Shrimp shapes a resistance trait against vibriosis by memorizing the colonization resistance of intestinal microbiota

PLoS Pathog. 2024 Jul 11;20(7):e1012321. doi: 10.1371/journal.ppat.1012321. eCollection 2024 Jul.

Abstract

Vibriosis is one of the most serious diseases that commonly occurs in aquatic animals, thus, shaping a steady inherited resistance trait in organisms has received the highest priority in aquaculture. Whereas, the mechanisms underlying the development of such a resistance trait are mostly elusive. In this study, we constructed vibriosis-resistant and susceptible families of the Pacific white shrimp Litopenaeus vannamei after four generations of artificial selection. Microbiome sequencing indicated that shrimp can successfully develop a colonization resistance trait against Vibrio infections. This trait was characterized by a microbial community structure with specific enrichment of a single probiotic species (namely Shewanella algae), and notably, its formation was inheritable and might be memorized by host epigenetic remodeling. Regardless of the infection status, a group of genes was specifically activated in the resistant family through disruption of complete methylation. Specifically, hypo-methylation and hyper-expression of genes related to lactate dehydrogenase (LDH) and iron homeostasis might provide rich sources of specific carbon (lactate) and ions for the colonization of S. algae, which directly results in the reduction of Vibrio load in shrimp. Lactate feeding increased the survival of shrimp, while knockdown of LDH gene decreased the survival when shrimp was infected by Vibrio pathogens. In addition, treatment of shrimp with the methyltransferase inhibitor 5-azacytidine resulted in upregulations of LDH and some protein processing genes, significant enrichment of S. algae, and simultaneous reduction of Vibrio in shrimp. Our results suggest that the colonization resistance can be memorized as epigenetic information by the host, which has played a pivotal role in vibriosis resistance. The findings of this study will aid in disease control and the selection of superior lines of shrimp with high disease resistance.

MeSH terms

  • Animals
  • Aquaculture
  • Disease Resistance* / genetics
  • Gastrointestinal Microbiome*
  • Penaeidae* / immunology
  • Penaeidae* / microbiology
  • Vibrio Infections* / immunology
  • Vibrio*

Grants and funding

This study was supported by the Natural Science Foundation of China (Grant 31830100 to FL and 42176105 to JY), the National Key Research & Development Program of China (Grant 2022YFD2400203 to FL), the China Agriculture Research system-48 (Grant CARS-48 to FL), and the Taishan Scholars Program (to FL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.