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Innate immune priming increases an organism’s survival of a second infection after an initial, non-lethal infection. We usedDrosophila melanogasterand an insect-derived strain ofEnterococcus faecalisto study transcriptional control of priming. In contrast to other pathogens, the enhanced survival in primed animals does not correlate with decreasedE.faecalisload. Further analysis shows that primed organisms tolerate, rather than resist infection. Using RNA-seq of immune tissues, we found many genes were upregulated in only primed flies, suggesting a distinct transcriptional program in response to initial and secondary infections. In contrast, few genes continuously express throughout the experiment or more efficiently re-activate upon reinfection. Priming experiments in immune deficient mutants revealed Imd is largely dispensable for responding to a single infection but needed to fully prime. Together, this indicates the fly’s innate immune response is plastic—differing in immune strategy, transcriptional program, and pathway use depending on infection history.