Transcriptomic insights into detoxification and mitochondrial responses of Tribolium castaneum (Coleoptera: Tenebrionidae) to carbonyl sulfide exposure

Abstract

Carbonyl sulfide (COS) is a novel grain fumigant effective against several stored-grain pests, including Tribolium castaneum. While COS has demonstrated high toxicity and broad efficacy, the molecular mechanisms underlying COS toxicity remain largely unexplored. In this study, we analyzed the transcriptome in the malpighian tubules and fat body tissues of adult T. castaneum upon COS fumigation. Our analysis identified 3034 and 2973 differentially expressed genes (DEGs) in the malpighian tubules and fat body, respectively. Key DEGs associated with insecticide detoxification, mitochondrial functions, and carbonic anhydrase (CA) activity were significantly expressed between the COS-treated and control groups. Functional annotation and pathway analyzes were performed on these DEGs, and 24 genes were selected for further validation, including those encoding cytochrome P450 (P450s), esterases (ESTs), glutathione-S-transferase (GST), UDP-glucuronosyltransferases (UGTs), ATP-binding cassette transporters (ABCs), ATP synthase, NADH dehydrogenase (NADH), succinate dehydrogenase (SDH), cytochrome c oxidase (COX) and CA enzymes. We analyzed the impact of acetazolamide, a CA inhibitor, on the survival rates of T. castaneum larvae and adults following COS exposure, suggesting that acetazolamide may reduce COS toxicity by inhibiting CA activity. Furthermore, RNA interference (RNAi) was employed to silence the CA3 gene, exploring its role in CA-mediated COS metabolism in T. castaneum. This study presents the first comparative transcriptome investigation of the malpighian tubules and fat body in T. castaneum, enhancing our understanding of the molecular basis of COS toxicity and its potential as an effective alternative for control of this significant storage pest.