Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China.
Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, 430070, China.
Fish Shellfish Immunol. 2023 Nov;142:109166. doi: 10.1016/j.fsi.2023.109166. Epub 2023 Oct 14.
Respiratory structures are crucial for vertebrate survival, as they serve not only to perform gas-exchange processes but also as entry points for opportunistic pathogens. Previous studies have demonstrated that fish contain gill mucosal-associated lymphoid tissue, and harbor a large number of commensal bacteria on their surface and contribute to maintaining fish health. However, by far, very limited information is known regarding the effects of viral infection on gill mucosal immunity and microbiota homeostasis. In this study, we conducted an infection model by bath with infectious hematopoietic necrosis virus (IHNV) and revealed a 27 % mortality rate among rainbow trout in the first two weeks after infection. Moreover, we found that diseased fish with the highest IHNV loads in gills exhibiting severe damage, as well as increased goblet cell counts in both primary lamellae (PL) and secondary lamellae (SL). Additionally, RT-qPCR and RNA-seq analyses revealed that IHNV infection induced a strong innate and adaptive antiviral immune responses. Interestingly, an antibacterial immune response was also observed, suggesting that a secondary bacterial infection occurred in trout gills after viral infection. Furthermore, 16S rRNA analysis of trout gills revealed a profound dysbiosis marked by a loss of beneficial taxa and expansion of pathobionts following IHNV infection. Overall, our finding demonstrates that IHNV infection induces significant changes of the microbial community in the fish respiratory surface, thus triggering local antiviral and bacterial mucosal immunity.
呼吸结构对脊椎动物的生存至关重要，因为它们不仅用于进行气体交换过程，还是机会性病原体进入的入口。先前的研究表明，鱼类含有鳃粘膜相关淋巴组织，并在其表面栖息着大量共生细菌，有助于维持鱼类健康。然而，迄今为止，对于病毒感染对鳃粘膜免疫和微生物组稳态的影响，我们所了解的信息非常有限。在这项研究中，我们通过水浴感染传染性造血坏死病毒（IHNV）建立了感染模型，在感染后两周内，虹鳟鱼的死亡率达到 27%。此外，我们发现患有 IHNV 负荷量最高的鱼的鳃严重受损，初级鳃片（PL）和次级鳃片（SL）中的杯状细胞计数也增加了。此外，RT-qPCR 和 RNA-seq 分析表明，IHNV 感染诱导了强烈的先天和适应性抗病毒免疫反应。有趣的是，还观察到了抗菌免疫反应，这表明在病毒感染后，虹鳟鱼的鳃中发生了继发性细菌感染。此外，对虹鳟鱼鳃的 16S rRNA 分析表明，IHNV 感染后，微生物群落发生了深刻的失调，有益菌群减少，病原菌扩张。总的来说，我们的发现表明，IHNV 感染会引起鱼类呼吸表面微生物群落的显著变化，从而引发局部抗病毒和细菌粘膜免疫。
