Serial comparative transcriptomics reveals dynamic and coordinated immune-metabolic responses in the liver-spleen axis of Oplegnathus punctatus to Edwardsiella piscicida infection.

Abstract

Oplegnathus punctatus is a high-value marine fish in aquaculture, yet its production is severely threatened by pathogen infections such as Edwardsiella piscicida (the old name called as Edwardsiellatarda). Understanding the systemic host response is essential for developing effective control strategies. This study investigated the dynamic and coordinated immune-metabolic reactions in the liver and spleen of O. punctatus following E. piscicida infection. Serial transcriptomic analyses of liver and spleen were conducted at 0, 12, 24, 48, 72 h post-infection (hpi). Results revealed that the spleen initiated rapid innate immune activation at 12 hpi, while the liver underwent persistent metabolic reprogramming and prioritizing protein synthesis while suppressing small-molecule metabolism. Weighted gene co-expression network analysis (WGCNA) further identified time-specific modules, that was, the midnightblue module (12 hpi) in the spleen was enriched for cytokine and pattern recognition receptor pathways, and the white module (72 hpi) in the liver linked metabolic processes with complement cascade. A core set of 218 genes was co-regulated in both tissues, primarily involved in antigen presentation and ubiquitination. These findings demonstrate that the liver and spleen form a functionally integrated immunometabolic axis, which coordinates temporally organized defense against E. piscicida. This work provides novel insights into systemic immunity in teleosts and supports the development of targeted health management strategies to enhance disease resistance in O. punctatus.