Role of gut symbionts of insect pests: A novel target for insect-pest control

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TL;DR

This review examines the diverse roles of gut symbionts in insect pests, including nutrition, immunity, plant defence suppression, and pesticide detoxification. The authors propose that manipulating these symbionts through techniques such as CRISPR/Cas9, RNAi, paratransgenesis, and sterile insect techniques represents a promising eco-friendly alternative to chemical pesticides. The clinical significance lies in developing targeted, sustainable pest management strategies that could reduce the $70 million annual spend on pest control and mitigate associated biodiversity loss.

Full summary

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**Background:** Insects form a highly adaptable group, and their evolutionary success is partly due to associations with gut symbionts. While insects play key roles in pollination, some become pests causing ~40% crop losses annually (FAO). Chemical insecticides are the conventional control method, but environmental concerns, human health risks, and increasing pesticide resistance necessitate alternative strategies. This narrative review focuses on the roles of gut symbionts in insect pests and their potential as targets for eco-friendly pest management.

**Methods:** This is a narrative review synthesizing metagenomics studies (16S rRNA-based) of multiple insect pests, including data from Yong et al. (2017), Tokuda et al. (2018), Bozorov et al. (2019), Gawande et al. (2019), Shah et al. (2020), Asimakis et al. (2021), Deguenon et al. (2021), He et al. (2021), Tegtmeier et al. (2021), Yu et al. (2021), Csorba et al. (2022), Li S. et al. (2022), Majumder et al. (2022), and Wang et al. (2022). The review integrates evidence from functional omics, gene editing studies, and experimental manipulations of symbionts across diverse insect orders.

**Key Results:** The review identifies several critical roles of gut symbionts: (1) Nutrition: Obligate symbionts like Buchnera aphidicola in aphids synthesize essential amino acids and vitamins. In the glassy-wing sharpshooter Homalodisca vitripennis, a symbiotic pair of Sulcia and Baumannia cicadellinicola encodes pathways for all eight essential amino acids plus histidine and methionine. (2) Plant defence suppression: Symbionts such as Hamiltonella defensa in wheat aphids suppress SA and JA defence pathway gene expression. The leaf miner symbiont Wolbachia produces cytokinins that maintain chlorophyll content in apple leaves. (3) Protection against natural enemies: Hamiltonella defensa and Serratia symbiotica in pea aphids restrict parasitoid larval development. Rickettsiella infection in Acyrthosiphon pisum alters body color (red/green) to provide camouflage against predators or parasitoids. (4) Pesticide detoxification: Burkholderia in Riptortus pedestris degrades fenitrothion. Citrobacter sp. in Bactrocera dorsalis produces phosphatase hydrolase that detoxifies trichlorfon. Enterococcus sp. in Plutella xylostella hydrolyzes fenitrothion into less harmful compounds (dimethyl thiophosphate and 3-methyl-4-nitrophenol). (5) Immunity: Snodgrassella alvi and Gilliamella apicola form biofilms in honey bee guts that inhibit pathogen entry. (6) Behavior regulation: Pantoea agglomerans in locusts synthesizes cohesion pheromone. Acetobacter and Lactobacillus in Drosophila influence octopamine levels and aggressive behavior.

**Clinical Implications:** The review proposes several symbiont-targeting strategies for integrated pest management (IPM): (1) Antibiotic elimination of symbionts—tetracycline treatment in Nilaparvata lugens collapsed Wolbachia, Arsenophonus, Acinetobacter, Lactobacillus, and Klebsiella populations, increasing insecticide susceptibility via downregulation of P450 and GST genes. (2) CRISPR/Cas9 gene editing—knockout of the ompA gene in Cedecea neteri using Scarless Cas9 Assisted Recombineering (no-SCAR) strategy resulted in poor biofilm formation in Aedes aegypti gut. (3) Symbiont-mediated RNAi (SMR)—Candidatus Serratia symbiotica, the first facultative endosymbiont cultured on axenic media, has been used to deliver dsRNA targeting host insect genes. (4) Incompatible Insect Technique (IIT) using Wolbachia to induce cytoplasmic incompatibility. (5) Paratransgenesis—genetic modification of Rhodococcus rhodnii in Rhodnius prolixus to reduce insect populations. Challenges include high costs of sterile insect techniques, dsRNA stability and delivery issues for RNAi, and potential off-target effects of CRISPR/Cas9. The authors conclude that suppression of symbionts can hamper host insect nutrition, immunity, and detoxification, potentially leading to partial or complete pest removal with minimal ecological side effects.