Effects of Host Plant and Insect Generation on Shaping of the Gut Microbiota in the Rice Leaffolder, Cnaphalocrocis medinalis

Abstract

Gut microbes in insects may play an important role in the digestion, immunity and protection, detoxification of toxins, development, and reproduction. The rice leaffolder Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Crambidae) is a notorious insect pest that can damage rice, maize, and other gramineous plants. To determine the effects of host plants and generations on the gut microbiota of C. medinalis, we deciphered the bacterial configuration of this insect pest fed rice or maize for three generations by Illumina MiSeq technology. A total of 16 bacterial phyla, 34 classes, 50 orders, 101 families, 158 genera, and 44 species were identified in C. medinalis fed rice or maize for three generations. Host plants, insect generation, and their interaction did not influence the alpha diversity indices of the gut microbiota of C. medinalis. The dominant bacterial taxa were Proteobacteria and Firmicutes at the phylum level and Enterococcus and unclassified Enterobacteriaceae at the genus level. A number of twenty genera coexisted in the guts of C. medinalis fed rice or maize for three generations, and their relative abundances occupied more than 90% of the gut microbiota of C. medinalis. A number of two genera were stably found in the gut of rice-feeding C. medinalis but unstably found in the gut microbiota of maize-feeding C. medinalis, and seven genera were stably found in the gut of maize-feeding C. medinalis but unstably found in the gut of rice-feeding C. medinalis. In addition, many kinds of microbes were found in some but not all samples of the gut of C. medinalis fed on a particular host plant. PerMANOVA indicated that the gut bacteria of C. medinalis could be significantly affected by the host plant and host plant × generation. We identified 47 taxa as the biomarkers for the gut microbiota of C. medinalis fed different host plants by LEfSe. Functional prediction suggested that the most dominant role of the gut microbiota in C. medinalis is metabolism, followed by environmental information processing, cellular processes, and genetic information processing. Our findings will enrich the understanding of gut bacteria in C. medinalis and reveal the differences in gut microbiota in C. medinalis fed on different host plants for three generations.

Gut bacterial communities and their assembly processing in Cnaphalocrocis medinalis from different geographic sources

“…The structure and diversity of the gut microbiota in C. medinalis vary across the life cycle of C. medinalis ( Yang et al, 2020 ). Recently, we characterized the bacterial structures of C. medinalis fed rice or maize for three generations and found that host plant and host plant × generation might have a substantial effect on C. medinalis intestinal bacteria based on the PERMANOVA ( Yang et al, 2022 ). In this study, 22 bacterial phyla, 56 classes, 84 orders, 138 families, 228 genera, and 299 species were generated in C. medinalis from different geographic sources, including four sites in China, one in Thailand, and one in Vietnam.…”

“…Functional prediction of the gut microbiota revealed that metabolism (70.22–70.53%) was found to be the most functional category in this study, followed by environmental information processing (15.79–17.21%), cellular process (5.29–6.12%), genetic information processing (3.90–4.06%), human diseases (2.32–2.72%), and organismal systems (0.82–0.94%). Likewise, intestinal bacteria in C. medinalis fed different host plants perform metabolism most commonly, followed by environmental information processing, cellular process, and genetic information processing according to functional prediction ( Yang et al, 2022 ). Among the top 20 GO functional pathways, the relative abundances of three pathways in the LS population were significantly higher, and 11 pathways in the LS population were significantly lower than those in the other geographic populations.…”

“…Although microbes differ among the developmental stages of C. medinalis , some microbes, including Enterococcus , can be found across all the C. medinalis stages ( Yang et al, 2020 ). A recent study indicated that the host plant also affects the microbiota of C. medinalis along with the insect generation ( Yang et al, 2022 ). Communication between populations and geography may be the crucial factor affecting the ecological processing of the microbiota in C. medinalis .…”

Plasticity of the Gene Transcriptional Level and Microbiota in the Gut Contributes to the Adaptability of the Fall Armyworm to Rice Plants

“…At the phylum level, Firmicutes, Bacteroidetes, and Proteobacteria were dominant microbial communities in all samples from the G1 generation of both corn and rice strains, which were similar to some other Lepidoptera insects. 44,45 Previous studies have shown that Proteobacteria and Firmicutes contribute to environment adaptation, digestion, nutrient utilization, and energy metabolism. 44,46 At G3 and G5, the gut microbiota of the corn and rice strains displayed significant differentiation.…”

Gut bacterial community of Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Crambidae) is driven by rice varieties

“…Although the characterizations of gut bacteria were comparatively well advanced in humans, ruminants and other arthropods, this is still very limited in insect species (Dillon & Dillon, 2003). Most studies indicated that the composition of insect gut bacterial community was strongly affected by host's diet (Guo et al., 2015; Huang et al., 2021; Li et al., 2022; Yang et al., 2022b). However, the study of Tinker and Ottesen (2016) demonstrated that cockroaches have evolved unique mechanisms for establishing and maintaining a diverse and stable core hindgut microbiome in response to dietary shifts.…”