Endosymbiotic Fungal Diversity and Dynamics of the Brown Planthopper across Developmental Stages, Tissues, and Sexes Revealed Using Circular Consensus Sequencing

Simple Summary The brown planthopper (BPH, Nilaparvata lugens Stal) is the most destructive pest in rice. Understanding the endosymbiont communities hosted by this insect is a prerequisite for controlling BPH rice infestations. This study reveals the diversity and dynamics of endosymbiotic fungi in the developmental stages and various tissues of BPH by means of circular consensus sequencing (CCS), and we found three dominant yeast-like symbionts (YLSs) in almost all samples and the significant biomarkers between female and male adults. This suggests that these endosymbionts are necessary for BPH survival. This study provides a comprehensive survey of symbiotic fungi in the BPH and offers new strategies for pest management in rice.Abstract Endosymbiotic fungi play an important role in the growth and development of insects. Understanding the endosymbiont communities hosted by the brown planthopper (BPH; Nilaparvata lugens Stal), the most destructive pest in rice, is a prerequisite for controlling BPH rice infestations. However, the endosymbiont diversity and dynamics of the BPH remain poorly studied. Here, we used circular consensus sequencing (CCS) to obtain 87,131 OTUs (operational taxonomic units), which annotated 730 species of endosymbiotic fungi in the various developmental stages and tissues. We found that three yeast-like symbionts (YLSs), Polycephalomyces prolificus, Ophiocordyceps heteropoda, and Hirsutella proturicola, were dominant in almost all samples, which was especially pronounced in instar nymphs 4-5, female adults, and the fat bodies of female and male adult BPH. Interestingly, honeydew as the only in vitro sample had a unique community structure. Various diversity indices might indicate the different activity of endosymbionts in these stages and tissues. The biomarkers analyzed using LEfSe suggested some special functions of samples at different developmental stages of growth and the active functions of specific tissues in different sexes. Finally, we found that the incidence of occurrence of three species of Malassezia and Fusarium sp. was higher in males than in females in all comparison groups. In summary, our study provides a comprehensive survey of symbiotic fungi in the BPH, which complements the previous research on YLSs. These results offer new theoretical insights and practical implications for novel pest management strategies to understand the BPH-microbe symbiosis and devise effective pest control strategies.