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

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, fe...

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Autores principales: Zhang, Yuan, Wang, Fang, Zhao, Zihua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686292/
https://www.ncbi.nlm.nih.gov/pubmed/36439848
http://dx.doi.org/10.3389/fmicb.2022.1042145
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author Zhang, Yuan
Wang, Fang
Zhao, Zihua
author_facet Zhang, Yuan
Wang, Fang
Zhao, Zihua
author_sort Zhang, Yuan
collection PubMed
description 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.
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spelling pubmed-96862922022-11-25 Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects Zhang, Yuan Wang, Fang Zhao, Zihua Front Microbiol Microbiology 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. Frontiers Media S.A. 2022-11-10 /pmc/articles/PMC9686292/ /pubmed/36439848 http://dx.doi.org/10.3389/fmicb.2022.1042145 Text en Copyright © 2022 Zhang, Wang and Zhao. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Zhang, Yuan
Wang, Fang
Zhao, Zihua
Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects
title Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects
title_full Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects
title_fullStr Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects
title_full_unstemmed Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects
title_short Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects
title_sort metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686292/
https://www.ncbi.nlm.nih.gov/pubmed/36439848
http://dx.doi.org/10.3389/fmicb.2022.1042145
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