Effects of Gelsemium elegans extract on the red fire ant: disruption of peritrophic membrane integrity and alteration of gut microbial diversity, composition, and function

Abstract

Gelsemium elegans Benth. (Loganiaceae), also known as heartbreak herb, can be used in the manufacture of herbal medicines. Insecticidal activity has also been found and can be used to develop botanical insecticides. This study aimed to reveal the insecticidal mechanism of its extracts against red fire ants and provide strategies for the development of biopesticides and the promotion of green and sustainable agriculture. 16s rRNA, pathohistological, behavioral, and enzyme activity assays were performed to reveal its biological effects, including the effects on non-target organisms. Our results showed that red fire ants exposed to G. elegans extracts exhibited slowed growth, reduced feeding, and decreased aggressiveness. The midgut and its peritrophic membrane of red fire ant were significantly disrupted, the diversity of gut microbial community was reduced, and the balance of microbial composition was disturbed. Significant increases in functional abundance of xenobiotics biodegradation and metabolism pathway and P450s enzyme activity confirmed the toxic stress of G. elegans extract. Functional prediction of Kyoto Encyclopedia of Genes and Genomes pathway showed that the functional abundance of novobiocin biosynthesis, flavonoid biosynthesis, lysosome, proteasome, and wingless/integrated signaling pathways were significantly inhibited in the gut. Besides, G. elegans extracts induced an increase in acetylcholinesterase activity. These results revealed dysregulation of immune system and metabolic functions in red fire ants, as well as toxic effects of G. elegans extracts on physiological functions and nerves. These findings revealed the insecticidal mechanism of G. elegans and supported the development of eco-friendly insecticides for red fire ants.