The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levels
Prorocentrum donghaiense, a marine dinoflagellate, causes harmful algal blooms (HABs) characterised by the highest outbreak frequency and most extensive coverage among similar species in the East China Sea. Highly efficient and ecofriendly biocontrol strategies should be developed for HAB control. P...
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| Format: | Article |
| Language: | English |
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Elsevier
2021-12-01
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| Series: | Ecotoxicology and Environmental Safety |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651321010253 |
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| author | Yingjie Chen Guiying Luo Shuangshuang Chen Danyang Zhang Wanxin Xie Zengge Wang Wei Zheng Hong Xu |
| author_facet | Yingjie Chen Guiying Luo Shuangshuang Chen Danyang Zhang Wanxin Xie Zengge Wang Wei Zheng Hong Xu |
| author_sort | Yingjie Chen |
| collection | DOAJ |
| description | Prorocentrum donghaiense, a marine dinoflagellate, causes harmful algal blooms (HABs) characterised by the highest outbreak frequency and most extensive coverage among similar species in the East China Sea. Highly efficient and ecofriendly biocontrol strategies should be developed for HAB control. Prodigiosin is an efficient biological algicide that demonstrated strong algicidal activity towards P. donghaiense. However, the mechanism of its toxicity to P. donghaiense is unknown. These factors were investigated to evaluate potential use of prodigiosin for control of P. donghaiense blooms. Photosynthetic electron transport rate, maximum quantum yield and respiration rate of P. donghaiense decreased significantly upon exposure to prodigiosin, indicating that prodigiosin rapidly exerted adverse effects on the chloroplasts and mitochondria. Furthermore, a significant increase in dichlorofluorescein fluorescence intensity indicated an overproduction of reactive oxygen species (ROS). The antioxidant system of P. donghaiense scavenged ROS; however, an increase in malondialdehyde concentrations indicated that excessive ROS were still able to initiate lipid peroxidation. Thus, ROS production resulted in the formation of lipids with a reduced degree of unsaturation. Lipid peroxidation decreased lipid fluidity and rigidified the membrane system, causing serious functional destruction of the membrane. Flow cytometry analysis indicated that prodigiosin arrested the cell cycle of P. donghaiense. However, surviving algal cells were able to repair the damaged functions and resume the cell cycle after prodigiosin was removed by photodegradation. Otherwise, P. donghaiense cells lost their membrane integrity and died. To begin an evaluation of ecological safety of prodigiosin, we tested four marine organisms at various trophic levels. The results of these tests indicated that Chlorella vulgaris, Photobacterium phosphoreum, Artemia salina and Lateolabrax japonicus were less sensitive to prodigiosin than P. donghaiense. Toxicity to all five organisms declined after prodigiosin was exposed to sunlight for 6 h. Considering the toxic doses of prodigiosin to various organisms and its photodegradation characteristics, we suggest that prodigiosin has potential in controlling P. donghaiense blooms but should be applied at night, in small doses, with multiple applications. |
| first_indexed | 2024-12-17T21:10:05Z |
| format | Article |
| id | doaj.art-bc11d4223a0c43ccaed403e22ae160fb |
| institution | Directory Open Access Journal |
| issn | 0147-6513 |
| language | English |
| last_indexed | 2024-12-17T21:10:05Z |
| publishDate | 2021-12-01 |
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| series | Ecotoxicology and Environmental Safety |
| spelling | doaj.art-bc11d4223a0c43ccaed403e22ae160fb2022-12-21T21:32:29ZengElsevierEcotoxicology and Environmental Safety0147-65132021-12-01228112913The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levelsYingjie Chen0Guiying Luo1Shuangshuang Chen2Danyang Zhang3Wanxin Xie4Zengge Wang5Wei Zheng6Hong Xu7State Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR China; Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, Xiamen University, Xiamen, Fujian 361102, PR ChinaState Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR ChinaState Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR ChinaState Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR ChinaState Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR ChinaState Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR ChinaState Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR ChinaState Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR China; Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, Xiamen University, Xiamen, Fujian 361102, PR China; Corresponding author at: State Key Laboratory of Cellular Stress Biology, and School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, PR China.Prorocentrum donghaiense, a marine dinoflagellate, causes harmful algal blooms (HABs) characterised by the highest outbreak frequency and most extensive coverage among similar species in the East China Sea. Highly efficient and ecofriendly biocontrol strategies should be developed for HAB control. Prodigiosin is an efficient biological algicide that demonstrated strong algicidal activity towards P. donghaiense. However, the mechanism of its toxicity to P. donghaiense is unknown. These factors were investigated to evaluate potential use of prodigiosin for control of P. donghaiense blooms. Photosynthetic electron transport rate, maximum quantum yield and respiration rate of P. donghaiense decreased significantly upon exposure to prodigiosin, indicating that prodigiosin rapidly exerted adverse effects on the chloroplasts and mitochondria. Furthermore, a significant increase in dichlorofluorescein fluorescence intensity indicated an overproduction of reactive oxygen species (ROS). The antioxidant system of P. donghaiense scavenged ROS; however, an increase in malondialdehyde concentrations indicated that excessive ROS were still able to initiate lipid peroxidation. Thus, ROS production resulted in the formation of lipids with a reduced degree of unsaturation. Lipid peroxidation decreased lipid fluidity and rigidified the membrane system, causing serious functional destruction of the membrane. Flow cytometry analysis indicated that prodigiosin arrested the cell cycle of P. donghaiense. However, surviving algal cells were able to repair the damaged functions and resume the cell cycle after prodigiosin was removed by photodegradation. Otherwise, P. donghaiense cells lost their membrane integrity and died. To begin an evaluation of ecological safety of prodigiosin, we tested four marine organisms at various trophic levels. The results of these tests indicated that Chlorella vulgaris, Photobacterium phosphoreum, Artemia salina and Lateolabrax japonicus were less sensitive to prodigiosin than P. donghaiense. Toxicity to all five organisms declined after prodigiosin was exposed to sunlight for 6 h. Considering the toxic doses of prodigiosin to various organisms and its photodegradation characteristics, we suggest that prodigiosin has potential in controlling P. donghaiense blooms but should be applied at night, in small doses, with multiple applications.http://www.sciencedirect.com/science/article/pii/S0147651321010253Prorocentrum donghaienseProdigiosinAlgicidal mechanismEcotoxicityHarmful algal bloomsBiological algicide |
| spellingShingle | Yingjie Chen Guiying Luo Shuangshuang Chen Danyang Zhang Wanxin Xie Zengge Wang Wei Zheng Hong Xu The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levels Ecotoxicology and Environmental Safety Prorocentrum donghaiense Prodigiosin Algicidal mechanism Ecotoxicity Harmful algal blooms Biological algicide |
| title | The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levels |
| title_full | The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levels |
| title_fullStr | The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levels |
| title_full_unstemmed | The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levels |
| title_short | The potential of prodigiosin for control of Prorocentrum donghaiense blooms: Algicidal properties and acute toxicity to other marine organisms at various trophic levels |
| title_sort | potential of prodigiosin for control of prorocentrum donghaiense blooms algicidal properties and acute toxicity to other marine organisms at various trophic levels |
| topic | Prorocentrum donghaiense Prodigiosin Algicidal mechanism Ecotoxicity Harmful algal blooms Biological algicide |
| url | http://www.sciencedirect.com/science/article/pii/S0147651321010253 |
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