Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>

The fungus <i>Ascosphaera apis</i>, an obligate fungal pathogen of honey bee brood, causes chalkbrood disease in honey bee larvae worldwide. Biological characteristics of the fungal pathogen and the molecular interactions between <i>A. apis</i> and honey bees have been studie...

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Main Authors: Zhiguo Li, Mengshang Hou, Yuanmei Qiu, Bian Zhao, Hongyi Nie, Songkun Su
Format: Article
Language:English
Published: MDPI AG 2020-07-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/11/7/419
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author Zhiguo Li
Mengshang Hou
Yuanmei Qiu
Bian Zhao
Hongyi Nie
Songkun Su
author_facet Zhiguo Li
Mengshang Hou
Yuanmei Qiu
Bian Zhao
Hongyi Nie
Songkun Su
author_sort Zhiguo Li
collection DOAJ
description The fungus <i>Ascosphaera apis</i>, an obligate fungal pathogen of honey bee brood, causes chalkbrood disease in honey bee larvae worldwide. Biological characteristics of the fungal pathogen and the molecular interactions between <i>A. apis</i> and honey bees have been studied extensively. However, little is known about the effects of <i>A. apis</i> infection on antioxidant enzyme activities and metabolic profiles of the gut of honey bee larvae. In this study, sandwich enzyme-linked immunosorbent assay and LC-MS based untargeted metabolomic analysis were employed to determine the changes in the specific activities of antioxidant enzymes and the metabolomic profiles in gut tissues of <i>A. apis</i>-infected larvae (10<sup>5</sup> <i>A. apis</i> spores per larva) and controls. Results showed that specific activities of superoxide dismutase, catalase and glutathione S-transferase were significantly higher in the guts of the control larvae than in the guts of the <i>A. apis</i>-infected larvae. The metabolomic data revealed that levels of 28 and 52 metabolites were significantly higher and lower, respectively, in the guts of <i>A. apis</i>-infected larvae than in the guts of control larvae. The 5-oxo-ETE level in the infected larvae was two times higher than that in the control larvae. Elevated 5-oxo-ETE levels may act as a potential metabolic biomarker for chalkbrood disease diagnosis, suggesting that <i>A. apis</i> infection induced obvious oxidative stress in the honey bee larvae. The levels of metabolites such as taurine, docosahexaenoic acid, and L-carnitine involved in combating oxidative stress were significantly decreased in the gut of <i>A. apis</i>-infected larvae. Overall, our results suggest that <i>A. apis</i> infection may compromise the ability of infected larvae to cope with oxidative stress, providing new insight into changing patterns of physiological responses to <i>A. apis</i> infection in honey bee larvae by concurrent use of conventional biochemical assays and untargeted metabolomics.
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spelling doaj.art-01cd7b56bd154fbaa815834208114ac82023-11-20T05:55:13ZengMDPI AGInsects2075-44502020-07-0111741910.3390/insects11070419Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>Zhiguo Li0Mengshang Hou1Yuanmei Qiu2Bian Zhao3Hongyi Nie4Songkun Su5College of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaThe fungus <i>Ascosphaera apis</i>, an obligate fungal pathogen of honey bee brood, causes chalkbrood disease in honey bee larvae worldwide. Biological characteristics of the fungal pathogen and the molecular interactions between <i>A. apis</i> and honey bees have been studied extensively. However, little is known about the effects of <i>A. apis</i> infection on antioxidant enzyme activities and metabolic profiles of the gut of honey bee larvae. In this study, sandwich enzyme-linked immunosorbent assay and LC-MS based untargeted metabolomic analysis were employed to determine the changes in the specific activities of antioxidant enzymes and the metabolomic profiles in gut tissues of <i>A. apis</i>-infected larvae (10<sup>5</sup> <i>A. apis</i> spores per larva) and controls. Results showed that specific activities of superoxide dismutase, catalase and glutathione S-transferase were significantly higher in the guts of the control larvae than in the guts of the <i>A. apis</i>-infected larvae. The metabolomic data revealed that levels of 28 and 52 metabolites were significantly higher and lower, respectively, in the guts of <i>A. apis</i>-infected larvae than in the guts of control larvae. The 5-oxo-ETE level in the infected larvae was two times higher than that in the control larvae. Elevated 5-oxo-ETE levels may act as a potential metabolic biomarker for chalkbrood disease diagnosis, suggesting that <i>A. apis</i> infection induced obvious oxidative stress in the honey bee larvae. The levels of metabolites such as taurine, docosahexaenoic acid, and L-carnitine involved in combating oxidative stress were significantly decreased in the gut of <i>A. apis</i>-infected larvae. Overall, our results suggest that <i>A. apis</i> infection may compromise the ability of infected larvae to cope with oxidative stress, providing new insight into changing patterns of physiological responses to <i>A. apis</i> infection in honey bee larvae by concurrent use of conventional biochemical assays and untargeted metabolomics.https://www.mdpi.com/2075-4450/11/7/419<i>Apis mellifera</i>chalkbrood<i>Ascosphaera apis</i>metabolomicsenzyme activities
spellingShingle Zhiguo Li
Mengshang Hou
Yuanmei Qiu
Bian Zhao
Hongyi Nie
Songkun Su
Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>
Insects
<i>Apis mellifera</i>
chalkbrood
<i>Ascosphaera apis</i>
metabolomics
enzyme activities
title Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>
title_full Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>
title_fullStr Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>
title_full_unstemmed Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>
title_short Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (<i>Apis mellifera</i>) Larvae Infected with <i>Ascosphaera apis</i>
title_sort changes in antioxidant enzymes activity and metabolomic profiles in the guts of honey bee i apis mellifera i larvae infected with i ascosphaera apis i
topic <i>Apis mellifera</i>
chalkbrood
<i>Ascosphaera apis</i>
metabolomics
enzyme activities
url https://www.mdpi.com/2075-4450/11/7/419
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