Lactic acid bacteria modulate the CncC pathway to enhance resistance to β-cypermethrin in the oriental fruit fly

Author:

Zeng Tian12,Fu Qianyan12,Luo Fangyi34,Dai Jian12,Fu Rong12,Qi Yixiang12,Deng Xiaojuan34,Lu Yongyue12,Xu Yijuan12

Affiliation:

1. Guangdong Laboratory for Lingnan Modern Agriculture , Department of Entomology, , Guangzhou 510642 , China

2. South China Agricultural University , Department of Entomology, , Guangzhou 510642 , China

3. Guangdong Provincial Sericulture & Mulberry Engineering Research Center , Guangdong Prov Key Lab of AgroAnimal Genomics & Molecular Breeding, , Guangzhou 510642 , China

4. College of Animal Science, South China Agricultural University , Guangdong Prov Key Lab of AgroAnimal Genomics & Molecular Breeding, , Guangzhou 510642 , China

Abstract

Abstract The gut microbiota of insects has been shown to regulate host detoxification enzymes. However, the potential regulatory mechanisms involved remain unknown. Here, we report that gut bacteria increase insecticide resistance by activating the cap “n” collar isoform-C (CncC) pathway through enzymatically generated reactive oxygen species (ROS) in Bactrocera dorsalis. We demonstrated that Enterococcus casseliflavus and Lactococcus lactis, two lactic acid-producing bacteria, increase the resistance of B. dorsalis to β-cypermethrin by regulating cytochrome P450 (P450) enzymes and α-glutathione S-transferase (GST) activities. These gut symbionts also induced the expression of CncC and muscle aponeurosis fibromatosis. BdCncC knockdown led to a decrease in resistance caused by gut bacteria. Ingestion of the ROS scavenger vitamin C in resistant strain affected the expression of BdCncC/BdKeap1/BdMafK, resulting in reduced P450 and GST activity. Furthermore, feeding with E. casseliflavus or L. lactis showed that BdNOX5 increased ROS production, and BdNOX5 knockdown affected the expression of the BdCncC/BdMafK pathway and detoxification genes. Moreover, lactic acid feeding activated the ROS-associated regulation of P450 and GST activity. Collectively, our findings indicate that symbiotic gut bacteria modulate intestinal detoxification pathways by affecting physiological biochemistry, thus providing new insights into the involvement of insect gut microbes in the development of insecticide resistance.

Funder

National Key R&D Program of China

Laboratory of Lingnan Modern Agriculture Project

Publisher

Oxford University Press (OUP)

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