Insecticide resistance by a host-symbiont reciprocal detoxification

Yuya Sato, Seonghan Jang, Kazutaka Takeshita, Hideomi Itoh, Hideaki Koike, Kanako Tago, Masahito Hayatsu, Tomoyuki Hori and Yoshitomo Kikuchi ()
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Yuya Sato: Environmental Management Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Center
Seonghan Jang: Hokkaido University
Kazutaka Takeshita: Akita Prefectural University
Hideomi Itoh: AIST, Hokkaido Center
Hideaki Koike: AIST, Tsukuba Center
Kanako Tago: Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO)
Masahito Hayatsu: Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO)
Tomoyuki Hori: Environmental Management Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Center
Yoshitomo Kikuchi: Hokkaido University

Nature Communications, 2021, vol. 12, issue 1, 1-8

Abstract: Abstract Insecticide resistance is one of the most serious problems in contemporary agriculture and public health. Although recent studies revealed that insect gut symbionts contribute to resistance, the symbiont-mediated detoxification process remains unclear. Here we report the in vivo detoxification process of an organophosphorus insecticide, fenitrothion, in the bean bug Riptortus pedestris. Using transcriptomics and reverse genetics, we reveal that gut symbiotic bacteria degrade this insecticide through a horizontally acquired insecticide-degrading enzyme into the non-insecticidal but bactericidal compound 3-methyl-4-nitrophenol, which is subsequently excreted by the host insect. This integrated “host-symbiont reciprocal detoxification relay” enables the simultaneous maintenance of symbiosis and efficient insecticide degradation. We also find that the symbiont-mediated detoxification process is analogous to the insect genome-encoded fenitrothion detoxification system present in other insects. Our findings highlight the capacity of symbiosis, combined with horizontal gene transfer in the environment, as a powerful strategy for an insect to instantly eliminate a toxic chemical compound, which could play a critical role in the human-pest arms race.

Date: 2021
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DOI: 10.1038/s41467-021-26649-2

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