Haase D*, Rieger JK*, Witten A, Stoll M, Bornberg-Bauer E, Kalbe M and Reusch TBH
Immunity comes first: The effect of parasite genotypes to adaptive immunity and immunization in three-spined sticklebacks
Development and Comparative Immunology, 2016

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While innate immune responses in vertebrates are the first line of defense against invading pathogens, adaptive immunity confers memory and thus increased resistance to certain pathogens upon re-infection. But the transition from innate to adaptive immunity and the underlying gene expression patterns of repeated exposure to specific parasite genotypes is poorly understood. In this study, we investigated the effects of consecutive infections with distinct clonal lineages of the eye fluke Diplostomum pseudospathaceum on gene expression patterns in three-spined sticklebacks (Gasterosteus aculeatus). We sequenced the transcriptome of gill and head kidney tissue from 57 individuals, subjected to homologous and heterologous exposures of genetically distinct parasite lineages. Thus we were able to investigate the relative contributions of immunization, the fortification against parasite derived agents, and final exposure on gene expression patterns of adaptive immunity in sticklebacks. Upon parasite exposure, 690 genes in gill and 585 in head kidney tissue were differentially expressed compared to unexposed controls. Multidimensional scaling showed that observable differences are largely attributable to final exposures. Pre-exposure to multiple genotypes showed a diversification of gene expression from both mono-clonal parasite genotypes which displayed no detectable differences to each other. However, we were not able to identify a transcription pattern characteristic for a general response to repeated infections with D. pseudospathaceum. Heterologous pre-exposures subjected to the same final treatment showed no overlap in expression of immune genes. Interestingly, heterologous final exposures indicated similarities between different treatment groups subjected to homologous pre-exposure. The observed pattern is supported by parasite infection rates, which show similar immunization effects over all treatments. Our findings suggest that host immunization is optimized towards an adaptive immune response that favours effectiveness against a large variety of genetic parasite diversity over specificity.