Unraveling the metabolic effects of benzophenone-3 on the endosymbiotic dinoflagellate Cladocopium goreaui

Kaidian Zhang; Kaidian Zhang; Zhen Shen; Zhen Shen; Weilu Yang; Weilu Yang; Jianing Guo; Jianing Guo; Zhicong Yan; Zhicong Yan; Jiashun Li; Jiamin Lin; Jiamin Lin; Xiaocong Cao; Xiaocong Cao; Jia Tang; Jia Tang; Zhaoqun Liu; Zhaoqun Liu; Zhi Zhou; Zhi Zhou; Senjie Lin; Senjie Lin; Senjie Lin; Senjie Lin

doi:10.3389/fmicb.2022.1116975

Frontiers in Microbiology (Mar 2023)

Unraveling the metabolic effects of benzophenone-3 on the endosymbiotic dinoflagellate Cladocopium goreaui

Kaidian Zhang,
Kaidian Zhang,
Zhen Shen,
Zhen Shen,
Weilu Yang,
Weilu Yang,
Jianing Guo,
Jianing Guo,
Zhicong Yan,
Zhicong Yan,
Jiashun Li,
Jiamin Lin,
Jiamin Lin,
Xiaocong Cao,
Xiaocong Cao,
Jia Tang,
Jia Tang,
Zhaoqun Liu,
Zhaoqun Liu,
Zhi Zhou,
Zhi Zhou,
Senjie Lin,
Senjie Lin,
Senjie Lin,
Senjie Lin

Affiliations

Kaidian Zhang: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Kaidian Zhang: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Zhen Shen: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Zhen Shen: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Weilu Yang: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Weilu Yang: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Jianing Guo: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Jianing Guo: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Zhicong Yan: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Zhicong Yan: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Jiashun Li: State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, Fujian, China
Jiamin Lin: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Jiamin Lin: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Xiaocong Cao: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Xiaocong Cao: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Jia Tang: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Jia Tang: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Zhaoqun Liu: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Zhaoqun Liu: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Zhi Zhou: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Zhi Zhou: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Senjie Lin: State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China
Senjie Lin: Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China
Senjie Lin: State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, Fujian, China
Senjie Lin: Department of Marine Sciences, University of Connecticut, Groton, CT, United States

DOI: https://doi.org/10.3389/fmicb.2022.1116975
Journal volume & issue: Vol. 13

Abstract

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As a well-known pseudo-persistent environmental pollutant, oxybenzone (BP-3) and its related organic ultraviolet (UV) filters have been verified to directly contribute to the increasing mortality rate of coral reefs. Previous studies have revealed the potential role of symbiotic Symbiodiniaceae in protecting corals from the toxic effects of UV filters. However, the detailed protection mechanism(s) have not been explained. Here, the impacts of BP-3 on the symbiotic Symbiodiniaceae Cladocopium goreaui were explored. C. goreaui cells exhibited distinct cell growth at different BP-3 doses, with increasing growth at the lower concentration (2 mg L–1) and rapid death at a higher concentration (20 mg L–1). Furthermore, C. goreaui cells showed a significant BP-3 uptake at the lower BP-3 concentration. BP-3 absorbing cells exhibited elevated photosynthetic efficiency, and decreased cellular carbon and nitrogen contents. Besides, the derivatives of BP-3 and aromatic amino acid metabolism highly responded to BP-3 absorption and biodegradation. Our physiological and metabolic results reveal that the symbiotic Symbiodiniaceae could resist the toxicity of a range of BP-3 through promoting cell division, photosynthesis, and reprogramming amino acid metabolism. This study provides novel insights into the influences of organic UV filters to coral reef ecosystems, which urgently needs increasing attention and management.

Published in Frontiers in Microbiology

ISSN: 1664-302X (Online)
Publisher: Frontiers Media S.A.
Country of publisher: Switzerland
LCC subjects: Science: Microbiology
Website: http://www.frontiersin.org/journals/microbiology

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