Role of Bacillus atrophaeus B1 in gut on nicotine tolerance of the fall armyworm

Abstract

The fall armyworm (FAW), Spodoptera frugiperda is one of the most destructive polyphagous herbivores. Some detoxification genes have been proved to be involved in the adaptability to host plants in FAW, while the role of its gut microbiota on the responses of host switches, and their ability to adapt to new host plants remain poorly understood. Herein, we isolated five strains of nicotine-degrading bacteria from the gut of S. frugiperda larvae, among which Bacillus atrophaeus B1 exhibited the highest nicotine tolerance. This strain showed a minimum inhibitory concentration (MIC) value of 2 g/L and a nicotine degradation rate of 46.36 %. We sequenced the complete genome of B. atrophaeus B1 and 15 candidate genes were identified maybe related to nicotine degradation, among which GE003027, GE002849, GE002602, GE000220 and GE002708 had significantly higher expression when exposed to nicotine. Non-targeted metabolomics revealed 98 differentially accumulated metabolites (DAMs) under nicotine stress, which were 72 metabolites upregulated and 26 metabolites downregulated, and the pathways most affected involved xenobiotic biodegradation and metabolism, energy metabolism, and amino acid metabolism. B. atrophaeus B1 may accumulate 2-ketoglutaric acid and γ-aminobutyric acid during degradation of nicotine, which is non-toxic to S. frugiperda, and participated in the tricarboxylic acid (TCA) cycle. Additionally, 2-ketoglutaric acid and γ-aminobutyric acid were detected both in B. atrophaeus B1 and S. frugiperda treated with nicotine. Antibiotic treatment deprived most of the gut bacteria, followed by a decrease in tolerance of S. frugiperda to nicotine, and the nicotine degradation rate was significantly increased as expected after reinfection with B. atrophaeus B1. These findings provide new insights into the bacterial metabolism of nicotine degradation and offer a theoretical basis for understanding the rapid adaptability of S. frugiperda to various host plants.