Small immune effectors coordinate peptidoglycan-derived immunity to regulate intestinal bacteria in shrimp

PLoS Pathog. 2022 Nov 23;18(11):e1010967. doi: 10.1371/journal.ppat.1010967. eCollection 2022 Nov.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Wall
  • Intestines
  • Lectins, C-Type
  • Penaeidae*
  • Peptidoglycan*

Substances

  • Peptidoglycan
  • Lectins, C-Type

Grants and funding

This work was supported financially by the National Key Research and Development Program of China (2018YFD0900505), the Natural Science Foundation of China (32173008, 31873043, 31622058) to XWW. The funders have no role in the design and conduct of the study, in the collection, analysis, and interpretation of the data, and in the preparation, review, or approval of the manuscript.