Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>

<i>Drosophila melanogaster</i> is broadly used to model host–pathogen interactions. Entomopathogenic nematodes are excellent research tools for dissecting the molecular and functional basis of parasitism and the host’s anti-parasitic response. In this work, we used discovery metabolomics...

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Main Authors: Yayra T. Tuani, Navid J. Ayon, Rosemary M. Onjiko, Sam B. Choi, Shruti Yadav, Ioannis Eleftherianos, Peter Nemes
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Molecules
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Online Access:https://www.mdpi.com/1420-3049/30/9/2023
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author Yayra T. Tuani
Navid J. Ayon
Rosemary M. Onjiko
Sam B. Choi
Shruti Yadav
Ioannis Eleftherianos
Peter Nemes
author_facet Yayra T. Tuani
Navid J. Ayon
Rosemary M. Onjiko
Sam B. Choi
Shruti Yadav
Ioannis Eleftherianos
Peter Nemes
author_sort Yayra T. Tuani
collection DOAJ
description <i>Drosophila melanogaster</i> is broadly used to model host–pathogen interactions. Entomopathogenic nematodes are excellent research tools for dissecting the molecular and functional basis of parasitism and the host’s anti-parasitic response. In this work, we used discovery metabolomics to explore the differences in the metabolome composition of wild type <i>D. melanogaster</i> larvae that were infected with symbiotic nematodes (<i>Steinernema carpocapsae</i> carrying <i>Xenorhabdus nematophila</i> mutualistic bacteria) or axenic nematodes (<i>S. carpocapsae</i> lacking their bacterial partners). Benefiting from their high separation power, sensitivity, and compatibility with low amounts of the starting metabolome, we leveraged microanalytical capillary electrophoresis electrospray ionization mass spectrometry (CE-ESI-MS) to profile the small (<500 Da) polar portion of the metabolome among these experimental treatments. We detected and quantified 122 different small molecules, of which 50 were identified with high confidence. Supervised multivariate analysis revealed that the infection was paralleled with changes in amino acid biosynthesis (arginine, phenylalanine, tryptophan, and tyrosine), metabolism (alanine, arginine, aspartate, glutamate, glycine, proline, serine, and threonine), and classical signalling (aspartate, γ-aminobutyrate, glutamate, and pyridoxine). This study demonstrates the ability of high-sensitivity CE-ESI-MS to uncover metabolic perturbations during infection. The results from the metadata may facilitate the design of targeted studies to explore small biomolecules and their functions during host–pathogen interaction.
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spelling doaj-art-ae8fb5a2b32a404f999d6b53bb27bcd52025-08-20T02:59:08ZengMDPI AGMolecules1420-30492025-05-01309202310.3390/molecules30092023Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>Yayra T. Tuani0Navid J. Ayon1Rosemary M. Onjiko2Sam B. Choi3Shruti Yadav4Ioannis Eleftherianos5Peter Nemes6Department of Chemistry & Biochemistry, University of Maryland, College Park, MD 20742, USADepartment of Chemistry & Biochemistry, University of Maryland, College Park, MD 20742, USADepartment of Chemistry & Biochemistry, University of Maryland, College Park, MD 20742, USADepartment of Chemistry & Biochemistry, University of Maryland, College Park, MD 20742, USADepartment of Biological Sciences, The George Washington University, Washington, DC 20052, USADepartment of Biological Sciences, The George Washington University, Washington, DC 20052, USADepartment of Chemistry & Biochemistry, University of Maryland, College Park, MD 20742, USA<i>Drosophila melanogaster</i> is broadly used to model host–pathogen interactions. Entomopathogenic nematodes are excellent research tools for dissecting the molecular and functional basis of parasitism and the host’s anti-parasitic response. In this work, we used discovery metabolomics to explore the differences in the metabolome composition of wild type <i>D. melanogaster</i> larvae that were infected with symbiotic nematodes (<i>Steinernema carpocapsae</i> carrying <i>Xenorhabdus nematophila</i> mutualistic bacteria) or axenic nematodes (<i>S. carpocapsae</i> lacking their bacterial partners). Benefiting from their high separation power, sensitivity, and compatibility with low amounts of the starting metabolome, we leveraged microanalytical capillary electrophoresis electrospray ionization mass spectrometry (CE-ESI-MS) to profile the small (<500 Da) polar portion of the metabolome among these experimental treatments. We detected and quantified 122 different small molecules, of which 50 were identified with high confidence. Supervised multivariate analysis revealed that the infection was paralleled with changes in amino acid biosynthesis (arginine, phenylalanine, tryptophan, and tyrosine), metabolism (alanine, arginine, aspartate, glutamate, glycine, proline, serine, and threonine), and classical signalling (aspartate, γ-aminobutyrate, glutamate, and pyridoxine). This study demonstrates the ability of high-sensitivity CE-ESI-MS to uncover metabolic perturbations during infection. The results from the metadata may facilitate the design of targeted studies to explore small biomolecules and their functions during host–pathogen interaction.https://www.mdpi.com/1420-3049/30/9/2023metabolomics<i>Steinernema carpocapsae</i><i>Xenorhabdus nematophila</i>nematodeparasitismsymbiosis
spellingShingle Yayra T. Tuani
Navid J. Ayon
Rosemary M. Onjiko
Sam B. Choi
Shruti Yadav
Ioannis Eleftherianos
Peter Nemes
Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>
Molecules
metabolomics
<i>Steinernema carpocapsae</i>
<i>Xenorhabdus nematophila</i>
nematode
parasitism
symbiosis
title Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>
title_full Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>
title_fullStr Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>
title_full_unstemmed Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>
title_short Capillary Electrophoresis Electrospray Ionization Mass Spectrometry Reveals Metabolic Perturbations During Nematode Infection in <i>Drosophila melanogaster</i>
title_sort capillary electrophoresis electrospray ionization mass spectrometry reveals metabolic perturbations during nematode infection in i drosophila melanogaster i
topic metabolomics
<i>Steinernema carpocapsae</i>
<i>Xenorhabdus nematophila</i>
nematode
parasitism
symbiosis
url https://www.mdpi.com/1420-3049/30/9/2023
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