Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid
Imidacloprid severely poisons the nontarget insect honey bee Apis mellifera. Few treatments are available to mitigate the adverse effects of imidacloprid. The primary concern is that the molecular understanding of imidacloprid toxicity is not comprehensive enough. Oxidative stress is the primary pat...
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| Format: | Article |
| Language: | English |
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Elsevier
2022-07-01
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| Series: | Ecotoxicology and Environmental Safety |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651322004626 |
| _version_ | 1818554084264771584 |
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| author | Zhi Li Jiaxin Duan Lanchun Chen Yuedi Wang Qiqian Qin Xiaoqun Dang Zeyang Zhou |
| author_facet | Zhi Li Jiaxin Duan Lanchun Chen Yuedi Wang Qiqian Qin Xiaoqun Dang Zeyang Zhou |
| author_sort | Zhi Li |
| collection | DOAJ |
| description | Imidacloprid severely poisons the nontarget insect honey bee Apis mellifera. Few treatments are available to mitigate the adverse effects of imidacloprid. The primary concern is that the molecular understanding of imidacloprid toxicity is not comprehensive enough. Oxidative stress is the primary pathophysiological mechanism by which pesticides cause high mortality. Our pilot study found for the first time that imidacloprid stimulates bee brains to secrete melatonin, a free radical scavenger. However, the molecular basis for imidacloprid toxicity and the role of melatonin in coping with imidacloprid have not been systematically investigated in bees. This study administered an environmental dose of imidacloprid (36 ng/bee) orally to A. mellifera. The detoxification gene cytochrome P450 CYP4G11 was significantly induced. However, potent cytotoxicity of imidacloprid suppressed the expression of the antioxidants catalase (CAT) and thioredoxin reductase (TrxR), and the activity of guaiacol peroxidase (GPX), superoxide dismutase (SOD), and reduced glutathione (GSH) was not induced. The levels of reactive oxygen species (ROS) and the lipid peroxidation marker malondialdehyde (MDA) were increased. The expression of the apoptotic genes cysteinyl aspartate specific proteinase (Caspase-3) and apoptosis inducing factor (AIF) increased, and the apoptotic features of midgut cells were prominently apparent. These results suggest that imidacloprid disrupts the bee antioxidant system, causing severe oxidative stress and tissue damage and ultimately leading to apoptosis. Significantly, however, imidacloprid exposure also stimulated bee brains to continuously secrete melatonin. Further preadministration of exogenous melatonin (200 ng/bee) orally to bees significantly reversed and enhanced the activity of the imidacloprid-suppressed antioxidants CAT, SOD, and GSH, which allowed imidacloprid-induced ROS accumulation to be effectively alleviated. The MDA content, apoptotic genes Caspase-3 and AIF, and detoxification gene CYPG411 expression were restored to normalization; midgut cell damage, apoptosis, and mortality were significantly reduced. These findings strongly suggest that melatonin enhanced bee antioxidant capacity, thus attenuating oxidative stress and apoptosis to confer imidacloprid tolerance to honey bees. Melatonin secretion may be a defense mechanism to mitigate imidacloprid toxicity. |
| first_indexed | 2024-12-12T09:34:36Z |
| format | Article |
| id | doaj.art-06876101563c4b61b15b07449cf26a05 |
| institution | Directory Open Access Journal |
| issn | 0147-6513 |
| language | English |
| last_indexed | 2024-12-12T09:34:36Z |
| publishDate | 2022-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj.art-06876101563c4b61b15b07449cf26a052022-12-22T00:28:45ZengElsevierEcotoxicology and Environmental Safety0147-65132022-07-01239113622Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidaclopridZhi Li0Jiaxin Duan1Lanchun Chen2Yuedi Wang3Qiqian Qin4Xiaoqun Dang5Zeyang Zhou6College of Life Sciences, Chongqing Normal University, Chongqing, China; Chongqing Key Laboratory of Animal Biology, China; Corresponding author at: College of Life Sciences, Chongqing Normal University, Chongqing, China.College of Life Sciences, Chongqing Normal University, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Chongqing Key Laboratory of Animal Biology, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Chongqing Key Laboratory of Microsporidia Infection and Control, China; The State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing, ChinaImidacloprid severely poisons the nontarget insect honey bee Apis mellifera. Few treatments are available to mitigate the adverse effects of imidacloprid. The primary concern is that the molecular understanding of imidacloprid toxicity is not comprehensive enough. Oxidative stress is the primary pathophysiological mechanism by which pesticides cause high mortality. Our pilot study found for the first time that imidacloprid stimulates bee brains to secrete melatonin, a free radical scavenger. However, the molecular basis for imidacloprid toxicity and the role of melatonin in coping with imidacloprid have not been systematically investigated in bees. This study administered an environmental dose of imidacloprid (36 ng/bee) orally to A. mellifera. The detoxification gene cytochrome P450 CYP4G11 was significantly induced. However, potent cytotoxicity of imidacloprid suppressed the expression of the antioxidants catalase (CAT) and thioredoxin reductase (TrxR), and the activity of guaiacol peroxidase (GPX), superoxide dismutase (SOD), and reduced glutathione (GSH) was not induced. The levels of reactive oxygen species (ROS) and the lipid peroxidation marker malondialdehyde (MDA) were increased. The expression of the apoptotic genes cysteinyl aspartate specific proteinase (Caspase-3) and apoptosis inducing factor (AIF) increased, and the apoptotic features of midgut cells were prominently apparent. These results suggest that imidacloprid disrupts the bee antioxidant system, causing severe oxidative stress and tissue damage and ultimately leading to apoptosis. Significantly, however, imidacloprid exposure also stimulated bee brains to continuously secrete melatonin. Further preadministration of exogenous melatonin (200 ng/bee) orally to bees significantly reversed and enhanced the activity of the imidacloprid-suppressed antioxidants CAT, SOD, and GSH, which allowed imidacloprid-induced ROS accumulation to be effectively alleviated. The MDA content, apoptotic genes Caspase-3 and AIF, and detoxification gene CYPG411 expression were restored to normalization; midgut cell damage, apoptosis, and mortality were significantly reduced. These findings strongly suggest that melatonin enhanced bee antioxidant capacity, thus attenuating oxidative stress and apoptosis to confer imidacloprid tolerance to honey bees. Melatonin secretion may be a defense mechanism to mitigate imidacloprid toxicity.http://www.sciencedirect.com/science/article/pii/S0147651322004626ImidaclopridMelatoninOxidative stressAntioxidantApis mellifera |
| spellingShingle | Zhi Li Jiaxin Duan Lanchun Chen Yuedi Wang Qiqian Qin Xiaoqun Dang Zeyang Zhou Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid Ecotoxicology and Environmental Safety Imidacloprid Melatonin Oxidative stress Antioxidant Apis mellifera |
| title | Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid |
| title_full | Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid |
| title_fullStr | Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid |
| title_full_unstemmed | Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid |
| title_short | Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid |
| title_sort | melatonin enhances the antioxidant capacity to rescue the honey bee apis mellifera from the ecotoxicological effects caused by environmental imidacloprid |
| topic | Imidacloprid Melatonin Oxidative stress Antioxidant Apis mellifera |
| url | http://www.sciencedirect.com/science/article/pii/S0147651322004626 |
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