One dies, the other survives – A comparison of the early transcriptomic immune responses in zebrafish and rainbow trout infected with Ichthyophthirius multifiliis

Ichthyophthirius multifiliis (Ich) is the causative agent of white spot disease which is associated with high mortality, morbidity, and significant economic losses. While the majority of freshwater fish species are susceptible to the infection the zebrafish exhibits natural resistance. Acute immune responses during early stage infection have been suggested to play a role for the subsequent disease severity. Therefore, this study provides the first comparative transcriptomic investigation of the early gill immune responses to Ich infection in zebrafish (naturally resistant) and rainbow trout (susceptible), which was further supported by real-time qPCR analyses. Zebrafish and rainbow trout were infected with Ich, and gill samples were collected at 2, 24, 48, and 72 hours post-infection (hpi). Zebrafish mounted a rapid response that peaked at 24 hpi, whereas rainbow trout showed a delayed and markedly weaker response. In zebrafish, differentially expressed genes (DEGs) at 24 hpi were linked to six downregulated immune-related pathways; Toll-like, NOD-like, C-type lectin, RIG-I-like receptor signaling pathways, Cytosolic DNA-sensing pathway and Intestinal immune network for IgA production, suggesting a controlled resolution of the response following an early parasite clearance. This was supported by a decrease in Ich genome transcripts in zebrafish indicating disease clearance, whereas transcript numbers increased in rainbow trout indicating disease progression. Upregulation of several cytokines and chemokines in zebrafish, including Cxcl8a, Cxcl11 (24 hpi) and Cxcl13 (48 hpi) highlights the involvement of cellular and mucosal immune mechanisms in early resistance. This study underscores the importance of early immune responses in determining the severity of Ich infection and provide new insights into host–parasite interactions.