Absence of conserved immune signalling pathways and increased pathogen susceptibility associated to photosymbiosis in acoels

Abstract Background Host immunity plays an important role in coral symbiosis with dinoflagellates. Photosymbiosis (the association between hosts and photosynthetic endosymbionts) has evolved multiple times within animals, e.g. within acoels, which are soft-bodied marine invertebrates whose immunity remains so far undescribed. Results Our predicted proteome searches show that acoels lack major signal transduction pathways usually involved in animal immunity. Their loss in acoels predates the occurrence of photosymbiosis in this clade. Immune challenges with the coral pathogen and bleaching agent, Vibrio coralliilyticus, increase acoel mortality and decrease symbiont abundance in adults of the photosymbiotic acoel Convolutriloba macropyga. Mortality in aposymbiotic C. macropyga juveniles or aposymbiotic species Hofstenia miamia is not affected. Ultrastructural studies of immune-challenged animals by transmission electron microscopy show damages at the cellular and organelle level, as well as a degradation of potential pathogens by the host. In situ hybridisation and differential gene expression analysis point to some areas of interaction between pattern recognition receptors and microbes, as well as to the involvement of acoel-specific or uncharacterised genes. Conclusions Based on our findings, photosymbiosis evolution in acoels could have been favoured by the loss of immune signalling pathways. Photosymbiosis in acoels seems to increase susceptibility to pathogen exposure and is disrupted by pathogens. Our data also suggests phagocytosis of pathogens and the possibility of a novel molecular immune response specific to acoels.