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. 2022 Nov 10:13:1042145.
doi: 10.3389/fmicb.2022.1042145. eCollection 2022.

Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

Yuan Zhang  1 , Fang Wang  2 , Zihua Zhao  1
Affiliations

Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

Yuan Zhang et al. Front Microbiol. .

Abstract

The entomopathogenic nematode (EPN) Steinernema feltiae, which carries the symbiotic bacterium Xenorhabdus bovienii in its gut, is an important biocontrol agent. This EPN could produce a suite of complex metabolites and toxin proteins and lead to the death of host insects within 24-48 h. However, few studies have been performed on the key biomarkers released by EPNs to kill host insects. The objective of this study was to examine what substances produced by EPNs cause the death of host insects. We found that all densities of nematode suspensions exhibited insecticidal activities after hemocoelic injection into Galleria mellonella larvae. EPN infection 9 h later led to immunosuppression by activating insect esterase activity, but eventually, the host insect darkened and died. Before insect immunity was activated, we applied a high-resolution mass spectrometry-based metabolomics approach to determine the hemolymph of the wax moth G. mellonella infected by EPNs. The results indicated that the tryptophan (Trp) pathway of G. mellonella was significantly activated, and the contents of kynurenine (Kyn) and 3-hydroxyanthranilic acid (3-HAA) were markedly increased. Additionally, 3-HAA was highly toxic to G. mellonella and resulted in corrected mortalities of 62.50%. Tryptophan metabolites produced by EPNs are a potential marker to kill insects, opening up a novel line of inquiry into exploring the infestation mechanism of EPNs.

Keywords: 3-HAA; EPNs; Steinernema feltiae; Trp metabolism; Xenorhabdus bovienii.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Changes in G. mellonella after nematode injection: (A) Insecticidal activity of S. feltiae injected with different densities against G. mellonella. Analysis using the logistic function (y = A2 + (A1 − A2)/(1 + (x/x0)^p)) in nonlinear fitting. (B) Apparent changes in the phenotype and esterase activity of G. mellonella. After exposure of 20 IJs to the body cavity.
Figure 2
Figure 2
Statistical analysis of the normalized dataset: (A) PCA score plot of the 3 treatments. Green indicates CK, blue indicates H2O, and orange indicates SF; (B) Volcano plots of SF vs. CK and SF vs. H2O. Blue represents downregulation, orange represents significant upregulation, and silver represents upregulation but no significant difference. (C) Venn diagram of significantly differentially abundant compounds. (D) Results of pathway analysis. The pathway impact value was calculated by pathway topology analysis.
Figure 3
Figure 3
The upregulation of Trp metabolites by injection of S. feltiae-X. bovienii (Created with BioRender.com).
Figure 4
Figure 4
Preliminary insecticidal activity of Trp metabolites.
See this image and copyright information in PMC

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