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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. [ABSTRACT FROM AUTHOR]

Insects and bacteria, two of the most widespread groups of organisms on earth, establish diverse symbiotic associations from strict parasitism to obligate mutualism. Mutualistic relationships can be instrumental for insects to adapt and survive, and insects are expected to have evolved ways of facilitating the colonization and proliferation of the symbiotic bacteria. Pederin-producing endosymbionts (PPE) in the rove beetle Paederus fuscipes produce the toxic substance pederin, which provides the beetle with a defense against insect and arachnid predators. Most previous studies on this mutualism have focused on the bacteria, but the molecular basis for its interactions with the beetle host are not known. Here we sequenced and annotated the genome of P. fuscipes, representing the first complete genome sequence of a member of the beetle family Staphylinidae; we found expansions of P450 and GST gene families potentially contributing to the wide distribution of P. fuscipes. By assessing the microbiota of P. fuscipes and FISH visualization, we showed that PPE were the dominant bacterial phylotype in females and were common in female reproductive organs. In addition, we found that immune genes up-regulated in reproductive tissues were hostile to Gram-positive bacteria, but likely provided a favorable environment for the colonization and proliferation of Gram-negative PPE bacteria in female reproductive tissues. This work combining multi-omics with FISH analyses thereby helps to unravel this mutualistic interaction and other mutualistic insect-endosymbiont systems. [ABSTRACT FROM AUTHOR]