Tenuazonic acid alters immune and physiological reactions and susceptibility to pathogens in Galleria mellonella larvae

Tenuazonic acid (TeA) is synthesized by phytopathogenic and opportunistic fungi and is detected in a broad range of foods. This natural compound is of interest in terms of toxicity to animals, but its mechanisms of action on insects are poorly understood. We administered TeA orally at different concentrations (0.2-5.0 mg/[gram of a growth medium]) to the model insect Galleria mellonella, with subsequent estimation of physiological, histological, and immunological parameters in different tissues (midgut, fat body, and hemolymph). Susceptibility of the TeA-treated larvae to pathogenic microorganisms Beauveria bassiana and Bacillus thuringiensis was also analyzed. The feeding of TeA to the larvae led to a substation delay of larval growth, apoptosis-like changes in midgut cells, and an increase in midgut bacterial load. A decrease in activities of detoxification enzymes and downregulation of genes Nox, lysozyme, and cecropin in the midgut and/or hemocoel tissues were detected. By contrast, genes gloverin, gallerimycin, and galiomycin and phenoloxidase activity proved to be upregulated in the studied tissues. Hemocyte density did not change under the influence of TeA. TeA administration increased susceptibility of the larvae to B. bassiana but diminished their susceptibility to B. thuringiensis. The results indicate that TeA disturbs wax moth gut physiology and immunity and also exerts a systemic action on this insect. Mechanisms underlying the observed changes in wax moth susceptibility to the pathogens are discussed.

Automated summary

Tenuazonic acid (TeA), synthesized by phytopathogenic fungi, is found in a wide range of foods and its toxicity to animals is known, but its mechanisms of action on insects are unclear. In this study, TeA was orally administered to Galleria mellonella larvae, resulting in delayed growth, apoptosis-like changes in midgut cells, and increased midgut bacterial load. Decreased activities of detoxification enzymes and downregulation of certain genes were observed, while other genes and phenoloxidase activity were upregulated. TeA increased susceptibility to Beauveria bassiana but decreased susceptibility to Bacillus thuringiensis. These findings suggest that TeA affects gut physiology, immunity, and systemic responses in wax moth larvae.