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

文献类型： 外文期刊

第一作者： Zhou, Xiao

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

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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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