired via en bloc mobilization from a direct predecessor of equine pVAPA. Loss of pVAPN rendered R. equi avirulent in macrophages and mice. Mating experiments using an in vivo transconjugant selection strategy demonstrated that pVAPN transfer is sufficient to confer virulence to a plasmid-cured R. equi recipient. Phylogenetic analyses assigned the vap multigene family complement from pVAPN, pVAPA, and pVAPB to seven monophyletic clades, each containing plasmid type-specific allelic variants of a precursor vap gene carried by the nearest vap island ancestor. Deletion of vapN, the predicted "bovine-type" allelic counterpart of vapA, essential for virulence in pVAPA, abrogated pVAPN-mediated intramacrophage proliferation and virulence in mice. Our findings support a model in which R. equi virulence is conferred by host-adapted plasmids. Their central role is mediating intracellular proliferation in macrophages, promoted by a key vap determinant present in the common ancestor of the plasmid-specific vap islands, with host tropism as a secondary trait selected during coevolution with specific animal species.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

An Invertron-Like Linear Plasmid Mediates Intracellular Survival and Virulence in Bovine Isolates of Rhodococcus equi

et al. 2015

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“…The conjugative machinery used to translocate dsDNA to the recipient cell is structurally much simpler than the T4SS used for transfer of ssDNA. TraB, also known as TraSA or Tra, a single protein subunit resembling the prokaryotic septal DNA translocator protein FtsK, is sufficient for this process (24). Although the molecular aspects of dsDNA transfer have not yet been elucidated for AICEs, the process is thought to be similar to the transfer of the conjugative plasmid pSVH1 of Streptomyces venezuelae (24).…”

Section: General Mechanism Of Disseminationmentioning

confidence: 99%

“…TraB, also known as TraSA or Tra, a single protein subunit resembling the prokaryotic septal DNA translocator protein FtsK, is sufficient for this process (24). Although the molecular aspects of dsDNA transfer have not yet been elucidated for AICEs, the process is thought to be similar to the transfer of the conjugative plasmid pSVH1 of Streptomyces venezuelae (24). A cis-acting locus for transfer (clt) is thought to be recognized and bound by TraB.…”

Section: General Mechanism Of Disseminationmentioning

confidence: 99%

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

Carraro

Burrus

2014

Microbiol Spectr

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Integrative and Conjugative Elements (ICEs) are bacterial mobile genetic elements that play a key role in bacterial genomes dynamics and evolution. ICEs are widely distributed among virtually all bacterial genera. Recent extensive studies have unraveled their high diversity and complexity. The present review depicts the general conserved features of ICEs and describes more precisely three major families of ICEs that have been extensively studied in the past decade for their biology, their evolution and their impact on genomes dynamics. First, the large SXT/R391 family of ICEs disseminates antibiotic resistance genes and drives the exchange of mobilizable genomic islands (MGIs) between many enteric pathogens such as Vibrio cholerae. Second, ICEBs1 of Bacillus subtilis is the most well understood ICE of Gram-positive bacteria, notably regarding the regulation of its dissemination and its initially unforeseen extrachromosomal replication, which could be a common feature of ICEs of both Gram-positive and Gram-negative bacteria. Finally, ICESt1 and ICESt3 of Streptococcus thermophilus are the prototypes of a large family of ICEs widely distributed among various streptococci. These ICEs carry an original regulation module that associates regulators related to those of both SXT/R391 and ICEBs1. Study of ICESt1 and ICESt3 uncovered the cis-mobilization of related genomic islands (CIMEs) by a mechanism called accretion-mobilization, which likely represents a paradigm for the evolution of many ICEs and genomic islands. These three major families of ICEs give a glimpse about ICEs dynamics and their high impact on bacterial adaptation.

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“…In contrast, in M. smegmatis, DNA transfer is mediated by the virulenceassociated locus esx-1 (45). In another example of unconventional conjugation models, Streptomyces conjugative transfer seems to depend exclusively on a single polar protein (17), which resembles the FtsK/SpoIIIE system (46). In the genus Thermus, the presence of a conspicuous conjugative T4SS is restricted to a few strains and species, including T. thermophilus strains SG0.5J (21) and JL-18 (NC_017590).…”

Section: Figmentioning

confidence: 99%

Noncanonical Cell-to-Cell DNA Transfer in Thermus spp. Is Insensitive to Argonaute-Mediated Interference

et al. 2015

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bHorizontal gene transfer drives the rapid evolution of bacterial populations. Classical processes that promote the lateral flow of genetic information are conserved throughout the prokaryotic world. However, some species have nonconserved transfer mechanisms that are not well known. This is the case for the ancient extreme thermophile Thermus thermophilus. In this work, we show that T. thermophilus strains are capable of exchanging large DNA fragments by a novel mechanism that requires cell-tocell contacts and employs components of the natural transformation machinery. This process facilitates the bidirectional transfer of virtually any DNA locus but favors by 10-fold loci found in the megaplasmid over those in the chromosome. In contrast to naked DNA acquisition by transformation, the system does not activate the recently described DNA-DNA interference mechanism mediated by the prokaryotic Argonaute protein, thus allowing the organism to distinguish between DNA transferred from a mate and exogenous DNA acquired from unknown hosts. This Argonaute-mediated discrimination may be tentatively viewed as a strategy for safe sharing of potentially "useful" traits by the components of a given population of Thermus spp. without increasing the genome sizes of its individuals. L ateral gene flow is responsible for the enormous plasticity observed in prokaryotic genomes, which confers on these organisms the ability to adapt rapidly to environmental changes (1-5). Three conserved mechanisms are traditionally associated with lateral gene transfer (LGT) in prokaryotes: phage-mediated transduction, natural transformation, and conjugation. Besides, alternative DNA transfer systems based on nanotubes (6), membrane vesicles, and nanopods in Archaea (7-9), or on the so-called "gene transfer agents" (10), have been described as contributors to genetic exchange among prokaryotes. Among these processes, transformation and conjugation depend only on functions encoded by the bacterial cell. Transformation involves the uptake of naked DNA from the environment and relies entirely on the ability of a competent recipient cell to incorporate DNA. Conjugation, on the other hand, is traditionally seen as the unidirectional transfer of a plasmid DNA molecule from a donor to a recipient cell, where the proteins responsible for DNA transfer are provided exclusively by the donor cell (11).Conjugation differs from transformation not only in the imperative need for a mate for the transfer of DNA but also in the nature of the transferred DNA. While transformation can be envisioned as a mechanism that might have originally evolved in ancestral bacteria, such as Thermus spp., for the acquisition of DNA of any sort and origin as a nutrient, conjugation is more frequently associated with a gain of new capabilities from related species and commonly involves plasmids or megaplasmids that encode all the functions required for conjugation. In fact, transfer of chromosomal genes is apparently less common and in many cases requires the integration of a conjug...

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Conjugal plasmid transfer inStreptomycesresembles bacterial chromosome segregation by FtsK/SpoIIIE

Cited by 67 publications

References 49 publications

An Invertron-Like Linear Plasmid Mediates Intracellular Survival and Virulence in Bovine Isolates of Rhodococcus equi

An Invertron-Like Linear Plasmid Mediates Intracellular Survival and Virulence in Bovine Isolates of Rhodococcus equi

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

Noncanonical Cell-to-Cell DNA Transfer in Thermus spp. Is Insensitive to Argonaute-Mediated Interference

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