Unveiling a cost of mutualism involving insect-endosymbiont-microbe interactions

Microbe-microbe interactions – of central importance in biological systems – can be antagonistic or synergistic, acting to benefit or detriment of a host. Pederin-producing endosymbionts (PPE) are considered protective mutualists in their Paederus fuscipes (rove beetle) hosts but little is known about whether PPE affect other aspects of host fitness as well as host microbial diversity. We find strong deleterious costs of PPE infections on hosts related to an extended development time, smaller and shorter lifespan of females, as well as a lower hatching rates of progeny. 16S rRNA data reveal that PPE affect the microbiome of P. fuscipes depending on gender and organ, resulting in a decrease in the number of the potentially beneficial symbiotic bacteria Apibacter and the reproductive manipulator Wolbachia and an increase in the conditional pathogenic bacterium Bartonella. Predicted microbe functions related to metabolism, longevity, immunity and resistibility are enriched in uninfected females, potentially contributing to fitness costs of PPE infections. We further sequence and annotate the first complete genome of PPE and compare the pederin biosynthetic gene cluster (ped) with the pederin family biosynthetic gene cluster from other bacterial-eukaryote symbioses. This study highlights the fitness costs of PPE infections to P. fuscipes, even though the defensive pederin compound produced by PPE helps protect the host. The ecology and evolution of this mutualism is shaped by costs, not just the benefits they confer. Changes in the microbial community within infected rove beetles may mediate the negative impacts of PPE on fitness.