62 / 2024-10-24 09:52:05

A fimbriae loss accelerates the transovarial transmission of Salmonella Pullorum via stealth tactics

Fimbriae, one of the robust bacterial colonization factors, could also serve as pathogen-associated molecular patterns to provoke the host immune response. Salmonella Pullorum (SP) is an avian-specific pathogen causing significant economic loss in many developing countries. SP colonization in the reproductive system of adult hens could result in transovarial or vertical transmission to offspring. Our previous studies have shown that loss of type 1 fimbriae (also known as Fim or fim fimbriae) of SP contributes to enhanced virulence and pathoadaptation in chicks and chicken embryos, and increases survival in antimicrobial egg white and within macrophages, suggesting a preference for transovarial transmission. However, it remains unknown whether Fim adhesin plays a role in reproductive colonization and transovarial transmission. This study shows the reproductive system infection likely initiates from the ovaries, peaking on the 21st day post-infection. A subsequent experiment incorporating artificial insemination and incubation demonstrates that the Δfim mutant exhibits an enhanced and long-term persistence in reproductive tissues, and later, a higher detection rate in the hatched chicks (about three times that of the wild-type strain). Further RT-qPCR analyses reveal that Δfim mutant provokes limited inflammation in reproductive niches by down-regulating the expression of cytokines, chemokines, and Toll-Like Receptor 4 (TLR4), which recognizes Fim as a ligand. The collective RNA-seq and proteomic studying within macrophage response suggested that the TLR/MAPK pathway is significantly suppressed following Fim loss. Notably, Fim loss increases Lactobacillus and Ligilactobacillus abundance among oviducal contents, particularly in magnum, suggesting probiotic bacteria might also reduce inflammation and facilitate SP proliferation, while the causative factors for these changes require further study. Together, we uncover a new stealth tactic that SP deceives the host via fimbriae loss, evades the immune responses and promotes transovarial transmission.