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

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

doi:10.3389/fmicb.2022.1116975

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

Front Microbiol. 2023 Mar 1:13:1116975. doi: 10.3389/fmicb.2022.1116975. eCollection 2022.

Authors

Kaidian Zhang^{1

2}, Zhen Shen^{1

2}, Weilu Yang^{1

2}, Jianing Guo^{1

2}, Zhicong Yan^{1

2}, Jiashun Li³, Jiamin Lin^{1

2}, Xiaocong Cao^{1

2}, Jia Tang^{1

2}, Zhaoqun Liu^{1

2}, Zhi Zhou^{1

2}, Senjie Lin^{1

2

3

4}

Affiliations

¹ State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China.
² Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan, Hainan University, Haikou, China.
³ State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, Fujian, China.
⁴ Department of Marine Sciences, University of Connecticut, Groton, CT, United States.

Abstract

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.

Keywords: Cladocopium goreaui; UV filters; amino acid metabolism; coral reef ecosystems; oxybenzone; toxic effects.

Grants and funding

This research was supported by the National Key Research and Development Program of China (2022YFC3102003) and the Hainan Provincial Natural Science Foundation of China (422QN265 and 420CXTD432).