Variability of Gut Microbiota Across the Life Cycle of Grapholita molesta (Lepidoptera: Tortricidae)

Abstract

Grapholita molesta , the oriental fruit moth, is a serious global pest of many Rosaceae fruit trees. Gut microorganisms play important roles in host nutrition, digestion, detoxification, and resistance to pathogens. However, there are few studies on the microbiota of G. molesta , particularly during metamorphosis. Here, the diversity of gut microbiota across the holometabolous life cycle of G. molesta was investigated comprehensively by Illumina high-throughput sequencing technology. The results showed that the microbiota associated with eggs had a high number of operational taxonomic units (OTUs). OTU and species richness in early-instar larvae (first and second instars) were significantly higher than those in late-instar larvae (third to fifth instars). Species richness increased again in male pupae and adults, apparently during the process of metamorphosis, compared to late-instar larvae. Proteobacteria and Firmicutes were the dominant phyla in the gut and underwent notable changes during metamorphosis. At the genus level, gut microbial community shifts from Gluconobacter and Pantoea in early-instar larvae to Enterococcus and Enterobacter in late-instar larvae and to Serratia in pupae were apparent, in concert with host developmental changes. Principal coordinate analysis (PCoA) and linear discriminant analysis effect size (LEfSe) analyses confirmed the differences in the structure of gut microbiota across different developmental stages. In addition, sex-dependent bacterial community differences were observed. Microbial interaction network analysis showed different correlations among intestinal microbes at each developmental stage of G. molesta , which may result from the different abundance and diversity of gut microbiota at different life stages. Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) analysis indicated that most functional prediction categories of gut microbiota were related to membrane transport, carbohydrate and amino acid metabolism, and DNA replication and repair. Bacteria isolated by conventional culture-dependent methods belonged to Proteobacteria, Firmicutes, and Actinobacteria, which was consistent with high-throughput sequencing results. In conclusion, exploration of gut bacterial community composition in the gut of G. molesta should shed light into deeper understanding about the intricate associations between microbiota and host and might provide clues to the development of novel pest management strategies against fruit borers.

Comparison of Gut Bacterial Communities of Grapholita molesta (Lepidoptera: Tortricidae) Reared on Different Host Plants

“…At the phylum level, there were no significant differences in the bacterial composition of G. molesta across the five diets of apples, peaches, nectarines, crisp pears, and peach shoots, but the diversity of gut bacteria was significantly lower than that of the artificial feed and plums. In these five treatments, Proteobacteria was the absolute dominant phylum, and its relative abundances were more than 90%, similar to previous researches [20,31,33]. However, in the two treatment groups that fed on an artificial feed and plums, the following four phyla were dominant: Proteobacteria, Firmicutes, Bacteroidota, and Actinobacteriota.…”

“…Grapholita molesta, known as the oriental fruit moth, is an important fruit tree pest widely distributed in the fruit-growing areas of Asia, Europe, America, Australia, and Africa [17][18][19][20]. It has the characteristic of host shifting.…”

“…Yang et al revealed that the diversity of gut microbes in Plutella xylostella was significantly decreased after the host shifted from radishes to peas and was raised for 17 generations [7]. There have been some studies on the gut microbiota of G. molesta [20,31,33], but as far as we know, there are few reports about the structure of the gut bacterial communities when G. molesta feed on the fruits or young shoots of Rosaceae hosts.…”

Gut Structure and Microbial Communities in Sirex noctilio (Hymenoptera: Siricidae) and Their Predicted Contribution to Larval Nutrition

“…We found that the gut microbial communities were more similar between the female and male adults than that of larvae, indicating that the host developmental stage could influence the microbial community. This result was consistent with studies on Lepidopteran holometabolous insects (Wang et al, 2020). The gut bacterial and fungal community structures and diversity were similar between female and male adults of S. noctilio, which was in agreement with previous findings in Laodelphax striatellus, although Hemiptera is hemimetabolous insect (Bing et al, 2020).…”

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

“…However, a crucial consideration for Lepidoptera and other insects that undergo complete metamorphosis is that microbial associations may change between life stages (10). In Lepidoptera, larvae and adults do often differ in the composition and absolute abundance of their microbiomes (6,(11)(12)(13)(14)(15). Beyond this pattern, however, the ecology of adult-stage microbiomes remains poorly understood.…”