Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factor

Abstract Background Thermal regulation of gene expression occurs in many microorganisms, and is mediated via several typical mechanisms. Yersinia pestis is the causative agent of the plague and spreads by zoonotic transfer from fleas to mammalian blood with a concomitant rapid temperature change, fr...

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Main Authors: Abdulmajeed D. Al-Jawdah, Iglika G. Ivanova, Helen Waller, Neil D. Perkins, Jeremy H. Lakey, Daniel T. Peters
Format: Article
Language:English
Published: BMC 2019-03-01
Series:BMC Microbiology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12866-019-1444-4
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spelling doaj-643a3f1090f945b0aeea792b167e64152020-11-25T02:20:51ZengBMCBMC Microbiology1471-21802019-03-0119111210.1186/s12866-019-1444-4Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factorAbdulmajeed D. Al-Jawdah0Iglika G. Ivanova1Helen Waller2Neil D. Perkins3Jeremy H. Lakey4Daniel T. Peters5Institute for Cell and Molecular Biosciences, Medical School, Newcastle UniversityInstitute for Cell and Molecular Biosciences, Medical School, Newcastle UniversityInstitute for Cell and Molecular Biosciences, Medical School, Newcastle UniversityInstitute for Cell and Molecular Biosciences, Medical School, Newcastle UniversityInstitute for Cell and Molecular Biosciences, Medical School, Newcastle UniversityInstitute for Cell and Molecular Biosciences, Medical School, Newcastle UniversityAbstract Background Thermal regulation of gene expression occurs in many microorganisms, and is mediated via several typical mechanisms. Yersinia pestis is the causative agent of the plague and spreads by zoonotic transfer from fleas to mammalian blood with a concomitant rapid temperature change, from ambient to 37 °C, which induces the expression of capsular antigen (Caf1) that inhibits phagocytosis. Caf1 is formed into long polymeric fimbriae by a periplasmic chaperone (Caf1M) and outer membrane usher (Caf1A). All three are encoded on an operon regulated by an AraC-type transcription factor Caf1R. The aim of this study was to determine the role of Caf1R in the thermal control of caf1 operon gene expression. Results PCR analysis of cDNA demonstrated that the genes of the operon are transcribed as a single polycistronic mRNA. Bioinformatic analysis, supported by deletion mutagenesis, then revealed a region containing the promoter of this polycistronic transcript that was critical for Caf1 protein expression. Caf1R was found to be essential for Caf1 protein production. Finally, RT-PCR analysis and western blot experiments showed large, Caf1R dependent increases in caf1 operon transcripts upon a shift in temperature from 25 °C to 35 °C. Conclusions The results show that thermal control of Caf1 polymer production is established at the transcriptional level, in a Caf1R dependent manner. This gives us new insights into how a virulent pathogen evades destruction by the immune system by detecting and responding to environmental changes.http://link.springer.com/article/10.1186/s12866-019-1444-4Gene expression regulationYersinia pestisAraC transcription factorTemperatureFimbriae, bacterial
collection DOAJ
language English
format Article
sources DOAJ
author Abdulmajeed D. Al-Jawdah
Iglika G. Ivanova
Helen Waller
Neil D. Perkins
Jeremy H. Lakey
Daniel T. Peters
spellingShingle Abdulmajeed D. Al-Jawdah
Iglika G. Ivanova
Helen Waller
Neil D. Perkins
Jeremy H. Lakey
Daniel T. Peters
Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factor
BMC Microbiology
Gene expression regulation
Yersinia pestis
AraC transcription factor
Temperature
Fimbriae, bacterial
author_facet Abdulmajeed D. Al-Jawdah
Iglika G. Ivanova
Helen Waller
Neil D. Perkins
Jeremy H. Lakey
Daniel T. Peters
author_sort Abdulmajeed D. Al-Jawdah
title Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factor
title_short Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factor
title_full Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factor
title_fullStr Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factor
title_full_unstemmed Induction of the immunoprotective coat of Yersinia pestis at body temperature is mediated by the Caf1R transcription factor
title_sort induction of the immunoprotective coat of yersinia pestis at body temperature is mediated by the caf1r transcription factor
publisher BMC
series BMC Microbiology
issn 1471-2180
publishDate 2019-03-01
description Abstract Background Thermal regulation of gene expression occurs in many microorganisms, and is mediated via several typical mechanisms. Yersinia pestis is the causative agent of the plague and spreads by zoonotic transfer from fleas to mammalian blood with a concomitant rapid temperature change, from ambient to 37 °C, which induces the expression of capsular antigen (Caf1) that inhibits phagocytosis. Caf1 is formed into long polymeric fimbriae by a periplasmic chaperone (Caf1M) and outer membrane usher (Caf1A). All three are encoded on an operon regulated by an AraC-type transcription factor Caf1R. The aim of this study was to determine the role of Caf1R in the thermal control of caf1 operon gene expression. Results PCR analysis of cDNA demonstrated that the genes of the operon are transcribed as a single polycistronic mRNA. Bioinformatic analysis, supported by deletion mutagenesis, then revealed a region containing the promoter of this polycistronic transcript that was critical for Caf1 protein expression. Caf1R was found to be essential for Caf1 protein production. Finally, RT-PCR analysis and western blot experiments showed large, Caf1R dependent increases in caf1 operon transcripts upon a shift in temperature from 25 °C to 35 °C. Conclusions The results show that thermal control of Caf1 polymer production is established at the transcriptional level, in a Caf1R dependent manner. This gives us new insights into how a virulent pathogen evades destruction by the immune system by detecting and responding to environmental changes.
topic Gene expression regulation
Yersinia pestis
AraC transcription factor
Temperature
Fimbriae, bacterial
url http://link.springer.com/article/10.1186/s12866-019-1444-4
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