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Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp
oleh: Ping-Ping Liu, Zhe Wei, Zi-Hua Cheng, Xian-Wei Wang
Format: | Article |
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Diterbitkan: | Public Library of Science (PLoS) 2022-11-01 |
Deskripsi
Small antibacterial effectors, including lysozymes, lectins, and antimicrobial peptides, are key regulators of intestinal immunity. However, whether there is coordination among them during regulation is an interesting, but largely unknown, issue. In the present study, we revealed that small effectors synergistically regulate peptidoglycan-derived intestinal immunity in the kuruma shrimp, Marsupenaeus japonicus. A C-type lysozyme (LysC) was screened as a responsive factor for the intestine-bacteria interaction. LysC functions to restrict intestinal bacteria, mainly by cleaving Photobacterium damselae peptidoglycan to generate muropeptides which are powerful stimulators that induce anti-lipopolysaccharides factor B1 (AlfB1), an effective bactericidal peptide. The muropeptides also induce a C-type lectin (Ctl24), which recognizes peptidoglycan and coats bacteria. By counteracting LysC-mediated muropeptide release and AlfB1’s bactericidal activity, Ctl24 prevents the continuous elimination of intestinal bacteria. Therefore, this study demonstrates a mechanism by which small immune effectors coordinate to achieve intestinal homeostasis, and provides new insights into peptidoglycan-derived intestinal immunity in invertebrates. Author summary Intestinal homeostasis largely determines the healthy status of metazoan animals. Uncovering the mechanism for intestinal homeostasis would be helpful to develop new strategies for disease control. In this study, we demonstrated that small immune effectors, including lysozyme, lectin, and bactericidal peptide, collaborate to regulate shrimp intestinal homeostasis in shrimp. Intestinal bacterial peptidoglycan is digested by a lysozyme into muropeptides, which induce the expression of this lysozyme, a bactericidal peptide and a lectin. The former two effectors are able to restrict intestinal bacteria by generating muropeptides and killing bacteria, respectively, while the latter one counteracts their functions. By coating peptidoglycan, this lectin inhibits lysozyme-mediated muropeptides release, and bactericidal peptide-mediated killing of bacteria. Through controlling, but not eliminating intestinal bacteria, these small effectors together achieve a dynamic balance of intestinal bacteria in shrimp. Therefore, this study emphasized the significance of peptidoglycan as the driving force for intestinal homeostasis, and provides insights into generating a healthy intestinal microbiota by utilizing the synergy among small immune effectors.