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Beneficial gut bacteria can enhance herbivorous arthropod adaptation to plant secondary compounds (PSMs), and specialist herbivores provide excellent examples of this. Tea saponin (TS) of Camellia oleifera is triterpenoids toxic to seed-feeding weevil pest, Curculio chinensis (CW). Previous studies disclosed that Acinetobacter, which was specific enriched in the CW's gut, was involved in helping CW evade TS toxicity of C. oleifera . However, it is still not clear whether Acinetobacter is associated with other anti-insect compounds, and the molecular mechanism of Acinetobacter degradation of TS has not been clarified. To address these questions, we explored the relationship between host plant toxin content and Acinetobacter of CW gut bacteria. Results demonstrated that TS content significantly affected the CW gut microbiome structure and enriched bacteria functional for TS degradation. We further isolated Acinetobacter strain and conducted its genome and transcriptome analyses for bacterial characterization and investigation on its role in TS degradation. Biological tests were carried out to verify the ability of the functional bacterium within CW larvae to detoxify TS. Our results showed that TS-degrading bacteria strain (Acinetobacter sp. AS23) genome contains 47 genes relating to triterpenoids degradation. The AS23 strain improved the survival rate of CW larvae, and the steroid degradation pathway could be the key one for AS23 to degrade TS. This study provides the direct evidence that gut bacteria mediate adaptation of herbivorous insects to phytochemical resistance. IMPORTANCE Microorganism is directly exposed to the plant toxin environment and play a crucial third party in herbivores gut. Although previous studies have proved the existence of gut bacteria that help CWs degrade TS, the specific core flora and its function have not been explored. In this study, we investigated the correlation between the larva gut microbiome and plant secondary metabolites. Acinetobacter genus was the target flora related to TS degradation. There were many terpenoids genes in Acinetobacter sp. AS23 genome. Results of transcriptome analysis and biological tests suggested that steroid degradation pathway be the key pathway of AS23 to degrade TS. This study not only provides direct evidence that gut microbes mediate the rapid adaptation of herbivorous insects to phytochemical resistance, but also provides a theoretical basis for further research on the molecular mechanism of intestinal bacteria cooperating with pests to adapt to plant toxins.

Fast-growing bamboo may be a source of high-quality cellulose with the potential to contribute to energy sustainability, if an efficient and low-cost solution to bamboo cellulose decomposition can be developed. This study compared the gut microbiomes of rhinoceros beetle ( Trypoxylus dichotomus ) feeding on bamboo and wood fiber. The results revealed that diet has a distinctive effect on microbial composition in the midgut, including its most abundant microorganisms that in the fermentation and chemoheterotroph pathways. After identifying the 13 efficient bacterial isolates, we constructed a natural bacterial system based on the microbial relative abundance and an artificial bacterial system with equal proportions of each isolate to catabolize bamboo lignocellulose. The isolate Enterobacter sp. AZA_4_5 and the natural system showed higher degradation efficiency than other single strains or the artificial system. The results can thus serve as important reference for further research and development of a synthetic bacterial consortium to maximize lignocellulolytic ability. IMPORTANCE Bamboo produces a great yield of lignocellulosic biomass due to its high efficiency in carbon fixing. The gut microbiome of Trypoxylus dichotomus differed between bamboo and wood fiber diets. The lignocellulosic pathways were enriched in the gut bacteria of the bamboo diet. The highly efficient bacterial isolates were identified from midgut, whereas the natural bacterial system as well as one isolate showed the higher degradation efficiency of bamboo lignocellulose. The results indicate that the gut bacteria could provide an effective system to utilize the bamboo lignocellulosic biomass.

Plant secondary metabolites (PSMs) can affect the structures and functions of soil microbiomes. However, the core bacteria associated with PSMs, and their corresponding functions have not been explored extensively. In this study, soil physicochemical properties, tea saponin (TS) contents, microbial community compositions, and microbial community functions of different-age Camellia oleifera plantation soils from representative regions were analyzed. We evaluated the effects of plantation age increase on PSM accumulation, and the subsequent consequences on the structures and functions of soil microbiomes. Plantation ages increase positively correlated with accumulated TS contents, negative effects on soil physicochemical properties, and soil microbiome structures and functions. Clearly, the core functions of soil microbiomes transitioned to those associated with PSM metabolisms, while microbial pathways involved in cellulose degradation were inhibited. Our study systematically explored the influences of PSMs on soil microbiomes via the investigation of key bacterial populations and their functional pathways. With the increase in planting years, increased TS content simplified soil microbiome diversity, inhibited the degradation of organic matter, and enriched the genes related to the degradation of TS. These findings significantly advance our understanding on PSMs-microbiome interactions and could provide fundamental and important data for sustainable management of Camellia plantations. IMPORTANCE Plant secondary metabolites (PSMs) contained in plant litter will be released into soil with the decomposition process, which will affect the diversity and function of soil microbiomes. The response of soil microbiomes to PSMs in terms of diversity and function can provide an important theoretical basis for plantations to put forward rational soil ecological management measures. The effects of planting years on PSM content, soil physicochemical properties, microbial diversity, and function, as well as the interaction between each index in Camellia oleifera plantation soil are still unclear. We found that, with planting years increased, the accumulation of tea saponin (TS) led to drastic changes in the diversity and function of soil microbiomes, which hindered the decomposition of organic matter and enriched many genes related to PSM degradation. We first found that soil bacteria, represented by Acinetobacter, were significantly associated with TS degradation. Our results provide important data for proposing rational soil management measures for pure forest plantations.