The gut bacterium Serratia marcescens mediates detoxification of organophosphate pesticide in Riptortus pedestris by microbial degradation

Abstract

Organophosphate insecticides have been widely used in agriculture to control insect pests and raised growing problems including insecticide resistance. According to recent studies, microbial symbionts play important roles in developing insecticide resistance. The bean bug Riptortus pedestris is a notorious pest of leguminous crops, harbouring diverse microorganisms in their insect midguts. However, the potential biological roles of many gut‐associated bacteria are largely unknown. In this study, we isolated a bacterial strain from the midgut of R. pedestris and identified it as Serratia marcescens based on its morphological characteristics and the phylogenetic analysis of the 16S rRNA gene sequence. A halo of phosphorus‐solubilizing bacteria was observed on a medium containing lecithin and an organophosphorus insecticide dimethoate. Subsequently, the microbial degradation of dimethoate was determined using Gas Chromatography with Mass Spectroscopy (GC–MS). Further analysis indicated that the S. marcescens contained organophosphorus‐degrading MBL‐fold metallo‐hydrolase gene. Additionally, we discovered that the bacterium could colonize the insect midgut stably and enhance the host survivorship when exposed to dimethoate. Our results revealed that an insect gut‐associated bacterium could degrade organophosphorus compounds, thereby reducing related insecticide toxicity to the insect hosts. These findings provided further insights into the host‐microbiota interactions underpinning the development of insecticide resistance.

Symbiotic bacteria confer insecticide resistance by metabolizing buprofezin in the brown planthopper, Nilaparvata lugens (Stål)

“…Most symbionts that mediate the detoxification of pesticides are facultative symbionts [ 7 , 8 , 41 ] that are acquired from the environment. Although previous studies have reported that diverse microorganisms from the environment, including bacteria from the Paracoccus , Pseudomonas , Rhodococcus , and Bacillus genera have the capacity to degrade buprofezin as their sole source of carbon and energy for growth [ 17 , 19 , 42 , 43 ], none of these bacteria were linked to buprofezin-resistance in our study.…”

“…pedestris has shown that S . marcescens can utilize the herbicide atrazine and the insecticide dimethoate respectively as the sole carbon resources for growth and enhance host resistance to these compounds [ 6 , 41 ]. In addition, research on buprofezin resistance in the small brown planthopper infected with S .…”

“…Together, these results provide unequivocal evidence that Bup_Serratia has the capacity to directly metabolize buprofezin and confer resistance to this compound in N. lugens. Most symbionts that mediate the detoxification of pesticides are facultative symbionts [7,8,41] that are acquired from the environment. Although previous studies have reported that…”

“…sole carbon resources for growth and enhance host resistance to these compounds [6,41]. In addition, research on buprofezin resistance in the small brown planthopper infected with S. marcescens provided initial evidence that this bacterial strains may enhance resistance in this pest [49].…”

The ncRNA-mediated regulatory networks of defensins and lysozymes in Riptortus pedestris: involvement in response to gut bacterial disturbances

“…The bean bug, Riptortus pedestris (Hemiptera: Alydidae), is a major agricultural pest that is widely distributed in East Asia, such as South Korea, Japan, and China, resulting in significant yield losses and low seed quality of soybean (Glycine max), which is an important oil and cash crop (Shan et al, 2021;Wei et al, 2023). Evaluation of the associations between bean bugs and gut bacteria was performed in R. pedestris (Jang et al, 2023;Wei et al, 2023;Xia et al, 2023). For example, a specific gut bacterial symbiont, Caballeronia insecticola (Burkholderia insecticola), promoted the proliferation of stem cells and simultaneously inhibited apoptosis at the tip of gut crypts in R. pedestris (Jang et al, 2023).…”