Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gut

Abstract Background Campylobacter jejuni (C. jejuni) is a leading cause of foodborne gastroenteritis worldwide. This bacterium lacks many of the classical virulence factors, and flagellum-associated persistent colonization has been shown to be crucial for its pathogenesis. The flagellum plays a mult...

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Main Authors: Fangzhe Ren, Xiaofei Li, Haiyan Tang, Qidong Jiang, Xi Yun, Lin Fang, Pingyu Huang, Yuanyue Tang, Qiuchun Li, Jinlin Huang, Xin-an Jiao
Format: Article
Language:English
Published: BMC 2018-10-01
Series:BMC Microbiology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12866-018-1318-1
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author Fangzhe Ren
Xiaofei Li
Haiyan Tang
Qidong Jiang
Xi Yun
Lin Fang
Pingyu Huang
Yuanyue Tang
Qiuchun Li
Jinlin Huang
Xin-an Jiao
author_facet Fangzhe Ren
Xiaofei Li
Haiyan Tang
Qidong Jiang
Xi Yun
Lin Fang
Pingyu Huang
Yuanyue Tang
Qiuchun Li
Jinlin Huang
Xin-an Jiao
author_sort Fangzhe Ren
collection DOAJ
description Abstract Background Campylobacter jejuni (C. jejuni) is a leading cause of foodborne gastroenteritis worldwide. This bacterium lacks many of the classical virulence factors, and flagellum-associated persistent colonization has been shown to be crucial for its pathogenesis. The flagellum plays a multifunctional role in C. jejuni pathogenesis, and different flagellar elements make diverse contributions. The flhF gene encodes the flagellar biosynthesis regulator, which is important for flagellar biosynthesis. In this study, the influence of flhF on C. jejuni colonization was systematically studied, and the possible mechanisms were also analyzed. Results The flhF gene has a significant influence on C. jejuni colonization, and its inactivation resulted in severe defects in the commensal colonization of chicks, with approximately 104- to 107-fold reductions (for NCTC 11168 and a C. jejuni isolate respectively) observed in the bacterial caecal loads. Similar effects were observed in mice where the flhF mutant strain completely lost the ability to continuously colonize mice, which cleared the isolate at 7 days post inoculation. Characterization of the phenotypic properties of C. jejuni that influence colonization showed that the adhesion and invasion abilities of the C. jejuni flhF mutant were reduced to approximately 52 and 27% of that of the wild-type strain, respectively. The autoagglutination and biofilm-formation abilities of the flhF mutant strain were also significantly decreased. Further genetic investigation revealed that flhF is continuously upregulated during the infection process, which indicates a close association of this gene with C. jejuni pathogenesis. The transcription of some other infection-related genes that are not directly involved in flagellar assembly were also influenced by its inactivation, with the flagellar coexpressed determinants (Feds) being apparently affected. Conclusions Inactivation of flhF has a significant influence on C. jejuni colonization in both birds and mammals. This defect may be caused by the decreased adhesion, invasion, autoagglutination and biofilm-formation abilities of the flhF mutant strain, as well as the influence on the transcription of other infection related genes, which provides insights into this virulence factor and the flagellum mediated co-regulation of C. jejuni pathogenesis.
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spelling doaj.art-0c5f69485bf54b92a270758c5bab41f62022-12-21T19:06:37ZengBMCBMC Microbiology1471-21802018-10-0118111110.1186/s12866-018-1318-1Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gutFangzhe Ren0Xiaofei Li1Haiyan Tang2Qidong Jiang3Xi Yun4Lin Fang5Pingyu Huang6Yuanyue Tang7Qiuchun Li8Jinlin Huang9Xin-an Jiao10Jiangsu Key Lab of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityKey Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture of ChinaKey Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture of ChinaKey Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture of ChinaJoint International Research Laboratory of Agriculture and Agri-product Safety, Ministry of Education of ChinaJoint International Research Laboratory of Agriculture and Agri-product Safety, Ministry of Education of ChinaJoint International Research Laboratory of Agriculture and Agri-product Safety, Ministry of Education of ChinaJiangsu Key Lab of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Key Lab of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Key Lab of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Key Lab of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityAbstract Background Campylobacter jejuni (C. jejuni) is a leading cause of foodborne gastroenteritis worldwide. This bacterium lacks many of the classical virulence factors, and flagellum-associated persistent colonization has been shown to be crucial for its pathogenesis. The flagellum plays a multifunctional role in C. jejuni pathogenesis, and different flagellar elements make diverse contributions. The flhF gene encodes the flagellar biosynthesis regulator, which is important for flagellar biosynthesis. In this study, the influence of flhF on C. jejuni colonization was systematically studied, and the possible mechanisms were also analyzed. Results The flhF gene has a significant influence on C. jejuni colonization, and its inactivation resulted in severe defects in the commensal colonization of chicks, with approximately 104- to 107-fold reductions (for NCTC 11168 and a C. jejuni isolate respectively) observed in the bacterial caecal loads. Similar effects were observed in mice where the flhF mutant strain completely lost the ability to continuously colonize mice, which cleared the isolate at 7 days post inoculation. Characterization of the phenotypic properties of C. jejuni that influence colonization showed that the adhesion and invasion abilities of the C. jejuni flhF mutant were reduced to approximately 52 and 27% of that of the wild-type strain, respectively. The autoagglutination and biofilm-formation abilities of the flhF mutant strain were also significantly decreased. Further genetic investigation revealed that flhF is continuously upregulated during the infection process, which indicates a close association of this gene with C. jejuni pathogenesis. The transcription of some other infection-related genes that are not directly involved in flagellar assembly were also influenced by its inactivation, with the flagellar coexpressed determinants (Feds) being apparently affected. Conclusions Inactivation of flhF has a significant influence on C. jejuni colonization in both birds and mammals. This defect may be caused by the decreased adhesion, invasion, autoagglutination and biofilm-formation abilities of the flhF mutant strain, as well as the influence on the transcription of other infection related genes, which provides insights into this virulence factor and the flagellum mediated co-regulation of C. jejuni pathogenesis.http://link.springer.com/article/10.1186/s12866-018-1318-1flhFColonizationCampylobacter jejuni
spellingShingle Fangzhe Ren
Xiaofei Li
Haiyan Tang
Qidong Jiang
Xi Yun
Lin Fang
Pingyu Huang
Yuanyue Tang
Qiuchun Li
Jinlin Huang
Xin-an Jiao
Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gut
BMC Microbiology
flhF
Colonization
Campylobacter jejuni
title Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gut
title_full Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gut
title_fullStr Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gut
title_full_unstemmed Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gut
title_short Insights into the impact of flhF inactivation on Campylobacter jejuni colonization of chick and mice gut
title_sort insights into the impact of flhf inactivation on campylobacter jejuni colonization of chick and mice gut
topic flhF
Colonization
Campylobacter jejuni
url http://link.springer.com/article/10.1186/s12866-018-1318-1
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