Whole-Genome Sequences of 26 Vibrio cholerae Isolates

Watve, Samit S.; Chande, Aroon T.; Rishishwar, Lavanya; Mariño-Ramírez, Leonardo; Jordan, I. King; Hammer, Brian K.

doi:10.1128/genomea.01396-16

Cited by 9 publications

(11 citation statements)

References 16 publications

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“…Average nucleotide identity (ANI) was used to assess the genetic variation for environmental and clinical strains of V. cholerae from this study and for publicly available V. cholerae genomes from NCBI [31]. Strain and assembly information are summarized in Additional file 2: Table S1.…”

Section: Genome Sequencing and Assessment Of Diversity Across Isolatesmentioning

confidence: 99%

Analysis of Vibrio cholerae genomes identifies new type VI secretion system gene clusters

Crisan¹,

Chande²,

Williams³

et al. 2019

Genome Biol

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Background Like many bacteria, Vibrio cholerae deploys a harpoon-like type VI secretion system (T6SS) to compete against other microbes in environmental and host settings. The T6SS punctures adjacent cells and delivers toxic effector proteins that are harmless to bacteria carrying cognate immunity factors. Only four effector/immunity pairs encoded on one large and three auxiliary gene clusters have been characterized from largely clonal, patient-derived strains of V. cholerae . Results We sequence two dozen V. cholerae strain genomes from diverse sources and develop a novel and adaptable bioinformatics tool based on hidden Markov models. We identify two new T6SS auxiliary gene clusters and describe Aux 5 here. Four Aux 5 loci are present in the host strain, each with an atypical effector/immunity gene organization. Structural prediction of the putative effector indicates it is a lipase, which we name TleV1 (type VI lipase effector Vibrio ). Ectopic TleV1 expression induces toxicity in Escherichia coli , which is rescued by co-expression of the TliV1a immunity factor. A clinical V. cholerae reference strain expressing the Aux 5 cluster uses TleV1 to lyse its parental strain upon contact via its T6SS but is unable to kill parental cells expressing the TliV1a immunity factor. Conclusion We develop a novel bioinformatics method and identify new T6SS gene clusters in V. cholerae . We also show the TleV1 toxin is delivered in a T6SS manner by V. cholerae and can lyse other bacterial cells. Our web-based tool can be modified to identify additional novel T6SS genomic loci in diverse bacterial species. Electronic supplementary material The online version of this article (10.1186/s13059-019-1765-5) contains supplementary material, which is available to authorized users.

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Section: Genome Sequencing and Assessment Of Diversity Across Isolatesmentioning

confidence: 99%

Analysis of Vibrio cholerae genomes identifies new type VI secretion system gene clusters

Crisan¹,

Chande²,

Williams³

et al. 2019

Genome Biol

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“…Average nucleotide identity (ANI) was used to assess the genetic variation for environmental and clinical strains of V. cholerae from this study and for publicly available V. cholerae genomes from NCBI (31). Strain and assembly information are summarized in Supplementary Table 1.…”

Section: Genome Sequencing and Assessment Of Diversity Across Isolatesmentioning

confidence: 99%

“…EGT01 is genetically similar to BGT61, 71 and 72 but was collected 33 years later (2011) from grey water (water from non-sewage, home water sources) in Haiti following the 2010 cholera outbreak yet shares many of the same genomic features. EGT01 also encodes two bacterial CRISPR systems absent in the other strains, including one upstream of a T6SS cluster (31).…”

Section: Whole Genome Comparison and Diversity Assessmentmentioning

confidence: 99%

Analysis of Vibrio cholerae genomes using a novel bioinformatic tool identifies new, active Type VI Secretion System gene clusters

Crisan¹,

Chande²,

Williams³

et al. 2019

Preprint

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Background: Like many bacteria, Vibrio cholerae, which causes fatal cholera, deploys a harpoon-like Type VI Secretion System (T6SS) to compete against other microbes in environmental and host settings. The T6SS punctures adjacent cells and delivers toxic effector proteins that are harmless to bacteria carrying cognate immunity factors. Only four effector/immunity pairs encoded on one large and three auxiliary gene clusters have been characterized from largely clonal, patient-derived strains of V. cholerae. Results:We sequenced two dozen V. cholerae strain genomes from diverse sources and developed a novel and adaptable bioinformatic tool based on Hidden Markov Models. We identified two new T6SS auxiliary gene clusters; one, Aux 5, is described here. Four Aux 5 loci are present in the host strain, each with an atypical effector/immunity gene organization. Structural prediction of the putative effector indicated it is a lipase, which we name TleV1 (Type VI lipase effector Vibrio, TleV1). Ectopic TleV1 expression induced toxicity in E. coli, which was rescued by co-expression of the TleV1 immunity factor. A clinical V. cholerae reference strain expressing the Aux 5 cluster used TleV1 to lyse its parental strain upon contact via its T6SS but was unable to kill parental cells expressing TleV1's immunity factor. Conclusion:We developed a novel bioinformatic method and identified new T6SS gene clusters in V. cholerae. We also showed the TleV1 toxin is delivered in a T6SS-manner by V. cholerae and can lyse other bacterial cells. Our web-based tool may be modified to identify additional novel T6SS genomic loci in diverse bacterial species.

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“…One strain is derived from clinical reference isolate C6706 that is induced by chitin to express both the DNA uptake apparatus and the T6SS. The other is recently sequenced environmental isolate 692-79 [20], defective at DNA uptake and yet T6SS-proficient. Here we show that co-culturing of these two strains in the presence of chitin induces unidirectional horizontal transfer of novel T6 effector/immunity pairs to the clinical isolate by homologous recombination.…”

Section: Introductionmentioning

confidence: 99%

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

Thomas

Watve

Ratcliff

et al. 2017

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Horizontal gene transfer (HGT) 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 that Vibrio cholerae can 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. Using spatially explicit modeling, we examine how this process could affect the ecology and evolution of surfaceattached microbial populations. HGT of T6SS effector-immunity pairs is risky: transformation brings a cell into conflict with its former clone mates 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 a hedge against competitors with unpredictable T6SS efficacy. We conclude that antagonism and horizontal transfer drive successive rounds of weapon optimization and selective sweeps, dynamically shaping the composition of microbial communities. IMPORTANCEThe contact-dependent type VI secretion system (T6SS) is frequently used by Proteobacteria to kill adjacent competitors. While DNA released by T6 killing can be horizontally acquired, it remains untested whether T6 genes themselves can be horizontally acquired and then utilized to compete with neighboring cells. Using naturally transformable Vibrio cholerae, we provide the first direct empirical support for the hypothesis that T6 genes are exchanged horizontally (e.g., from dead competitors) and functionally deployed to compete with neighboring cells. Using computational simulations, we also demonstrate that high rates of HGT can be adaptive, allowing V. cholerae to improve upon existing T6 weaponry and survive direct encounters with otherwise superior competitors. We anticipate that our evolutionary results are of broad microbiological relevance, applying to many bacteria capable of HGT that utilize the T6SS or similar antagonistic systems, and highlight the profound impact of HGT in shaping microbial community structure.KEYWORDS type VI secretion, Vibrio cholerae, genetics, horizontal gene transfer, natural transformation systems H orizontal gene transfer (HGT) by plasmid conjugation, viral transduction, and natural transformation plays a fundamental role in the evolution of bacteria and archaea and also in plants and other eukaryotes (1). Genomic analyses implicate HGT as a major factor responsible for the mosaic genomes of many bacteria, including the waterborne microbe Vibrio cholerae, which often carries the cholera toxin (CTX)-encoding prophage responsible for major cholera outbreaks in Haiti and regions of endemicity (2-5...

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Whole-Genome Sequences of 26 Vibrio cholerae Isolates

Cited by 9 publications

References 16 publications

Analysis of Vibrio cholerae genomes identifies new type VI secretion system gene clusters

Analysis of Vibrio cholerae genomes identifies new type VI secretion system gene clusters

Analysis of Vibrio cholerae genomes using a novel bioinformatic tool identifies new, active Type VI Secretion System gene clusters

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

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