Oral transmission of rock bream iridovirus (RBIV) drives delayed systemic infection and organ specific immune reprogramming in rock bream (Oplegnathus fasciatus).

Abstract

Rock bream iridovirus (RBIV) is a major threat in marine fish aquaculture, but the role of oral transmission in disease progression remains poorly understood. Here, we compared intraperitoneal (i.p.) and oral infection routes in rock bream (Oplegnathus fasciatus) to evaluate viral replication, pathology, and immune responses. Fish infected via the i.p. route showed rapid systemic spread and 100 % mortality within 17-35 days post infection (dpi). In contrast, oral infection caused delayed mortality, occurring 15-20 days later, reflecting the additional mucosal barriers encountered during viral entry. Despite this delay, viral loads in orally infected fish eventually reached levels comparable to those in i.p. infected fish. Hematological and cytological analyses revealed distinct outcomes: i.p. infection rapidly induced anemia and splenic enlarged basophilic cells, whereas oral infection produced delayed blood cell changes and later appearance of atypical basophilic cells. Organ-specific immune gene expression highlighted a clear dichotomy. The head kidney and intestine acted as viral persistence sites, showing strong early innate signaling but suppression of apoptosis. In contrast, the stomach mounted robust late-phase responses, with activation of cytotoxic and apoptosis-related genes. Our findings fill a critical gap in fish iridovirus research by experimentally establishing an oral route to lethal disease and mapping organ-resolved mucosal versus systemic programs, thereby providing actionable baselines for mucosal-targeted surveillance and next-generation oral vaccines.