Soil-derived bacteria endow Camellia weevil with more ability to resist plant chemical defense

Abstract

Background Herbivorous insects acquire their gut microbiota from diverse sources, and these microorganisms play significant roles in insect hosts’ tolerance to plant secondary defensive compounds. Camellia weevil (Curculio chinensis) (CW) is an obligate seed parasite of Camellia oleifera plants. Our previous study linked the CW’s gut microbiome to the tolerance of the tea saponin (TS) in C. oleifera seeds. However, the source of these gut microbiomes, the key bacteria involved in TS tolerance, and the degradation functions of these bacteria remain unresolved. Results Our study indicated that CW gut microbiome was more affected by the microbiome from soil than that from fruits. The soil-derived Acinetobacter served as the core bacterial genus, and Acinetobacter sp. was putatively regarded responsible for the saponin-degradation in CW guts. Subsequent experiments using fluorescently labeled cultures verified that the isolate Acinetobacter sp. AS23 can migrate into CW larval guts, and ultimately endow its host with the ability to degrade saponin, thereby allowing CW to subsist as a pest within plant fruits resisting to higher concentration of defensive chemical. Conclusions The systematic studies of the sources of gut microorganisms, the screening of taxa involved in plant secondary metabolite degradation, and the investigation of bacteria responsible for CW toxicity mitigation provide clarified evidence that the intestinal microorganisms can mediate the tolerance of herbivorous insects against plant toxins.

Functional and Compositional Changes in Sirex noctilio Gut Microbiome in Different Habitats: Unraveling the Complexity of Invasive Adaptation

“…Similar results demonstrating the importance of stochastic processes were also observed in studies on gut microbial communities in Drosophila simulans and Dicranocephalus wallichii bowringi [ 39 ]. Another study also showed that Curculio chinensis gut microbiome was derived from the surrounding environmental microbiome and was more affected by the microbiome from soil than that from fruits [ 40 ]. However, our results demonstrated that both factors contribute to gut microbiome community assembly, which would perhaps be more conducive to S. noctilio spreading colonization.…”

Altitude as a key environmental factor shaping microbial communities of tea green leafhoppers ( Matsumurasca onukii )

“…It was found that higher tiers of endosymbionts (i.e., Wolbachia , Sodalis, and Rickettsia ) were present in weevils at localities with higher temperatures; lower numbers of Wolbachia and Rickettsia were detected in a population found in regions with higher snowfall. Furthermore, microorganisms acquired from the surrounding environment can enhance the fitness of insect hosts ( 4 , 5 ).…”

Specific Enriched Acinetobacter in Camellia Weevil Gut Facilitate the Degradation of Tea Saponin: Inferred from Bacterial Genomic and Transcriptomic Analyses

“…Tea saponin (TS) of Camellia oleifera is triterpenoids that is toxic to seed-feeding weevil pest, Curculio chinensis (CW) ( 2 , 20 , 21 ). The TS content in different insect-resistant C. oleifera clones was negatively correlated with the damage level of CW ( 2 , 20 , 21 ). Studies have shown that over 220 insect species can feed on C. oleifera , and only CW is specialized seed feeder ( 19 , 20 ).…”

“…It was found that Acinetobacter sp. AS23 strain was the dominant strain in the gut microbiome of the surviving larvae with high resistance to host plants, and the abundance of AS23 strain was positively correlated with the TS content of host plants ( 21 ). Traceability analysis showed that the probability of the bacteria coming from soil was as high as 96% ( 21 ).…”

“…AS23 strain was the dominant strain in the gut microbiome of the surviving larvae with high resistance to host plants, and the abundance of AS23 strain was positively correlated with the TS content of host plants ( 21 ). Traceability analysis showed that the probability of the bacteria coming from soil was as high as 96% ( 21 ). However, plants have multiple anti-insect compounds, whether the specific enrichment of Acinetobacter is also related to other compounds.…”