Literature DB >> 29247061

Impact of Cell Surface Molecules on Conjugative Transfer of the Integrative and Conjugative Element ICESt3 of Streptococcus thermophilus.

Narimane Dahmane1, Emilie Robert1, Julien Deschamps2, Thierry Meylheuc2,3, Christine Delorme2, Romain Briandet2, Nathalie Leblond-Bourget1, Eric Guédon4, Sophie Payot5.   

Abstract

Integrative conjugative elements (ICEs) are chromosomal elements that are widely distributed in bacterial genomes, hence contributing to genome plasticity, adaptation, and evolution of bacteria. Conjugation requires a contact between both the donor and the recipient cells and thus likely depends on the composition of the cell surface envelope. In this work, we investigated the impact of different cell surface molecules, including cell surface proteins, wall teichoic acids, lipoteichoic acids, and exopolysaccharides, on the transfer and acquisition of ICESt3 from Streptococcus thermophilus The transfer of ICESt3 from wild-type (WT) donor cells to mutated recipient cells increased 5- to 400-fold when recipient cells were affected in lipoproteins, teichoic acids, or exopolysaccharides compared to when the recipient cells were WT. These mutants displayed an increased biofilm-forming ability compared to the WT, suggesting better cell interactions that could contribute to the increase of ICESt3 acquisition. Microscopic observations of S. thermophilus cell surface mutants showed different phenotypes (aggregation in particular) that can also have an impact on conjugation. In contrast, the same mutations did not have the same impact when the donor cells, instead of recipient cells, were mutated. In that case, the transfer frequency of ICESt3 decreased compared to that with the WT. The same observation was made when both donor and recipient cells were mutated. The dominant effect of mutations in donor cells suggests that modifications of the cell envelope could impair the establishment or activity of the conjugation machinery required for DNA transport.IMPORTANCE ICEs contribute to horizontal gene transfer of adaptive traits (for example, virulence, antibiotic resistance, or biofilm formation) and play a considerable role in bacterial genome evolution, thus underlining the need of a better understanding of their conjugative mechanism of transfer. While most studies focus on the different functions encoded by ICEs, little is known about the effect of host factors on their conjugative transfer. Using ICESt3 of S. thermophilus as a model, we demonstrated the impact of lipoproteins, teichoic acids, and exopolysaccharides on ICE transfer and acquisition. This opens up new avenues to control gene transfer mediated by ICEs.
Copyright © 2018 American Society for Microbiology.

Entities:  

Keywords:  Streptococcus thermophilus; biofilm; cell surface molecules; conjugation; exopolysaccharides; gene transfer; integrative conjugative element; lipoteichoic acids; mutant; wall teichoic acids

Mesh:

Year:  2018        PMID: 29247061      PMCID: PMC5812943          DOI: 10.1128/AEM.02109-17

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  46 in total

1.  Effect of D-alanine in teichoic acid from the Streptococcus thermophilus cell wall on the barrier-protection of intestinal epithelial cells.

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Journal:  Biosci Biotechnol Biochem       Date:  2012-02-07       Impact factor: 2.043

Review 2.  Beyond the canonical strategies of horizontal gene transfer in prokaryotes.

Authors:  Cristina García-Aljaro; Elisenda Ballesté; Maite Muniesa
Journal:  Curr Opin Microbiol       Date:  2017-06-08       Impact factor: 7.934

3.  Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis subsp. cremoris using a new shuttle vector.

Authors:  Y A Que; J A Haefliger; P Francioli; P Moreillon
Journal:  Infect Immun       Date:  2000-06       Impact factor: 3.441

Review 4.  New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics.

Authors:  Pascal Hols; Frédéric Hancy; Laetitia Fontaine; Benoît Grossiord; Deborah Prozzi; Nathalie Leblond-Bourget; Bernard Decaris; Alexander Bolotin; Christine Delorme; S Dusko Ehrlich; Eric Guédon; Véronique Monnet; Pierre Renault; Michiel Kleerebezem
Journal:  FEMS Microbiol Rev       Date:  2005-08       Impact factor: 16.408

5.  Conjugative transfer of the integrative conjugative elements ICESt1 and ICESt3 from Streptococcus thermophilus.

Authors:  Xavier Bellanger; Adam P Roberts; Catherine Morel; Frédéric Choulet; Guillaume Pavlovic; Peter Mullany; Bernard Decaris; Gérard Guédon
Journal:  J Bacteriol       Date:  2009-01-30       Impact factor: 3.490

6.  Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus.

Authors:  Angelika Gründling; Olaf Schneewind
Journal:  Proc Natl Acad Sci U S A       Date:  2007-05-03       Impact factor: 11.205

Review 7.  Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies.

Authors:  Jochen Schmid; Volker Sieber; Bernd Rehm
Journal:  Front Microbiol       Date:  2015-05-26       Impact factor: 5.640

Review 8.  Cell wall structure and function in lactic acid bacteria.

Authors:  Marie-Pierre Chapot-Chartier; Saulius Kulakauskas
Journal:  Microb Cell Fact       Date:  2014-08-29       Impact factor: 5.328

Review 9.  The hidden life of integrative and conjugative elements.

Authors:  François Delavat; Ryo Miyazaki; Nicolas Carraro; Nicolas Pradervand; Jan Roelof van der Meer
Journal:  FEMS Microbiol Rev       Date:  2017-07-01       Impact factor: 16.408

10.  Two-enzyme systems for glycolipid and polyglycerolphosphate lipoteichoic acid synthesis in Listeria monocytogenes.

Authors:  Alexander J Webb; Maria Karatsa-Dodgson; Angelika Gründling
Journal:  Mol Microbiol       Date:  2009-08-04       Impact factor: 3.501

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  7 in total

1.  Key Role of Transconjugants for Dissemination of the Integrative Conjugative Element ICEBs1 in Biofilms.

Authors:  Sophie Payot
Journal:  J Bacteriol       Date:  2022-09-15       Impact factor: 3.476

Review 2.  Genome editing of lactic acid bacteria: opportunities for food, feed, pharma and biotech.

Authors:  Rosa A Börner; Vijayalakshmi Kandasamy; Amalie M Axelsen; Alex T Nielsen; Elleke F Bosma
Journal:  FEMS Microbiol Lett       Date:  2019-01-01       Impact factor: 2.742

3.  Structural and Biochemical Analysis of OrfG: The VirB8-like Component of the Conjugative Type IV Secretion System of ICESt3 From Streptococcus thermophilus.

Authors:  Julien Cappele; Abbas Mohamad Ali; Nathalie Leblond-Bourget; Sandrine Mathiot; Tiphaine Dhalleine; Sophie Payot; Martin Savko; Claude Didierjean; Frédérique Favier; Badreddine Douzi
Journal:  Front Mol Biosci       Date:  2021-03-18

4.  A CRISPR interference screen reveals a role for cell wall teichoic acids in conjugation in Bacillus subtilis.

Authors:  M Michael Harden; Mary E Anderson; Alan D Grossman
Journal:  Mol Microbiol       Date:  2022-05-21       Impact factor: 3.979

5.  Chromosomal Conjugative and Mobilizable Elements in Streptococcus suis: Major Actors in the Spreading of Antimicrobial Resistance and Bacteriocin Synthesis Genes.

Authors:  Virginie Libante; Yves Nombre; Charles Coluzzi; Johan Staub; Gérard Guédon; Marcelo Gottschalk; Sarah Teatero; Nahuel Fittipaldi; Nathalie Leblond-Bourget; Sophie Payot
Journal:  Pathogens       Date:  2019-12-25

Review 6.  Safety Aspects of Genetically Modified Lactic Acid Bacteria.

Authors:  Tina Vida Plavec; Aleš Berlec
Journal:  Microorganisms       Date:  2020-02-21

7.  Mobilization of IMEs Integrated in the oriT of ICEs Involves Their Own Relaxase Belonging to the Rep-Trans Family of Proteins.

Authors:  Virginie Libante; Nazim Sarica; Abbas Mohamad Ali; Chloé Gapp; Anissa Oussalah; Gérard Guédon; Nathalie Leblond-Bourget; Sophie Payot
Journal:  Genes (Basel)       Date:  2020-08-26       Impact factor: 4.096

  7 in total

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