Temporal and pathogen-load dependent changes in rainbow trout ( Oncorhynchus mykiss) immune response traits following challenge with biotype 2 Yersinia ruckeri

Abstract

Rainbow trout infected with Yersinia ruckeri, the causative agent of enteric redmouth disease (ERM), produce a pro-inflammatory and acute-phase response attributed in part to the innate recognition of bacterial-produced flagellin. Recently, variants of Y. ruckeri have been identified that lack flagella and associated motility. These strains are classified as biotype 2 (BT2) Y. ruckeri and these are considered an emerging problem in salmonid aquaculture. Little is known about the salmonid immune response to these variants. Herein, we report temporal and quantitative changes in rainbow trout immune response parameters following a primary challenge with BT2 Y. ruckeri strain YRNC10. Fish were injection-challenged with ten-fold dilutions of viable bacteria and sampled on days 1, 3, 5 and 7 post-challenge. TNFα1 and IL1-β1 transcripts were increased by day 1 post-challenge, and on days 3, 5 and 7 maximal gene transcript up-regulation occurred at a threshold of ∼64–256 CFU per mg spleen tissue. Infection induced robust SAA gene up-regulation that was significantly correlated with increased gene expression of IL-1β1 ( r = 0.81, P < 0.0001) and TNFα1 ( r = 0.55, P < 0.0001). Y. ruckeri infection induced modest changes in INFγ and Mx-1 gene transcript abundance at intermediate or high challenge doses and the expression patterns of both genes were positively correlated with pro-inflammatory gene and acute-phase gene transcription patterns. TNF superfamily 13b (BAFF) gene expression was significantly down-regulated in response to infection on days 3, 5 and 7 at the highest challenge doses. The spleen somatic index was significantly increased on days 3, 5 and 7 post-infection and positively correlated with spleen colony forming units and abundance of gene transcripts SAA, TNFα1, and IL1-β1. In summary, rainbow trout had a strong innate response following challenge with BT2 Y. ruckeri strain YRNC10 indicating that flagellin expression is not required for production of a robust pro-inflammatory and acute-phase gene transcription response. This study further supports the use of SAA transcript abundance and spleen somatic index as general measures of immunological status and fish health.