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Genome degradation promotes Salmonella pathoadaptation by remodeling fimbriae-mediated proinflammatory response

文献类型: 外文期刊

作者: Zhou, Xiao 1 ; Kang, Xiamei 1 ; Chen, Jiaqi 1 ; Song, Yan 1 ; Jia, Chenghao 1 ; Teng, Lin 1 ; Tang, Yanting 1 ; Jiang, Zhijie 1 ; Peng, Xianqi 1 ; Tao, Xiaoxi 1 ; Xu, Yiwei 1 ; Huang, Linlin 1 ; Xu, Xuebin 5 ; Xu, Yaohui 6 ; Zhang, Tengfei 7 ; Yu, Shenye 8 ; Gong, Jiansen 9 ; Wang, Shaohui 10 ; Liu, Yuqing 11 ; Zhu, Guoqiang 12 ; Kehrenberg, Corinna 13 ; Weill, Francois-Xavier 14 ; Barrow, Paul 15 ; Li, Yan 1 ; Zhao, Guoping 16 ; Yue, Min 1 ;

作者机构: 1.Zhejiang Univ, Inst Prevent Vet Sci, Hangzhou 310058, Peoples R China

2.Zhejiang Univ, Coll Anim Sci, Dept Vet Med, Hangzhou 310058, Peoples R China

3.Zhejiang Univ, Hainan Inst, Sanya 572025, Peoples R China

4.Ningbo Acad Agr Sci, Ningbo 315040, Peoples R China

5.Shanghai Municipal Ctr Dis Control & Prevent, Dept Microbiol Lab, Shanghai 200336, Peoples R China

6.Henan Univ Anim Husb & Econ, Coll Vet Med, Zhengzhou 450053, Peoples R China

7.Hubei Acad Agr Sci, Key Lab Prevent & Control Agents Anim Bacteriosis, Inst Anim Husb & Vet, Wuhan 430064, Peoples R China

8.Chinese Acad Agr Sci, Harbin Vet Res Inst, Div Bacterial Dis, State Key Lab Vet Biotechnol, Harbin 150069, Peoples R China

9.Chinese Acad Agr Sci, Poultry Inst, Yangzhou 225125, Peoples R China

10.Chinese Acad Agr Sci, Shanghai Vet Res Inst, Dept Anim Publ Hlth, Shanghai 200241, Peoples R China

11.Shandong Acad Agr Sci, Inst Anim Sci & Vet Med, Shandong Key Lab Anim Dis Control & Breeding, Jinan 250100, Peoples R China

12.Yangzhou Univ, Coll Vet Med, Yangzhou 225009, Peoples R China

13.Justus Liebig Univ Giessen, Fac Vet Med, Inst Vet Food Sci, D-35392 Giessen, Germany

14.Univ Paris Cite, Inst Pasteur, Unite Bacteries Pathogenes Enter, F-75724 Paris, France

15.Univ Surrey, Sch Vet Med, Guildford GU2 7AL, England

16.Univ Chinese Acad Sci, Hangzhou Inst Adv Study, Sch Life Sci, Hangzhou 310024, Peoples R China

17.Chinese Acad Sci, Shanghai Inst Biol Sci, Inst Plant Physiol & Ecol, CAS,Key Lab Synthet Biol, Shanghai 200031, Peoples R China

18.Fudan Univ, Sch Life Sci, Dept Microbiol & Microbial Engn, Shanghai 200433, Peoples R China

19.Zhejiang Univ, State Key Lab Diag & Treatment Infect Dis, Natl Clin Res Ctr Infect Dis, Natl Med Ctr Infect Dis,Affiliated Hosp 1,Coll Med, Hangzhou 310003, Peoples R China

20.Zhejiang Prov Key Lab Prevent Vet Med, Hangzhou 310058, Peoples R China

关键词: Salmonella; host adaptation; pathogenic evolution; virulence evolution; vertical transmission; fimbrial adhesin

期刊名称:NATIONAL SCIENCE REVIEW ( 影响因子:20.6; 五年影响因子:22.3 )

ISSN: 2095-5138

年卷期: 2023 年 10 卷 10 期

页码:

收录情况: SCI

摘要: Understanding changes in pathogen behavior (e.g. increased virulence, a shift in transmission channel) is critical for the public health management of emerging infectious diseases. Genome degradation via gene depletion or inactivation is recognized as a pathoadaptive feature of the pathogen evolving with the host. However, little is known about the exact role of genome degradation in affecting pathogenic behavior, and the underlying molecular detail has yet to be examined. Using large-scale global avian-restricted Salmonella genomes spanning more than a century, we projected the genetic diversity of Salmonella Pullorum (bvSP) by showing increasingly antimicrobial-resistant ST92 prevalent in Chinese flocks. The phylogenomic analysis identified three lineages in bvSP, with an enhancement of virulence in the two recently emerged lineages (L2/L3), as evidenced in chicken and embryo infection assays. Notably, the ancestor L1 lineage resembles the Salmonella serovars with higher metabolic flexibilities and more robust environmental tolerance, indicating stepwise evolutionary trajectories towards avian-restricted lineages. Pan-genome analysis pinpointed fimbrial degradation from a virulent lineage. The later engineered fim-deletion mutant, and all other five fimbrial systems, revealed behavior switching that restricted horizontal fecal-oral transmission but boosted virulence in chicks. By depleting fimbrial appendages, bvSP established persistent replication with less proinflammation in chick macrophages and adopted vertical transovarial transmission, accompanied by ever-increasing intensification in the poultry industry. Together, we uncovered a previously unseen paradigm for remodeling bacterial surface appendages that supplements virulence-enhanced evolution with increased vertical transmission.

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