Literature DB >> 28348085

The extent of the temperature-induced membrane remodeling in two closely related Bordetella species reflects their adaptation to diverse environmental niches.

Gabriela Seydlova1, Jana Beranova1, Ilona Bibova2, Ana Dienstbier2, Jakub Drzmisek2, Jiri Masin3, Radovan Fiser1, Ivo Konopasek1, Branislav Vecerek4.   

Abstract

Changes in environmental temperature represent one of the major stresses faced by microorganisms as they affect the function of the cytoplasmic membrane. In this study, we have analyzed the thermal adaptation in two closely related respiratory pathogens Bordetella pertussis and Bordetella bronchiseptica Although B. pertussis represents a pathogen strictly adapted to the human body temperature, B. bronchiseptica causes infection in a broad range of animals and survives also outside of the host. We applied GC-MS to determine the fatty acids of both Bordetella species grown at different temperatures and analyzed the membrane fluidity by fluorescence anisotropy measurement. In parallel, we also monitored the effect of growth temperature changes on the expression and production of several virulence factors. In response to low temperatures, B. pertussis adapted its fatty acid composition and membrane fluidity to a considerably lesser extent when compared with B. bronchiseptica Remarkably, B. pertussis maintained the production of virulence factors at 24 °C, whereas B. bronchiseptica cells resumed the production only upon temperature upshift to 37 °C. This growth temperature-associated differential modulation of virulence factor production was linked to the phosphorylation state of transcriptional regulator BvgA. The observed differences in low-temperature adaptation between B. pertussis and B. bronchiseptica may result from selective adaptation of B. pertussis to the human host. We propose that the reduced plasticity of the B. pertussis membranes ensures sustained production of virulence factors at suboptimal temperatures and may play an important role in the transmission of the disease.
© 2017 by The American Society for Biochemistry and Molecular Biology, Inc.

Entities:  

Keywords:  bacterial pathogenesis; bacterial signal transduction; fatty acid; host adaptation; membrane function; virulence factor

Mesh:

Substances:

Year:  2017        PMID: 28348085      PMCID: PMC5427280          DOI: 10.1074/jbc.M117.781559

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  57 in total

1.  Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica.

Authors:  Julian Parkhill; Mohammed Sebaihia; Andrew Preston; Lee D Murphy; Nicholas Thomson; David E Harris; Matthew T G Holden; Carol M Churcher; Stephen D Bentley; Karen L Mungall; Ana M Cerdeño-Tárraga; Louise Temple; Keith James; Barbara Harris; Michael A Quail; Mark Achtman; Rebecca Atkin; Steven Baker; David Basham; Nathalie Bason; Inna Cherevach; Tracey Chillingworth; Matthew Collins; Anne Cronin; Paul Davis; Jonathan Doggett; Theresa Feltwell; Arlette Goble; Nancy Hamlin; Heidi Hauser; Simon Holroyd; Kay Jagels; Sampsa Leather; Sharon Moule; Halina Norberczak; Susan O'Neil; Doug Ormond; Claire Price; Ester Rabbinowitsch; Simon Rutter; Mandy Sanders; David Saunders; Katherine Seeger; Sarah Sharp; Mark Simmonds; Jason Skelton; Robert Squares; Steven Squares; Kim Stevens; Louise Unwin; Sally Whitehead; Bart G Barrell; Duncan J Maskell
Journal:  Nat Genet       Date:  2003-08-10       Impact factor: 38.330

2.  Antigenic modulation of Bordetella pertussis.

Authors:  B W LACEY
Journal:  J Hyg (Lond)       Date:  1960-03

3.  The RNA chaperone Hfq is required for virulence of Bordetella pertussis.

Authors:  Ilona Bibova; Karolina Skopova; Jiri Masin; Ondrej Cerny; David Hot; Peter Sebo; Branislav Vecerek
Journal:  Infect Immun       Date:  2013-08-26       Impact factor: 3.441

4.  Comparative analysis of the virulence control systems of Bordetella pertussis and Bordetella bronchiseptica.

Authors:  G Martínez de Tejada; J F Miller; P A Cotter
Journal:  Mol Microbiol       Date:  1996-12       Impact factor: 3.501

5.  Environmental regulation of expression of virulence determinants in Bordetella pertussis.

Authors:  A R Melton; A A Weiss
Journal:  J Bacteriol       Date:  1989-11       Impact factor: 3.490

6.  Bordetella pertussis adenylate cyclase: effects of affinity-purified adenylate cyclase on human polymorphonuclear leukocyte functions.

Authors:  R L Friedman; R L Fiederlein; L Glasser; J N Galgiani
Journal:  Infect Immun       Date:  1987-01       Impact factor: 3.441

7.  Thermal regulation of membrane fluidity in Escherichia coli. Effects of overproduction of beta-ketoacyl-acyl carrier protein synthase I.

Authors:  D de Mendoza; A Klages Ulrich; J E Cronan
Journal:  J Biol Chem       Date:  1983-02-25       Impact factor: 5.157

8.  Physiological differences between cyclopropane fatty acid-deficient mutants and the parent strain of Streptococcus faecalis.

Authors:  D L Jungkind; R C Wood
Journal:  Biochim Biophys Acta       Date:  1974-02-25

9.  In vivo phosphorylation dynamics of the Bordetella pertussis virulence-controlling response regulator BvgA.

Authors:  Alice Boulanger; Qing Chen; Deborah M Hinton; Scott Stibitz
Journal:  Mol Microbiol       Date:  2013-03-14       Impact factor: 3.501

10.  Characteristic lipids of Bordetella pertussis: simple fatty acid composition, hydroxy fatty acids, and an ornithine-containing lipid.

Authors:  Y Kawai; A Moribayashi
Journal:  J Bacteriol       Date:  1982-08       Impact factor: 3.490

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  5 in total

1.  Signal transduction-dependent small regulatory RNA is involved in glutamate metabolism of the human pathogen Bordetella pertussis.

Authors:  Kristina Keidel; Fabian Amman; Ilona Bibova; Jakub Drzmisek; Vladimir Benes; David Hot; Branislav Vecerek
Journal:  RNA       Date:  2018-08-10       Impact factor: 4.942

2.  A Mutation Upstream of the rplN-rpsD Ribosomal Operon Downregulates Bordetella pertussis Virulence Factor Production without Compromising Bacterial Survival within Human Macrophages.

Authors:  Jakub Novák; David Jurnečka; Irena Linhartová; Jana Holubová; Ondřej Staněk; Daniel Štipl; Ana Dienstbier; Branislav Večerek; Nayara Azevedo; Jan Provazník; Vladimír Beneš; Peter Šebo
Journal:  mSystems       Date:  2020-12-08       Impact factor: 6.496

3.  A Unique Reverse Adaptation Mechanism Assists Bordetella pertussis in Resistance to Both Scarcity and Toxicity of Manganese.

Authors:  Jan Čapek; Ilona Procházková; Tomáš Matoušek; David Hot; Branislav Večerek
Journal:  mBio       Date:  2021-10-26       Impact factor: 7.867

Review 4.  Pathogenicity and virulence of Bordetella pertussis and its adaptation to its strictly human host.

Authors:  Thomas Belcher; Violaine Dubois; Alex Rivera-Millot; Camille Locht; Françoise Jacob-Dubuisson
Journal:  Virulence       Date:  2021-12       Impact factor: 5.882

5.  Distinct virulence ranges for infection of mice by Bordetella pertussis revealed by engineering of the sensor-kinase BvgS.

Authors:  Elodie Lesne; Loic Coutte; Luis Solans; Stephanie Slupek; Anne-Sophie Debrie; Véronique Dhennin; Philippe Froguel; David Hot; Camille Locht; Rudy Antoine; Françoise Jacob-Dubuisson
Journal:  PLoS One       Date:  2018-10-11       Impact factor: 3.240

  5 in total

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