The shrimp C-type lectins modulate intestinal microbiota homeostasis in microsporidia infection

Abstract

Enterocytozoon hepatopenaei (EHP) is abundant in the shrimp hepatopancreas and intestines and can be transmitted through the digestive system. But the relationship between EHP and intestines or gut microbiota is still unclear. In this study, the microbiome and proteome of shrimp Penaeus vannamei intestine were used to analyze the changes of the gut microbiome and the immune protein after EHP infection. Our results showed that EHP infection brought about a marked increase in the proportion of pathogenic bacteria, such as Shigella, Aeromonas, Faecalibacterium, and Streptococcus, suggesting that EHP infection would lead to the increasing of pathogenic bacteria. Proteome results indicated showed that down-regulated proteins were mainly concentrated in immune-related domains such as C-type lectins (CTLs), hemoglobin, and glutathione transferase, suggesting that EHP might lead to a weakening of the innate immunity of shrimp. In shrimp, CTLs can involve in innate immunity by regulating the transcription of various antimicrobial peptides, and directly participate in the inhibition of pathogens through binding and agglutination. On this basis, after successfully cloned and recombination expressed, three down-regulated CTLs (perlucin, mannose receptor 1 and c-type lectin domain family 17 with typical CTL domains) were proved to have binding and agglutinin ability against four pathogenic bacteria (Enterococcus faecalis, Shigella castellani, Salmonella enteritidis, Aeromonas hydrophila). These results suggested that EHP infection led to decrease the expression of three CTLs and increase secondary infection caused by pathogenic bacteria. And CTLs played important roles in maintaining the balance of shrimp gut microbiome in microsporidia infection. In a word, these results are helpful for us to better understand the interaction between EHP and intestinal microbiota of P. vannamei and will gain new insights into prevention and control of hepatopancreatic microsporidiosis.