Mandelonitrile produced by commensal bacteria protects the Colorado potato beetle against predation

Wei-Nan Kang, Yang Pan, Lan-Lan Liao, Yi-Kuan Wu, Xiao-Qing Zhang, Lin Jin, Kai-Yun Fu, Wen-Chao Guo and Guo-Qing Li ()
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Wei-Nan Kang: Nanjing Agricultural University
Yang Pan: Nanjing Agricultural University
Lan-Lan Liao: Nanjing Agricultural University
Yi-Kuan Wu: Nanjing Agricultural University
Xiao-Qing Zhang: Nanjing Agricultural University
Lin Jin: Nanjing Agricultural University
Kai-Yun Fu: Xinjiang Academy of Agricultural Sciences
Wen-Chao Guo: Xinjiang Academy of Agricultural Sciences
Guo-Qing Li: Nanjing Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: Abstract Larvae and adults of the Colorado potato beetle (Leptinotarsa decemlineata), a major pest of potato crops, display conspicuous coloration to advertise their toxicity to predators. However, the identity of the toxic compounds remains unclear. Here, we show that larvae and adults release toxic hydrogen cyanide (HCN) from the degradation of mandelonitrile and other cyano-compounds, which are produced by commensal bacteria. We isolate the bacterium Proteus vulgaris Ld01 from the insect’s gut, and show that it produces HCN and a mandelonitrile-producing cyanoglucoside, amygdalin. Knockout of a gene (hcnB) encoding putative hydrogen cyanide synthase impairs HCN production in P. vulgaris Ld01. Antibiotic treatment of larvae, to eliminate their commensal bacteria, leads to a substantial reduction of HCN emission in larvae and adults. HCN release by bacteria-deprived beetles can be restored by addition of mandelonitrile or by re-infection with P. vulgaris Ld01 (but not with its ∆hcnB1 or ∆hcnB2 mutants). Finally, we use dual-choice experiments to show that domestic chicks prefer to eat bacteria-deprived larvae over control larvae, larvae re-colonized with P. vulgaris Ld01, or mandelonitrile-injected larvae. Our work highlights the role of the beetle’s intestinal bacteria in the production of the cyanoglucoside amygdalin and its derived metabolites, including mandelonitrile and HCN, which protect the insect from predation.

Date: 2024
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DOI: 10.1038/s41467-024-54439-z

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