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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BMC
2019-03-01
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| Series: | BMC Microbiology |
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| Online Access: | http://link.springer.com/article/10.1186/s12866-019-1444-4 |
| _version_ | 1819162657819721728 |
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| author | Abdulmajeed D. Al-Jawdah Iglika G. Ivanova Helen Waller Neil D. Perkins Jeremy H. Lakey Daniel T. Peters |
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-22T17:31:44Z |
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| id | doaj.art-643a3f1090f945b0aeea792b167e6415 |
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| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-12-22T17:31:44Z |
| publishDate | 2019-03-01 |
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| series | BMC Microbiology |
| spelling | doaj.art-643a3f1090f945b0aeea792b167e64152022-12-21T18:18:36ZengBMCBMC 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 |
| 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 |
| title | 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_short | 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 |
| 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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