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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.
Highlights
The mucosa of vertebrates is a dynamic environment in which trillions of commensal microorganisms exist, known as the microbiota, which plays an important role in many biological functions including growth enhancement, nutrition, development, and metabolism [1, 2]
Homogenates of nose and pharynx tissues from control and infected fish were filtered, and reinfected epithelioma papillosum cyprini (EPC) cells, obvious cytopathic effects (CPEs), and a certain number of plaques were observed in infected groups EPC cells, whereas no such CPEs and plaques were observed in control groups of EPC cells (Figure 1B)
These results signified that the spring viremia of carp virus (SVCV) infection model of common carp was successfully constructed, and the SVCV can invade into the mucosal tissues of the nose and pharynx and gradually decreases over time
Summary
The mucosa of vertebrates is a dynamic environment in which trillions of commensal microorganisms exist, known as the microbiota, which plays an important role in many biological functions including growth enhancement, nutrition, development, and metabolism [1, 2]. Teleost fish have evolved both innate and adaptive immunity due to evolutionary pressures and can protect themselves against pathogens residing in the aquatic environment and maintain mucosal microbiota homeostasis [2, 5]. Given the uniqueness and complexity of the living environment of teleost, the mucosal tissues on the surface of these organisms are the first to contact the pathogen and are the first line of defense against pathogen invasion. It is worth noting that the innate immune response of the nasal and pharyngeal mucosa plays an important role in defending the host against viral infection. Previous studies demonstrated that both the nasal and pharyngeal mucosa of teleost were involved in immune responses against pathogen invasion. Secondary bacterial infection and the systematic changes of the immune pathways in the nasal and pharyngeal mucosa after virus infection remain uncharacterized
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