Literature DB >> 26240317

A globally distributed mobile genetic element inhibits natural transformation of Vibrio cholerae.

Ankur B Dalia1, Kimberley D Seed2, Stephen B Calderwood3, Andrew Camilli4.   

Abstract

Natural transformation is one mechanism of horizontal gene transfer (HGT) in Vibrio cholerae, the causative agent of cholera. Recently, it was found that V. cholerae isolates from the Haiti outbreak were poorly transformed by this mechanism. Here, we show that an integrating conjugative element (ICE)-encoded DNase, which we name IdeA, is necessary and sufficient for inhibiting natural transformation of Haiti outbreak strains. We demonstrate that IdeA inhibits this mechanism of HGT in cis via DNA endonuclease activity that is localized to the periplasm. Furthermore, we show that natural transformation between cholera strains in a relevant environmental context is inhibited by IdeA. The ICE encoding IdeA is globally distributed. Therefore, we analyzed the prevalence and role for this ICE in limiting natural transformation of isolates from Bangladesh collected between 2001 and 2011. We found that IdeA(+) ICEs were nearly ubiquitous in isolates from 2001 to 2005; however, their prevalence decreased to ∼40% from 2006 to 2011. Thus, IdeA(+) ICEs may have limited the role of natural transformation in V. cholerae. However, the rise in prevalence of strains lacking IdeA may now increase the role of this conserved mechanism of HGT in the evolution of this pathogen.

Entities:  

Keywords:  DNase; evolution; horizontal gene transfer; integrating conjugative element

Mesh:

Substances:

Year:  2015        PMID: 26240317      PMCID: PMC4547284          DOI: 10.1073/pnas.1509097112

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  39 in total

1.  DNA-uptake machinery of naturally competent Vibrio cholerae.

Authors:  Patrick Seitz; Melanie Blokesch
Journal:  Proc Natl Acad Sci U S A       Date:  2013-10-14       Impact factor: 11.205

2.  Genome sequence of hybrid Vibrio cholerae O1 MJ-1236, B-33, and CIRS101 and comparative genomics with V. cholerae.

Authors:  Christopher J Grim; Nur A Hasan; Elisa Taviani; Bradd Haley; Jongsik Chun; Thomas S Brettin; David C Bruce; J Chris Detter; Cliff S Han; Olga Chertkov; Jean Challacombe; Anwar Huq; G Balakrish Nair; Rita R Colwell
Journal:  J Bacteriol       Date:  2010-03-26       Impact factor: 3.490

Review 3.  Cholera.

Authors:  Jason B Harris; Regina C LaRocque; Firdausi Qadri; Edward T Ryan; Stephen B Calderwood
Journal:  Lancet       Date:  2012-06-30       Impact factor: 79.321

4.  The origin of the Haitian cholera outbreak strain.

Authors:  Chen-Shan Chin; Jon Sorenson; Jason B Harris; William P Robins; Richelle C Charles; Roger R Jean-Charles; James Bullard; Dale R Webster; Andrew Kasarskis; Paul Peluso; Ellen E Paxinos; Yoshiharu Yamaichi; Stephen B Calderwood; John J Mekalanos; Eric E Schadt; Matthew K Waldor
Journal:  N Engl J Med       Date:  2010-12-09       Impact factor: 91.245

5.  Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti.

Authors:  Lee S Katz; Aaron Petkau; John Beaulaurier; Shaun Tyler; Elena S Antonova; Maryann A Turnsek; Yan Guo; Susana Wang; Ellen E Paxinos; Fabini Orata; Lori M Gladney; Steven Stroika; Jason P Folster; Lori Rowe; Molly M Freeman; Natalie Knox; Mike Frace; Jacques Boncy; Morag Graham; Brian K Hammer; Yan Boucher; Ali Bashir; William P Hanage; Gary Van Domselaar; Cheryl L Tarr
Journal:  MBio       Date:  2013-07-02       Impact factor: 7.867

6.  Automated reconstruction of whole-genome phylogenies from short-sequence reads.

Authors:  Frederic Bertels; Olin K Silander; Mikhail Pachkov; Paul B Rainey; Erik van Nimwegen
Journal:  Mol Biol Evol       Date:  2014-03-05       Impact factor: 16.240

7.  Concerted spatio-temporal dynamics of imported DNA and ComE DNA uptake protein during gonococcal transformation.

Authors:  Heike Gangel; Christof Hepp; Stephanie Müller; Enno R Oldewurtel; Finn Erik Aas; Michael Koomey; Berenike Maier
Journal:  PLoS Pathog       Date:  2014-04-24       Impact factor: 6.823

8.  ComEA is essential for the transfer of external DNA into the periplasm in naturally transformable Vibrio cholerae cells.

Authors:  Patrick Seitz; Hassan Pezeshgi Modarres; Sandrine Borgeaud; Roman D Bulushev; Lorenz J Steinbock; Aleksandra Radenovic; Matteo Dal Peraro; Melanie Blokesch
Journal:  PLoS Genet       Date:  2014-01-02       Impact factor: 5.917

9.  Homopolymer tail-mediated ligation PCR: a streamlined and highly efficient method for DNA cloning and library construction.

Authors:  David W Lazinski; Andrew Camilli
Journal:  Biotechniques       Date:  2013-01       Impact factor: 1.993

10.  Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae.

Authors:  Ankur B Dalia; David W Lazinski; Andrew Camilli
Journal:  MBio       Date:  2014-01-28       Impact factor: 7.867

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  25 in total

Review 1.  The Large pBS32/pLS32 Plasmid of Ancestral Bacillus subtilis.

Authors:  Aisha T Burton; Daniel B Kearns
Journal:  J Bacteriol       Date:  2020-08-25       Impact factor: 3.490

2.  Systematic genetic dissection of PTS in Vibrio cholerae uncovers a novel glucose transporter and a limited role for PTS during infection of a mammalian host.

Authors:  Chelsea A Hayes; Triana N Dalia; Ankur B Dalia
Journal:  Mol Microbiol       Date:  2017-02-28       Impact factor: 3.501

3.  Redefinition and Unification of the SXT/R391 Family of Integrative and Conjugative Elements.

Authors:  Audrey Bioteau; Romain Durand; Vincent Burrus
Journal:  Appl Environ Microbiol       Date:  2018-06-18       Impact factor: 4.792

4.  Systematic genetic dissection of chitin degradation and uptake in Vibrio cholerae.

Authors:  Chelsea A Hayes; Triana N Dalia; Ankur B Dalia
Journal:  Environ Microbiol       Date:  2017-08-14       Impact factor: 5.491

5.  Phenotypic Analysis Reveals that the 2010 Haiti Cholera Epidemic Is Linked to a Hypervirulent Strain.

Authors:  Karla J F Satchell; Christopher J Jones; Jennifer Wong; Jessica Queen; Shivani Agarwal; Fitnat H Yildiz
Journal:  Infect Immun       Date:  2016-08-19       Impact factor: 3.441

6.  ZpdN, a Plasmid-Encoded Sigma Factor Homolog, Induces pBS32-Dependent Cell Death in Bacillus subtilis.

Authors:  B-E Myagmarjav; M A Konkol; J Ramsey; S Mukhopadhyay; D B Kearns
Journal:  J Bacteriol       Date:  2016-10-07       Impact factor: 3.490

7.  Functional Analysis of Bacteriophage Immunity through a Type I-E CRISPR-Cas System in Vibrio cholerae and Its Application in Bacteriophage Genome Engineering.

Authors:  Allison M Box; Matthew J McGuffie; Brendan J O'Hara; Kimberley D Seed
Journal:  J Bacteriol       Date:  2015-11-23       Impact factor: 3.490

8.  Diversity of Clinical and Environmental Isolates of Vibrio cholerae in Natural Transformation and Contact-Dependent Bacterial Killing Indicative of Type VI Secretion System Activity.

Authors:  Eryn E Bernardy; Maryann A Turnsek; Sarah K Wilson; Cheryl L Tarr; Brian K Hammer
Journal:  Appl Environ Microbiol       Date:  2016-04-18       Impact factor: 4.792

Review 9.  Interbacterial predation as a strategy for DNA acquisition in naturally competent bacteria.

Authors:  Jan-Willem Veening; Melanie Blokesch
Journal:  Nat Rev Microbiol       Date:  2017-07-10       Impact factor: 60.633

10.  Temporal shifts in antibiotic resistance elements govern phage-pathogen conflicts.

Authors:  Kristen N LeGault; Stephanie G Hays; Angus Angermeyer; Amelia C McKitterick; Fatema-Tuz Johura; Marzia Sultana; Tahmeed Ahmed; Munirul Alam; Kimberley D Seed
Journal:  Science       Date:  2021-07-30       Impact factor: 63.714

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