The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic Stress
The expression of flagellar proteins in <i>Brucella</i> species likely evolved through genetic transference from other microorganisms, and contributed to virulence, adaptability, and biofilm formation. Despite significant progress in defining the molecular mechanisms behind flagellar gen...
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MDPI AG
2022-08-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/17/9905 |
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| author | Jia Guo Xingmei Deng Yu Zhang Shengnan Song Tianyi Zhao Dexin Zhu Shuzhu Cao Peter Ivanovic Baryshnikov Gang Cao Hugh T. Blair Chuangfu Chen Xinli Gu Liangbo Liu Hui Zhang |
| author_facet | Jia Guo Xingmei Deng Yu Zhang Shengnan Song Tianyi Zhao Dexin Zhu Shuzhu Cao Peter Ivanovic Baryshnikov Gang Cao Hugh T. Blair Chuangfu Chen Xinli Gu Liangbo Liu Hui Zhang |
| author_sort | Jia Guo |
| collection | DOAJ |
| description | The expression of flagellar proteins in <i>Brucella</i> species likely evolved through genetic transference from other microorganisms, and contributed to virulence, adaptability, and biofilm formation. Despite significant progress in defining the molecular mechanisms behind flagellar gene expression, the genetic program controlling biofilm formation remains unclear. The flagellar transcriptional factor (FtcR) is a master regulator of the flagellar system’s expression, and is critical for <i>B. melitensis</i> 16M’s flagellar biogenesis and virulence. Here, we demonstrate that FtcR mediates biofilm formation under hyperosmotic stress. Chromatin immunoprecipitation with next-generation sequencing for FtcR and RNA sequencing of <i>ftcR</i>-mutant and wild-type strains revealed a core set of FtcR target genes. We identified a novel FtcR-binding site in the promoter region of the osmotic-stress-response regulator gene <i>betI</i>, which is important for the survival of <i>B. melitensis</i> 16M under hyperosmotic stress. Strikingly, this site autoregulates its expression to benefit biofilm bacteria’s survival under hyperosmotic stress. Moreover, biofilm reduction in <i>ftcR</i> mutants is independent of the flagellar target gene <i>fliF</i>. Collectively, our study provides new insights into the extent and functionality of flagellar-related transcriptional networks in biofilm formation, and presents phenotypic and evolutionary adaptations that alter the regulation of <i>B. melitensis</i> 16M to confer increased tolerance to hyperosmotic stress. |
| first_indexed | 2024-03-10T01:43:18Z |
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| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T01:43:18Z |
| publishDate | 2022-08-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-6b8d563d32014164982c63b696a3f0632023-11-23T13:19:13ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-08-012317990510.3390/ijms23179905The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic StressJia Guo0Xingmei Deng1Yu Zhang2Shengnan Song3Tianyi Zhao4Dexin Zhu5Shuzhu Cao6Peter Ivanovic Baryshnikov7Gang Cao8Hugh T. Blair9Chuangfu Chen10Xinli Gu11Liangbo Liu12Hui Zhang13State International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430000, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi 832003, ChinaThe expression of flagellar proteins in <i>Brucella</i> species likely evolved through genetic transference from other microorganisms, and contributed to virulence, adaptability, and biofilm formation. Despite significant progress in defining the molecular mechanisms behind flagellar gene expression, the genetic program controlling biofilm formation remains unclear. The flagellar transcriptional factor (FtcR) is a master regulator of the flagellar system’s expression, and is critical for <i>B. melitensis</i> 16M’s flagellar biogenesis and virulence. Here, we demonstrate that FtcR mediates biofilm formation under hyperosmotic stress. Chromatin immunoprecipitation with next-generation sequencing for FtcR and RNA sequencing of <i>ftcR</i>-mutant and wild-type strains revealed a core set of FtcR target genes. We identified a novel FtcR-binding site in the promoter region of the osmotic-stress-response regulator gene <i>betI</i>, which is important for the survival of <i>B. melitensis</i> 16M under hyperosmotic stress. Strikingly, this site autoregulates its expression to benefit biofilm bacteria’s survival under hyperosmotic stress. Moreover, biofilm reduction in <i>ftcR</i> mutants is independent of the flagellar target gene <i>fliF</i>. Collectively, our study provides new insights into the extent and functionality of flagellar-related transcriptional networks in biofilm formation, and presents phenotypic and evolutionary adaptations that alter the regulation of <i>B. melitensis</i> 16M to confer increased tolerance to hyperosmotic stress.https://www.mdpi.com/1422-0067/23/17/9905<i>Brucella melitensis</i> 16Mflagellar transcriptional factor FtcR<i>betI</i>biofilmhyperosmotic stress |
| spellingShingle | Jia Guo Xingmei Deng Yu Zhang Shengnan Song Tianyi Zhao Dexin Zhu Shuzhu Cao Peter Ivanovic Baryshnikov Gang Cao Hugh T. Blair Chuangfu Chen Xinli Gu Liangbo Liu Hui Zhang The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic Stress International Journal of Molecular Sciences <i>Brucella melitensis</i> 16M flagellar transcriptional factor FtcR <i>betI</i> biofilm hyperosmotic stress |
| title | The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic Stress |
| title_full | The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic Stress |
| title_fullStr | The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic Stress |
| title_full_unstemmed | The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic Stress |
| title_short | The Flagellar Transcriptional Regulator FtcR Controls <i>Brucella melitensis</i> 16M Biofilm Formation via a <i>betI</i>-Mediated Pathway in Response to Hyperosmotic Stress |
| title_sort | flagellar transcriptional regulator ftcr controls i brucella melitensis i 16m biofilm formation via a i beti i mediated pathway in response to hyperosmotic stress |
| topic | <i>Brucella melitensis</i> 16M flagellar transcriptional factor FtcR <i>betI</i> biofilm hyperosmotic stress |
| url | https://www.mdpi.com/1422-0067/23/17/9905 |
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