Insecticide resistance governed by gut symbiosis in a rice pest, Cletus punctiger, under laboratory conditions

Abstract

Resistance to toxins in insects is generally thought of as their own genetic trait, but recent studies have revealed that gut microorganisms could mediate resistance by detoxifying phytotoxins and man-made insecticides. By laboratory experiments, we here discovered a striking example of gut symbiont-mediated insecticide resistance in a serious rice pest, Cletus punctiger . The rice bug horizontally acquired fenitrothion-degrading Burkholderia through oral infection and housed it in midgut crypts. Fenitrothion-degradation test revealed that the gut-colonizing Burkholderia retains a high degrading activity of the organophosphate compound in the insect gut. This gut symbiosis remarkably increased resistance against fenitrothion treatment in the host rice bug. Considering that many stinkbug pests are associated with soil-derived Burkholderia , our finding strongly supports that a number of stinkbug species could gain resistance against insecticide simply by acquiring insecticide-degrading gut bacteria.

Contribution of insect gut microbiota and their associated enzymes in insect physiology and biodegradation of pesticides

“…Results of this study demonstrated that a rice bug effectively degraded organophosphate fenitrothion by Burkholderia bacterial specie via oral infection and stayed it in the midgut part of the rice bug. The degradation of fenitrothion by the isolating bacterial species from the midgut revealed that gut microbiomes are highly capable of degrading pesticides in insects, and insect gut symbiosis plays a significant role in the development of resistance against fenitrothion in the host rice bug ( Ishigami et al, 2021 ). In another study, the resistance of stored grain products against phosphine fumigation was studied.…”

Eating eggplants as a cucurbit feeder: Dietary shifts affect the gut microbiome of the melon flyZeugodacus cucurbitae(Diptera, Tephritidae)

“…In this context, the insect gut microbiome plays a central role in adaptation to novel host plants as it is of crucial importance for the complex interactions with insect metabolic pathways, which ultimately affect insect fitness (Hammer & Bowers, 2015; Zilber‐Rosenberg & Rosenberg, 2008). The gut microbiome of phytophagous insects can help to (1) break down the complex polysaccharides of the host plant cell wall, and (2) supplement nitrogen, vitamins, and sterols to nutritionally poor diets (Ben‐Yosef et al, 2010, 2014; Douglas, 2009), and (3) detoxify host plant allelochemicals (Hammer & Bowers, 2015) and insecticides (Ishigami et al, 2021; Kikuchi et al, 2012). For example, the symbiotic bacterium “ Candidatus Erwinia dacicola” is essential for the metabolism of larvae of the olive fly Bactrocera oleae (Rossi, 1790) (Diptera, Tephritidae) as it allows them to feed on unripe olives rich in allelochemicals (Ben‐Yosef et al, 2015; Pavlidi et al, 2017).…”

High nitrogen in maize enriches gut microbiota conferring insecticide tolerance in lepidopteran pest Spodoptera litura

“…Members of other gut microbiomes can also degrade insecticides in vitro . For example, degradation test revealed that the gut-colonizing Burkholderia retains a high degrading activity of the organophosphate compound in the gut of rice bug Cletus punctiger ( Ishigami et al., 2021 ). A gut bacteria Lactobacillus plantarum was shown to metabolize organophosphate insecticide chlorpyrifos and may be beneficial to reducing chlorpyrifos toxicity in Drosophila melanogaster ( Daisley et al., 2018 ).…”