WSV056-mediated downregulation of PvSMCT1 contributes to immune evasion of white spot syndrome virus in the infection of Penaeus vannamei

Sodium-coupled monocarboxylate transporter 1 (SMCT1) belongs to the solute linked carrier (SLC) gene family SLC5. SMCT1 was first identified from mammalian species playing a major role in the transmembrane transferation a variety of monocarboxylate substrates in a Na+-coupled manner. SMCT1 also functions as a tumor suppressor in a wide range of tissues. The role of SMCT1 in the innate immune system in response to viral pathogen remains unclear. A significant decrease in the transcription of Drosophila SMCT1 homolog CG9657 was observed in the transgenic fly line overexpressing white spot syndrome virus (WSSV) immediate early (IE) protein WSV056. We demonstrated that CG9657 mediated resistance to Drosophila C virus (DCV), a native RNA virus of Drosophila. CG9657 knockdown flies showed increased viral replication and accelerated death after DCV infection. RNA interference of CG9657 led to increased DCV viral load at the cellular level. A novel SMCT1 (PvSMCT1) gene was cloned from Penaeus vannamei to explore if the shrimp SMCT1 gene is involved in WSSV infection resistance. The deduced amino acid sequence of PvSMCT1 contained a conserved SLC5sbd_NIS-SMVT domain characteristic of the SLC5 family. PvSMCT1 expression was evidently reduced by recombinant WSV056 injection or WSSV infection. The WSSV replication and shrimp cumulative mortality increased after PvSMCT1 knockdown. In addition, RNAi of PvSMCT1 significantly suppressed the expression of antimicrobial peptides (AMPs). Results showed that PvSMCT1 exerts a positive effect on the antiviral defense by influencing the expression of AMPs in P. vannamei. However, the IE gene WSV056 may contribute to shrimp immunity avoidance by downregulating PvSMCT1 and, thus favoring viral infection.

Automated summary

Sodium-coupled monocarboxylate transporter 1 (SMCT1) plays a crucial role in the transmembrane transfer of monocarboxylate substrates in cells and also acts as a tumor suppressor in various tissues. This study demonstrates the significance of SMCT1 in the innate immune response against viral pathogens in Drosophila and Penaeus vannamei (whiteleg shrimp).