Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection

Abstract

The crosstalk between the immune system and microbiota drives an amazingly complex mutualistic symbiosis. In mammals, the upper respiratory tract acts as a gateway for pathogen invasion, and the dynamic interaction between microbiota and mucosal immunity on its surface can effectively prevent disease development. However, the relationship between virus-mediated mucosal immune responses and microbes in lower vertebrates remains uncharacterized. In this study, we successfully constructed an infection model by intraperitoneally injecting common carp (Cyprinus carpio) with spring viremia of carp virus (SVCV). In addition to the detection of the SVCV in the nose and pharynx of common carp, we also identified obvious histopathological changes following viral infection. Moreover, numerous immune-related genes were significantly upregulated in the nose and pharynx at the peak of SVCV infection, after which the expression levels decreased to levels similar to those of the control group. Transcriptome sequencing results revealed that pathways associated with bacterial infection in the Toll-like receptor pathway and the Nod-like receptor pathway were activated in addition to the virus-related Rig-I-like receptor pathway after SVCV infection, suggesting that viral infection may be followed by opportunistic bacterial infection in these mucosal tissues. Using 16S rRNA gene sequencing, we further identified an upward trend in pathogenic bacteria on the mucosal surface of the nose and pharynx 4 days after SVCV infection, after which these tissues eventually reached new homeostasis. Taken together, our results suggest that the dynamic interaction between mucosal immunity and microbiota promotes the host to a new ecological state.

Response of immunoglobulin M in gut mucosal immunity of common carp (Cyprinus carpio) infected with Aeromonas hydrophila

“…A previous study demonstrated that Apo A-1 has bacteriostatic activity against A. hydrophila and bactericidal activity against E. coli ( 61 ). Interestingly, apoa-1 and apoa-14 were first downregulated and then upregulated during the infection process, which was consistent with the findings of a previous study in carp infected with SVCV ( 62 ). The expression of apoa-1 and apoa-14 were upregulated in the foregut, midgut, and hindgut of common carp post the second infection.…”

Expression analysis of Igs and mucosal immune responses upon SVCV infection in common carp (Cyprinus carpio L.)

“…At 1, 7, 14, 28 days post infection (dpi), the common carp were anesthetized with MS-222 for sampling as previous study [36] . For histological and pathological studies, skin, gill and gut of common carp were directly taken from control and infected fish, and then fixed immediately at 4% (v/v) neutral buffer paraformaldehyde for at least 24 h. For RNA extraction and qPCR, tissues including gill, skin and gut were collected in Trizol reagent and stored at -80 °C until use.…”