What doesn’t kill you makes you live longer – Longevity of a social host linked to parasite proteins

Parasites with complex lifecycles are known to manipulate the phenotype of their intermediate hosts to increase the probability of transmission to their definitive hosts. Anomotaenia brevis, a cestode that uses Temnothorax nylanderi ants as intermediate hosts, extends the lifespan of these hosts several fold and changes their behaviour, morphology, and colouration. The mechanisms behind these changes are unknown, as is whether the increased longevity is achieved through manipulation of the parasite. Here we show that the prolonged lifespan of infected ants is probably due to the secretion of antioxidants and possibly novel substances by the parasite. These parasitic proteins make up a substantial portion of the host haemolymph proteome, and thioredoxin peroxidase and superoxide dismutase, two antioxidants, exhibited the highest abundances among them. The largest part of the secreted proteins could not be annotated, indicating they are either novel or severely altered during recent coevolution to function in host manipulation. We found not only secreted proteins, but also shifts in the host proteome, in particular an overabundance of vitellogenin-like A in infected ants, a protein that regulates division of labour in Temnothorax ants, which fits the observed behavioural changes. Our results thus point at two different strategies that are likely employed by this parasite to manipulate its host – by secretion of proteins with immediate influence on the host’s phenotype and by altering the host’s translational activity. Our results reveal the intricate molecular interplay required to influence host phenotype and shed light on potential signalling pathways and genes.