Department of Food Science, Cornell Universitygrid.5386.8, Ithaca, New York, USA.
mSystems. 2022 Jun 28;7(3):e0011522. doi: 10.1128/msystems.00115-22. Epub 2022 Apr 25.
Salmonella is one of the most successful foodborne pathogens worldwide, owing in part to its ability to colonize or infect a wide range of hosts. Salmonella serovars are known to encode a variety of different fimbriae (hairlike organelles that facilitate binding to surfaces); however, the distribution, number, and sequence diversity of fimbriae encoded across different lineages of Salmonella were unknown. We queried whole-genome sequence (WGS) data for 242 Salmonella enterica subsp. (subspecies ) isolates from the top 217 serovars associated with isolation from humans and agricultural animals; this effort identified 2,894 chaperone-usher (CU)-type fimbrial usher sequences, representing the most conserved component of CU fimbriae. On average, isolates encoded 12 different CU fimbrial ushers (6 to 18 per genome), although the distribution varied significantly ( = 1.328E-08) by phylogenetic clade, with isolates in section Typhi having significantly fewer fimbrial ushers than isolates in clade A2 (medians = 10 and 12 ushers, respectively). Characterization of fimbriae in additional non- subspecies genomes suggested that 8 fimbrial ushers were classified as being unique to subspecies isolates, suggesting that the majority of fimbriae were most likely acquired prior to the divergence of subspecies . Characterization of mobile elements suggested that plasmids represent an important vehicle facilitating the acquisition of a wide range of fimbrial ushers, particularly for the acquisition of fimbriae from other Gram-negative genera. Overall, our results suggest that differences in the number and type of fimbriae encoded most likely reflect differences in phylogenetic clade rather than differences in host range. Fimbriae of the CU assembly pathway represent important organelles that mediate Salmonella's interactions with host tissues and abiotic surfaces. Our analyses provide a comprehensive overview of the diversity of CU fimbriae in Salmonella spp., highlighting that the majority of CU fimbriae are distributed broadly across multiple subspecies and suggesting that acquisition most likely occurred prior to the divergence of subspecies . Our data also suggest that plasmids represent the primary vehicles facilitating the horizontal transfer of diverse CU fimbriae in Salmonella. Finally, the observed high sequence similarity between some ushers suggests that different names may have been assigned to closely related fimbrial ushers that likely should be represented by a single designation. This highlights the need to establish standard criteria for fimbria classification and nomenclature, which will also facilitate future studies seeking to associate virulence factors with adaptation to or differences in the likelihood of causing disease in a given host.
沙门氏菌是全球最成功的食源性病原体之一，部分原因是它能够在广泛的宿主中定植或感染。沙门氏菌血清型已知编码多种不同的菌毛（有助于与表面结合的毛发状细胞器）；然而，沙门氏菌不同谱系中编码的菌毛的分布、数量和序列多样性尚不清楚。我们查询了来自与人类和农业动物分离相关的前 217 种血清型的 242 株肠沙门氏菌亚种（亚种）分离株的全基因组序列（WGS）数据；这项工作确定了 2894 个伴侣蛋白-usher（CU）型菌毛usher 序列，代表了 CU 菌毛最保守的成分。平均而言，分离株编码 12 种不同的 CU 菌毛usher（每个基因组 6 到 18 种），尽管分布差异显著（= 1.328E-08），按系统发育分支聚类，伤寒血清型分离株的菌毛usher 明显少于 A2 聚类（中位数分别为 10 和 12 个菌毛usher）。在其他非亚种基因组中的菌毛特征表明，8 个菌毛usher 被归类为仅存在于亚种分离株中，这表明大多数菌毛很可能是在亚种分离之前获得的。移动元件的特征表明，质粒是促进广泛菌毛usher 获得的重要载体，特别是从其他革兰氏阴性菌属获得菌毛。总体而言，我们的结果表明，编码的菌毛数量和类型的差异很可能反映了系统发育分支的差异，而不是宿主范围的差异。CU 组装途径的菌毛代表了介导沙门氏菌与宿主组织和非生物表面相互作用的重要器官。我们的分析提供了沙门氏菌 CU 菌毛多样性的全面概述，突出表明大多数 CU 菌毛广泛分布于多个亚种中，并表明获得菌毛很可能发生在亚种分离之前。我们的数据还表明，质粒是促进沙门氏菌中不同 CU 菌毛水平转移的主要载体。最后，一些 usher 之间的高序列相似性表明，可能已经为密切相关的菌毛 usher 分配了不同的名称，这些 usher 可能应该由单个名称表示。这突出表明需要建立菌毛分类和命名的标准准则，这也将有助于未来的研究将毒力因子与在特定宿主中适应或导致疾病的可能性相关联。
