Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan, 430079, China.
Microbiome. 2023 May 20;11(1):116. doi: 10.1186/s40168-023-01538-6.
The insect hemolymph (blood-equivalent fluid), composed of a large number of hemocytes (blood cells) and a variety of soluble immune effectors, is hostile for pathogens including fungi. In order to survive in the insect hemocoel (body cavity), the entomopathogenic fungus (EPF) has evolved two classical coping strategies, namely evasion and suppression of the host immune reactions. However, it remains unclear whether EPF has other ways of coping with host immunity.
In this study, we demonstrated that Metarhizium rileyi (an EPF) infection by injection of blastospores into the hemocoel enhanced the plasma antibacterial activity of cotton bollworm (Helicoverpa armigera), which was partially due to the enhanced expression of antimicrobial peptides (AMPs). The early stage of M. rileyi infection induced the translocation of gut bacteria into the hemocoel, where they were subsequently cleared due to the enhanced plasma antibacterial activity. Further, we showed that the enhanced plasma antibacterial activity and AMP expression were attributable to M. rileyi but not the invasive gut bacteria (opportunistic bacteria). Elevated ecdysone (major steroid hormone in insects) levels in the hemolymph at 48 h post-M. rileyi infection might contribute to the enhanced expression of AMPs. The fungus-elicited AMPs, such as cecropin 3 or lebocin, exhibited potent inhibitory activity against the opportunistic bacteria but not against hyphal bodies. In addition, the opportunistic bacteria competed with hyphal bodies for amino acid nutrients.
M. rileyi infection induced the translocation of gut bacteria, and then the fungi activated and exploited its host humoral antibacterial immunity to eliminate opportunistic bacteria, preventing them from competing for nutrients in the hemolymph. Unlike the classical strategies, EPF utilizes to evade or suppress host immunity, our findings reveal a novel strategy of interaction between EPF and host immunity. Video Abstract.
昆虫血淋巴（血液等效液）由大量血细胞（hemocytes）和各种可溶性免疫效应物组成，对真菌等病原体具有敌意。为了在昆虫血腔（体腔）中生存，昆虫病原真菌（EPF）进化出了两种经典的应对策略，即逃避和抑制宿主免疫反应。然而，EPF 是否还有其他应对宿主免疫的方法尚不清楚。
在这项研究中，我们证明了通过将芽生孢子注入血腔来感染玫烟色棒束孢（一种 EPF）会增强棉铃虫（Helicoverpa armigera）的血浆抗菌活性，这部分是由于抗菌肽（AMPs）的表达增强。M. rileyi 感染的早期诱导肠道细菌向血腔转移，由于血浆抗菌活性增强，这些细菌随后被清除。此外，我们表明，增强的血浆抗菌活性和 AMP 表达归因于 M. rileyi 而不是入侵的肠道细菌（机会性细菌）。在 M. rileyi 感染后 48 小时，血液中蜕皮激素（昆虫主要类固醇激素）水平升高可能有助于 AMPs 的表达增强。真菌诱导的 AMPs，如 Cecropin 3 或 lebocin，对机会性细菌表现出强烈的抑制活性，但对菌丝体没有抑制活性。此外，机会性细菌与菌丝体竞争氨基酸营养物质。
M. rileyi 感染诱导肠道细菌转移，然后真菌激活并利用其宿主体液抗菌免疫来消除机会性细菌，防止它们在血淋巴中竞争营养物质。与逃避或抑制宿主免疫的经典策略不同，我们的发现揭示了 EPF 与宿主免疫相互作用的一种新策略。视频摘要。
