Abstract
The development of insecticide resistance in insect pests is a worldwide concern and elucidating the underlying mechanisms is critical for effective crop protection. Recent studies have indicated potential links between insect gut microbiota and insecticide resistance and these may apply to the diamondback moth, Plutella xylostella (L.), a globally and economically important pest of cruciferous crops. We isolated Enterococcus sp. (Firmicutes), Enterobacter sp. (Proteobacteria), and Serratia sp. (Proteobacteria) from the guts of P. xylostella and analyzed the effects on, and underlying mechanisms of insecticide resistance. Enterococcus sp. enhanced resistance to the widely used insecticide, chlorpyrifos, in P. xylostella, while in contrast, Serratia sp. decreased resistance and Enterobacter sp. and all strains of heat-killed bacteria had no effect. Importantly, the direct degradation of chlorpyrifos in vitro was consistent among the three strains of bacteria. We found that Enterococcus sp., vitamin C, and acetylsalicylic acid enhanced insecticide resistance in P. xylostella and had similar effects on expression of P. xylostella antimicrobial peptides. Expression of cecropin was down-regulated by the two compounds, while gloverin was up-regulated. Bacteria that were not associated with insecticide resistance induced contrasting gene expression profiles to Enterococcus sp. and the compounds. Our studies confirmed that gut bacteria play an important role in P. xylostella insecticide resistance, but the main mechanism is not direct detoxification of insecticides by gut bacteria. We also suggest that the influence of gut bacteria on insecticide resistance may depend on effects on the immune system. Our work advances understanding of the evolution of insecticide resistance in this key pest and highlights directions for research into insecticide resistance in other insect pest species.
Highlights
The animal gut is a complicated ecosystem inhabited by a large number of microbes that play important roles in insect physiology and behavior, such as food digestion (Warnecke et al, 2007), host nutrition (Engel et al, 2012), immune response (Ryu et al, 2010), pathogen defense (Dillon et al, 2005), plant specialization (McLean et al, 2011), and mating preference (Sharon et al, 2010)
When we examined the introduction of bacteria into the gut of P. xylostella, we found that all three strains of bacteria increased in abundance compared with the control (Enterococcus sp.: t = 3.43, P = 0.003; Enterobacter sp.: t = 4.00, P = 0.003; and, Serratia sp.: t = 8.24, P < 0.001; Figure 1)
The insecticide resistance bioassay indicated that Enterococcus sp. significantly enhanced insecticide resistance in P. xylostella after 24 h [survival rate: 86.7 ± 15.3% compared to the 63.3 ± 15.3% in the control, F(4, 10) = 8.02, P < 0.05] and 36 h [survival rate: 46.7 ± 5.8% compared to the 23.3 ± 5.8% in the control, F(4, 10) = 8.71, P < 0.05], but Serratia sp. decreased insecticide resistance at 24 h [survival rate: 40.0% ± 10.0% compared to the 63.3 ± 15.3% in the control, P < 0.05], while Enterobacter sp. had no effect [survival rate: 80.0 ± 10.0% compared to the 63.3 ± 15.3% in the control, P = 0.07; Figure 2A]
Summary
The animal gut is a complicated ecosystem inhabited by a large number of microbes that play important roles in insect physiology and behavior, such as food digestion (Warnecke et al, 2007), host nutrition (Engel et al, 2012), immune response (Ryu et al, 2010), pathogen defense (Dillon et al, 2005), plant specialization (McLean et al, 2011), and mating preference (Sharon et al, 2010). It is known that the insect gut microenvironment influences or may even determine the structure of the gut microbial community and the structure and diversity of the gut microbiota, together with their metabolic activities, may have physiological effects in insects (Zilber-Rosenberg and Rosenberg, 2008; Tang et al, 2012). Studies have increasingly suggested links between insect gut microbiota and insecticide resistance (Broderick et al, 2006; Kikuchi et al, 2012; Engel and Moran, 2013; Xia et al, 2013). Some studies have explored the functions of the insect gut microbial communities and how they may contribute to insecticide resistance. In their study of a different symbiont, Cheng et al (2017) reported that trichlorphon-degrading strains of Citrobacter sp. (CF-BD) isolated from the gut of Bactrocera dorsalis (Diptera) increased insecticide resistance
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