The type VI secretion system ofVibrio choleraefosters horizontal gene transfer

Science ◽  
2015 ◽  
Vol 347 (6217) ◽  
pp. 63-67 ◽  
Author(s):  
Sandrine Borgeaud ◽  
Lisa C. Metzger ◽  
Tiziana Scrignari ◽  
Melanie Blokesch
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Live Cell Imaging ◽  
Cell Imaging ◽  
Positive Control ◽  
Secretion System ◽  
Type Vi Secretion System ◽  
Natural Competence ◽  
Type Vi Secretion ◽  
Encoding Gene

Natural competence for transformation is a common mode of horizontal gene transfer and contributes to bacterial evolution. Transformation occurs through the uptake of external DNA and its integration into the genome. Here we show that the type VI secretion system (T6SS), which serves as a predatory killing device, is part of the competence regulon in the naturally transformable pathogenVibrio cholerae. The T6SS-encoding gene cluster is under the positive control of the competence regulators TfoX and QstR and is induced by growth on chitinous surfaces. Live-cell imaging revealed that deliberate killing of nonimmune cells via competence-mediated induction of T6SS releases DNA and makes it accessible for horizontal gene transfer inV. cholerae.

scholarly journals Type VI secretion system: secretion by a contractile nanomachine

2015 ◽  
Vol 370 (1679) ◽  
pp. 20150021 ◽  
Author(s):  
Marek Basler
Keyword(s):  
Live Cell Imaging ◽  
Effector Cell ◽  
Cell Imaging ◽  
Secretion System ◽  
Target Cells ◽  
Gram Negative Bacteria ◽  
Type Vi Secretion System ◽  
Secretion Systems ◽  
Membrane Complex ◽  
Type Vi Secretion

The type VI secretion systems (T6SS) are present in about a quarter of all Gram-negative bacteria. Several key components of T6SS are evolutionarily related to components of contractile nanomachines such as phages and R-type pyocins. The T6SS assembly is initiated by formation of a membrane complex that binds a phage-like baseplate with a sharp spike, and this is followed by polymerization of a long rigid inner tube and an outer contractile sheath. Effectors are preloaded onto the spike or into the tube during the assembly by various mechanisms. Contraction of the sheath releases an unprecedented amount of energy, which is used to thrust the spike and tube with the associated effectors out of the effector cell and across membranes of both bacterial and eukaryotic target cells. Subunits of the contracted sheath are recycled by T6SS-specific unfoldase to allow for a new round of assembly. Live-cell imaging has shown that the assembly is highly dynamic and its subcellular localization is in certain bacteria regulated with a remarkable precision. Through the action of effectors, T6SS has mainly been shown to contribute to pathogenicity and competition between bacteria. This review summarizes the knowledge that has contributed to our current understanding of T6SS mode of action.

scholarly journals Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation

2017 ◽  
Author(s):  
Jacob Thomas ◽  
Samit S. Watve ◽  
William C. Ratcliff ◽  
Brian K. Hammer
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Horizontal Transfer ◽  
Direct Injection ◽  
Spatially Explicit ◽  
Type Vi Secretion System ◽  
Effector Genes ◽  
Type Vi Secretion ◽  
A Cell ◽  
Explicit Simulation

AbstractHorizontal gene transfer can have profound effects on bacterial evolution by allowing individuals to rapidly acquire adaptive traits that shape their strategies for competition. One strategy for intermicrobial antagonism often used by Proteobacteria is the genetically-encoded contact-dependent Type VI secretion system (T6SS); a weapon used to kill heteroclonal neighbors by direct injection of toxic effectors. Here, we experimentally demonstrate thatVibrio choleraecan acquire new T6SS effector genes via horizontal transfer and utilize them to kill neighboring cells. Replacement of one or more parental alleles with novel effectors allows the recombinant strain to dramatically outcompete its parent. Through spatially-explicit simulation modeling, we show that the HGT is risky: transformation brings a cell into conflict with its former clonemates, but can be adaptive when superior T6SS alleles are acquired. More generally, we find that these costs and benefits are not symmetric, and that high rates of HGT can act as hedge against competitors with unpredictable T6SS efficacy. We conclude that antagonism and horizontal transfer drive successive rounds of weapons-optimization and selective sweeps, dynamically shaping the composition of microbial communities.

scholarly journals Neighbor predation linked to natural competence fosters the transfer of large genomic regions in Vibrio cholerae

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Noémie Matthey ◽  
Sandrine Stutzmann ◽  
Candice Stoudmann ◽  
Nicolas Guex ◽  
Christian Iseli ◽  
...  
Keyword(s):  
Vibrio Cholerae ◽  
Genetic Material ◽  
Secretion System ◽  
Degraded Dna ◽  
Dependent Manner ◽  
Type Vi Secretion System ◽  
Natural Competence ◽  
Type Vi Secretion ◽  
Genomic Regions ◽  
Coding Capacity

Natural competence for transformation is a primary mode of horizontal gene transfer. Competent bacteria are able to absorb free DNA from their surroundings and exchange this DNA against pieces of their own genome when sufficiently homologous. However, the prevalence of non-degraded DNA with sufficient coding capacity is not well understood. In this context, we previously showed that naturally competent Vibrio cholerae use their type VI secretion system (T6SS) to actively acquire DNA from non-kin neighbors. Here, we explored the conditions of the DNA released through T6SS-mediated killing versus passive cell lysis and the extent of the transfers that occur due to these conditions. We show that competent V. cholerae acquire DNA fragments with a length exceeding 150 kbp in a T6SS-dependent manner. Collectively, our data support the notion that the environmental lifestyle of V. cholerae fosters the exchange of genetic material with sufficient coding capacity to significantly accelerate bacterial evolution.

scholarly journals Pandemic Vibrio cholerae Acquired Competitive Traits from an Environmental Vibrio Species

2021 ◽  
Author(s):  
Francis J Santoriello ◽  
Paul Kirchberger ◽  
Yann Boucher ◽  
Stefan Pukatzki
Keyword(s):  
Gene Transfer ◽  
Vibrio Cholerae ◽  
Secretion System ◽  
Human Pathogen ◽  
Environmental Niche ◽  
Fish Pathogen ◽  
Type Vi Secretion System ◽  
Type Vi Secretion ◽  
Potential Reservoir ◽  
Environmental Reservoir

Background: Vibrio cholerae, the causative agent of cholera, is a human pathogen that thrives in estuarine environments. V. cholerae competes with neighboring microbes by the contact-dependent translocation of toxic effectors with the type VI secretion system (T6SS). Effector types are highly variable across V. cholerae strains, but all pandemic isolates encode the same set of distinct effectors. It is possible that acquisition of these effectors via horizontal gene transfer played a role in the development of pandemic V. cholerae. Results: We assessed the distribution of V. cholerae T6SS loci across multiple Vibrio species. We showed that the fish-pathogen V. anguillarum encodes all three V. cholerae core loci as well as two of the four additional auxiliary clusters. We further demonstrated that V. anguillarum shares T6SS effectors with V. cholerae, including every pandemic-associated V. cholerae effector. We identified a novel T6SS cluster (Accessory Aux1) that is widespread in V. anguillarum and encodes the pandemic V. cholerae effector TseL. We highlighted potential gene transfer events of Accessory Aux1 from V. anguillarum to V. cholerae. Finally, we showed that TseL from V. cholerae can be neutralized by the V. anguillarum Accessory Aux1 immunity protein and vice versa, indicating V. anguillarum as the donor of tseL to the V. cholerae species. Conclusions: V. anguillarum constitutes an environmental reservoir of pandemic-associated V. cholerae T6SS effectors. V. anguillarum and V. cholerae likely share an environmental niche, compete, and exchange T6SS effectors. Further, our findings highlight the fish as a potential reservoir of pandemic V. cholerae.

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