ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coli
Abstract Avian pathogenic Escherichia coli (APEC) is a notable subpathotype of the nonhuman extraintestinal pathogenic E. coli (ExPEC). Recognized as an extraintestinal foodborne pathogen, the zoonotic potential of APEC/ExPEC allows for cross-host transmission via APEC-contaminated poultry meat and...
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| Format: | Article |
| Language: | English |
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BMC
2023-11-01
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| Series: | Veterinary Research |
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| Online Access: | https://doi.org/10.1186/s13567-023-01241-2 |
| _version_ | 1797451761683791872 |
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| author | Zhongxing Wang Rui Chen Fufang Xia Min Jiang Dongyu Zhu Yuting Zhang Jianjun Dai Xiangkai Zhuge |
| author_facet | Zhongxing Wang Rui Chen Fufang Xia Min Jiang Dongyu Zhu Yuting Zhang Jianjun Dai Xiangkai Zhuge |
| author_sort | Zhongxing Wang |
| collection | DOAJ |
| description | Abstract Avian pathogenic Escherichia coli (APEC) is a notable subpathotype of the nonhuman extraintestinal pathogenic E. coli (ExPEC). Recognized as an extraintestinal foodborne pathogen, the zoonotic potential of APEC/ExPEC allows for cross-host transmission via APEC-contaminated poultry meat and eggs. ProQ, an RNA binding protein, is evolutionarily conserved in E. coli. However, its regulatory roles in the biofilm formation and virulence of APEC/ExPEC have not been explored. In this study, proQ deletion in the APEC strain FY26 significantly compromised its biofilm-forming ability. Furthermore, animal tests and cellular infection experiments showed that ProQ depletion significantly attenuated APEC virulence, thereby diminishing its capacity for bloodstream infection and effective adherence to and persistence within host cells. Transcriptome analysis revealed a decrease in the transcription level of the small RNA (sRNA) RyfA in the mutant FY26ΔproQ, suggesting a direct interaction between the sRNA RyfA and ProQ. This interaction might indicate that sRNA RyfA is a novel ProQ-associated sRNA. Moreover, the direct binding of ProQ to the sRNA RyfA was crucial for APEC biofilm formation, pathogenicity, adhesion, and intracellular survival. In conclusion, our findings provide detailed insight into the interaction between ProQ and sRNA RyfA and deepen our understanding of the regulatory elements that dictate APEC virulence and biofilm development. Such insights are instrumental in developing strategies to counteract APEC colonization within hosts and impede APEC biofilm establishment on food surfaces. |
| first_indexed | 2024-03-09T14:59:04Z |
| format | Article |
| id | doaj.art-6fff1de0f7a7495eaef1fd8bc8237bc5 |
| institution | Directory Open Access Journal |
| issn | 1297-9716 |
| language | English |
| last_indexed | 2024-03-09T14:59:04Z |
| publishDate | 2023-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Veterinary Research |
| spelling | doaj.art-6fff1de0f7a7495eaef1fd8bc8237bc52023-11-26T13:59:53ZengBMCVeterinary Research1297-97162023-11-0154111710.1186/s13567-023-01241-2ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coliZhongxing Wang0Rui Chen1Fufang Xia2Min Jiang3Dongyu Zhu4Yuting Zhang5Jianjun Dai6Xiangkai Zhuge7Department of Nutrition and Food Hygiene, School of Public Health, Nantong UniversityMOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityDepartment of Nutrition and Food Hygiene, School of Public Health, Nantong UniversityMOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityDepartment of Nutrition and Food Hygiene, School of Public Health, Nantong UniversityDepartment of Nutrition and Food Hygiene, School of Public Health, Nantong UniversityMOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityDepartment of Nutrition and Food Hygiene, School of Public Health, Nantong UniversityAbstract Avian pathogenic Escherichia coli (APEC) is a notable subpathotype of the nonhuman extraintestinal pathogenic E. coli (ExPEC). Recognized as an extraintestinal foodborne pathogen, the zoonotic potential of APEC/ExPEC allows for cross-host transmission via APEC-contaminated poultry meat and eggs. ProQ, an RNA binding protein, is evolutionarily conserved in E. coli. However, its regulatory roles in the biofilm formation and virulence of APEC/ExPEC have not been explored. In this study, proQ deletion in the APEC strain FY26 significantly compromised its biofilm-forming ability. Furthermore, animal tests and cellular infection experiments showed that ProQ depletion significantly attenuated APEC virulence, thereby diminishing its capacity for bloodstream infection and effective adherence to and persistence within host cells. Transcriptome analysis revealed a decrease in the transcription level of the small RNA (sRNA) RyfA in the mutant FY26ΔproQ, suggesting a direct interaction between the sRNA RyfA and ProQ. This interaction might indicate that sRNA RyfA is a novel ProQ-associated sRNA. Moreover, the direct binding of ProQ to the sRNA RyfA was crucial for APEC biofilm formation, pathogenicity, adhesion, and intracellular survival. In conclusion, our findings provide detailed insight into the interaction between ProQ and sRNA RyfA and deepen our understanding of the regulatory elements that dictate APEC virulence and biofilm development. Such insights are instrumental in developing strategies to counteract APEC colonization within hosts and impede APEC biofilm establishment on food surfaces.https://doi.org/10.1186/s13567-023-01241-2APEC/ExPECProQsRNA RyfAvirulencebiofilm formation |
| spellingShingle | Zhongxing Wang Rui Chen Fufang Xia Min Jiang Dongyu Zhu Yuting Zhang Jianjun Dai Xiangkai Zhuge ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coli Veterinary Research APEC/ExPEC ProQ sRNA RyfA virulence biofilm formation |
| title | ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coli |
| title_full | ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coli |
| title_fullStr | ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coli |
| title_full_unstemmed | ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coli |
| title_short | ProQ binding to small RNA RyfA promotes virulence and biofilm formation in avian pathogenic Escherichia coli |
| title_sort | proq binding to small rna ryfa promotes virulence and biofilm formation in avian pathogenic escherichia coli |
| topic | APEC/ExPEC ProQ sRNA RyfA virulence biofilm formation |
| url | https://doi.org/10.1186/s13567-023-01241-2 |
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