Unveiling transgenerational effects on Drosophila immunity, the microbiome, and a gut pathogen interaction

In many insects, parents and offspring share the same eco-environment, meaning that the offspring are likely to encounter pathogens similar to those encountered by the parents, and thus the offspring's ability to defend may be influenced in part by the parents' eco-environment, which is modulated by previous pathogen encounters. Furthermore, immunological challenge may also influence the microbiome, and thus altering host physiology. The microbiome's impact on general host physiology is being extensively studied, however, the connections between the microbiome and immunity over generations have received less attention. Here, we use the Drosophila melanogaster model to investigate the transgenerational effects of host immunity, the microbiome, and a gut pathogen interaction. We challenged Drosophila females orally with different doses of Pseudomonas entomophila (Pe), a lethal pathogen due to its inhibition of gut epithelial renewal, which in basal conditions is modulated by the gut microbiota. We found that the Pe challenge in the parents led to a persistence of infection in the offspring, and as such the offspring from previously challenged parents are continuously exposed to Pe. However, these offspring exhibit similar survival after a new Pe challenge, but the offspring experience microbiome remodeling after infection that is dependent on parental treatment. In addition, we explored if parental challenge leads to additional host physiological alterations, including fecundity and the starvation resistance response in offspring. Overall, our results highlight the dynamics of host-pathogen interactions across generations, indicating that infection-induced microbiome disturbance cause additional host physiological alterations.