A shrimp C-type lectin inhibits proliferation of the hemolymph microbiota by maintaining the expression of antimicrobial peptides

J Biol Chem. 2014 Apr 25;289(17):11779-11790. doi: 10.1074/jbc.M114.552307. Epub 2014 Mar 11.

Abstract

Some aquatic invertebrates such as shrimp contain low albeit stable numbers of bacteria in the circulating hemolymph. The proliferation of this hemolymph microbiota in such a nutrient-rich environment is tightly controlled in healthy animals, but the mechanisms responsible had remained elusive. In the present study, we report a C-type lectin (MjHeCL) from the kuruma shrimp (Marsupenaeus japonicus) that participates in restraining the hemolymph microbiota. Although the expression of MjHeCL did not seem to be modulated by bacterial challenge, the down-regulation of its expression by RNA interference led to proliferation of the hemolymph microbiota, ultimately resulting in shrimp death. This phenotype was rescued by the injection of recombinant MjHeCL, which restored the healthy status of the knockdown shrimp. A mechanistic analysis revealed that MjHeCL inhibited bacterial proliferation by modulating the expression of antimicrobial peptides. The key function of MjHeCL in the shrimp immune homeostasis might be related to its broader recognition spectrum of the hemolymph microbiota components than other lectins. Our study demonstrates the role of MjHeCL in maintaining the healthy status of shrimp and provides new insight into the biological significance of C-type lectins, a diversified and abundant lectin family in invertebrate species.

Keywords: Antimicrobial Peptides; C-type Lectin; Hemolymph Microbiota; Invertebrates; Lectin; Pattern Recognition Receptor; RNA Interference (RNAi); Shrimp.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Anti-Infective Agents / pharmacology*
  • Base Sequence
  • Crustacea
  • DNA Primers
  • Hemolymph / microbiology*
  • Lectins, C-Type / metabolism*
  • Microbiota / drug effects*
  • Peptides / pharmacology*

Substances

  • Anti-Infective Agents
  • DNA Primers
  • Lectins, C-Type
  • Peptides