Actinobacteria engage in defensive symbioses with several insect taxa, but reports of nutritional contributions to their hosts have been exceptionally rare. Cotton stainers (Dysdercus fasciatus) and red firebugs (Pyrrhocoris apterus) (both Hemiptera, Pyrrhocoridae) harbour the actinobacterial symbionts Coriobacterium glomerans and Gordonibacter sp. as well as Firmicutes (Clostridium sp. and Lactococcus sp.) and Proteobacteria (Klebsiella sp. and a Rickettsiales bacterium) in the M3 region of their mid-gut. We combined experimental manipulation with community-level analyses to elucidate the function of the gut symbionts in both pyrrhocorid species. Elimination of symbionts by egg-surface sterilization resulted in significantly higher mortality and reduced growth rates, indicating that the microbial community plays an important role for host nutrition. Fitness of symbiont-deprived bugs could be completely restored by re-infection with the original microbiota, while reciprocal cross-infections of microbial communities across both pyrrhocorid species only partially rescued fitness, demonstrating a high degree of host–symbiont specificity. Community-level analyses by quantitative PCRs targeting the dominant bacterial strains allowed us to link the observed fitness effects to the abundance of the two actinobacterial symbionts. The nutritional mutualism with Actinobacteria may have enabled pyrrhocorid bugs to exploit Malvales seeds as a food source and thereby possibly allowed them to occupy and diversify in this ecological niche.
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