Endosymbionts can profoundly affect the nutrition, immunity, development, and reproduction of insect hosts, but the effects of multiple endosymbiont infections on microbiota and the interaction of these effects with insect host fitness are not well known. By establishing S. furcifera lines with different endosymbiont infection status, we found that Cardinium and the combined Cardinium + Wolbachia infections differentially reduced bacterial diversity as well as changing bacterial community structure and affecting metabolism, which may connect to negative fitness effects of the endosymbionts on their host.

Symbiotic microorganisms in invertebrates play vital roles in host ecology and evolution. Cardinium, a common intracellular symbiont, is transinfected into the important agricultural pest Nilaparvata lugens (rice brown planthopper) to regulate its reproduction, but how this impacts its microbial community is unknown. Here, we characterized the bacterial microbiota from N. lugens, with or without Cardinium, at different developmental stages and in various adult tissues using 16S rRNA gene sequencing. Upon infection with Cardinium, we found that microbial diversity in the different developmental stages of N. lugens (especially females), and in female midguts and male testes, was lower than in the uninfected control. There was a negative correlation between Cardinium and most related genera and between Bacteroidetes and Proteobacteria. Although the microbial structure varied during Cardinium infection, Acinetobacter spp. was a core microbiome genus. The Cardinium infection enhanced the relative density of midgut-associated Acinetobacter spp., with both bacteria exhibiting tissue-specific tropism. In addition, this infection caused the changes of main microbial functions in N. lugens. These results offer insights into the effects of alien (i.e. newly-introduced from other organism) Cardinium infection on N. lugens-associated microbiotas, aiding in the development of transinfected endosymbionts for pest control.

In this study we established aCardinium-infectedN. lugensline that possessed complete maternal transmission.Cardiniumhad a widespread distribution in tissues ofN. lugens, and this infection decreased the fecundity and hatching rate of the host. Our findings emphasize the feasibility of transinfection ofCardiniumin insects, which expands the range of endosymbionts that could be manipulated for pest control.