An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph
Abstract Background 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) ha...
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-023-01538-6 |
| _version_ | 1797822766092648448 |
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| author | Jia-Lin Wang Jing Sun Ya-Jing Song Huan-Huan Zheng Gui-Jie Wang Wen-Xia Luo Li Li Xu-Sheng Liu |
| author_facet | Jia-Lin Wang Jing Sun Ya-Jing Song Huan-Huan Zheng Gui-Jie Wang Wen-Xia Luo Li Li Xu-Sheng Liu |
| author_sort | Jia-Lin Wang |
| collection | DOAJ |
| description | Abstract Background 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. Results 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. Conclusions 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 |
| first_indexed | 2024-03-13T10:14:00Z |
| format | Article |
| id | doaj.art-d953feacef874e85870be01c8be187a6 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-13T10:14:00Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-d953feacef874e85870be01c8be187a62023-05-21T11:21:31ZengBMCMicrobiome2049-26182023-05-0111111810.1186/s40168-023-01538-6An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymphJia-Lin Wang0Jing Sun1Ya-Jing Song2Huan-Huan Zheng3Gui-Jie Wang4Wen-Xia Luo5Li Li6Xu-Sheng Liu7Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityHubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityHubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityHubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityHubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityHubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityHubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityHubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal UniversityAbstract Background 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. Results 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. Conclusions 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 Abstracthttps://doi.org/10.1186/s40168-023-01538-6Entomopathogenic fungusAntimicrobial peptideGut microbiotaCompetitionHelicoverpa armigera |
| spellingShingle | Jia-Lin Wang Jing Sun Ya-Jing Song Huan-Huan Zheng Gui-Jie Wang Wen-Xia Luo Li Li Xu-Sheng Liu An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph Microbiome Entomopathogenic fungus Antimicrobial peptide Gut microbiota Competition Helicoverpa armigera |
| title | An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph |
| title_full | An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph |
| title_fullStr | An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph |
| title_full_unstemmed | An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph |
| title_short | An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph |
| title_sort | entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph |
| topic | Entomopathogenic fungus Antimicrobial peptide Gut microbiota Competition Helicoverpa armigera |
| url | https://doi.org/10.1186/s40168-023-01538-6 |
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