Metabolomics Reveal That Octocrylene Accumulates in <i>Pocillopora damicornis</i> Tissues as Fatty Acid Conjugates and Triggers Coral Cell Mitochondrial Dysfunction

Stien, Didier; Clergeaud, Fanny; Rodrigues, A. S.; Lebaron, Karine; Pillot, Rémi; Romans, Pascal; Fagervold, Sonja K.; Lebaron, Philippe

doi:10.1021/acs.analchem.8b04187

Cited by 63 publications

(91 citation statements)

References 28 publications

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“…We also observed a concentration-dependent increase in mortality of Artemia with respect to the control. This is congruent with the toxicity observed, at lower concentration, on coral (50 µg/L) [23], urchin, mussel and algae (40-80 µg/L) [19]. OC also affects the developmental process in zebrafish [37].…”

Section: Effects On Artemia Salina Mortalitysupporting

confidence: 86%

“…Several studies have demonstrated that some of these compounds can disrupt survival [12][13][14]. behavior [15,16], growth [14,17,18], development [19,20], metabolism [21][22][23], gene expression [24,25] and reproduction [15,26,27] in various species. It should be noted that most toxicological studies on organic UV filters were conducted on BP3, EMC and 4-MBC [7].…”

Section: Introductionmentioning

confidence: 99%

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Effect of 10 UV Filters on the Brine Shrimp Artemia salina and the Marine Microalga Tetraselmis sp.

Thorel

Clergeaud

Jaugeon

et al. 2020

Toxics

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The presence of pharmaceutical and personal care product (PPCP) residues in the aquatic environment is an emerging issue due to their uncontrolled release through gray water, and accumulation in the environment that may affect living organisms, ecosystems and public health. The aim of this study is to assess the toxicity of benzophenone-3 (BP-3), bis-ethylhexyloxyphenol methoxyphenyl triazine (BEMT), butyl methoxydibenzoylmethane (BM), methylene bis-benzotriazolyl tetramethylbutylphenol (MBBT), 2-ethylhexyl salicylate (ES), diethylaminohydroxybenzoyl hexyl benzoate (DHHB), diethylhexyl butamido triazone (DBT), ethylhexyl triazone (ET), homosalate (HS) and octocrylene (OC) on marine organisms from two major trophic levels, including autotrophs (Tetraselmis sp.) and heterotrophs (Artemia salina). In general, results showed that both HS and OC were the most toxic UV filters for our tested species, followed by a significant effect of BM on Artemia salina due to BM—but only at high concentrations (1 mg/L). ES, BP3 and DHHB affected the metabolic activity of the microalgae at 100 µg/L. BEMT, DBT, ET, MBBT had no effect on the tested organisms, even at high concentrations (2 mg/L). OC toxicity represents a risk for those species, since concentrations used in this study are 15–90 times greater than those reported in occurrence studies for aquatic environments. For the first time in the literature, we report HS toxicity on a microalgae species at concentrations complementing those found in aquatic environments. These preliminary results could represent a risk in the future if concentrations of OC and HS continue to increase.

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Section: Effects On Artemia Salina Mortalitysupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Effect of 10 UV Filters on the Brine Shrimp Artemia salina and the Marine Microalga Tetraselmis sp.

Thorel

Clergeaud

Jaugeon

et al. 2020

Toxics

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“…To this end, it has been suggested that studying the coral polyps, which serves as model organisms for reef corals, is a more plausible way to acquire the necessary physiological information to understand the biological behaviors of reef corals [11][12][13][14][15] . However, it still remains a challenge to collect and culture single coral polyps in vitro 16 .…”

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confidence: 99%

A polyp-on-chip for coral long-term culture

Pang

Luo

et al. 2020

Sci Rep

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Coral polyps are basic clonal biological units of reef corals. However, in vitro experimental model for long-term physiological and ecological studies has not been well developed due to the difficulty of effectively acquiring and culturing single polyps. This study developed an experimental platform based on microfluidics for culturing single coral polyps and tracing its growth state over time in the long run. The corresponding computational modeling was conducted to predict the metabolic processes under the static and dynamic conditions by coupling the mass transfer and reaction with Navier-Stokes equations. Design and fabrication of the microfluidic chip was the key to provide a constant laminar flow environment that enabled the controlled high oxygen and bicarbonate transfer for the cultivation of the single coral polyps. The single coral polyps were induced to bail out of the coral reef upon the chemical stress and cultured for more than fifteen days in the microfluidic chip. It was found that the single coral polyps in the microfluidic chip can maintain their normal metabolic process over the cultivation period, suggesting that our microfluidic platform can serve as a suitable tool to study the coral polyps by providing a controllable and suitable biological microenvironment.

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“…In the current study, P. damicornis nubbins were exposed to ES for 7 days at concentrations of 5, 50, 300 and 1000 µg/L. As with OC previously, the extracts prepared from the coral nubbins exposed to ES were analyzed by UHPLC-ESI + -HRMS 2 and compared with control experiment 7 .…”

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confidence: 99%

“…Interestingly, the differential analysis www.nature.com/scientificreports www.nature.com/scientificreports/ showed that all these compounds were significantly upregulated when the coral was exposed to ES at concentrations ranging from 50 to 1000 µg/L. It turned out that the concentration of 14 also increased upon exposition to OC 7 , and at this point, it was clearly necessary to determine unambiguously the structure of compound 14. Extensive fractionation allowed for the isolation of 14 in its pure form, which was ultimately identified by NMR as the known steroid (3β,5α,8α)-5, 8-epidioxy-ergosta-6,24(28)-dien-3-ol.…”

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confidence: 99%

A unique approach to monitor stress in coral exposed to emerging pollutants

Stien

Suzuki

Rodrigues

et al. 2020

Sci Rep

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Metabolomic profiling of the hexacoral Pocillopora damicornis exposed to solar filters revealed a metabolomic signature of stress in this coral. It was demonstrated that the concentration of the known steroid (3β, 5α, 8α)-5, 8-epidioxy-ergosta-6, 24(28)-dien-3-ol (14) increased in response to octocrylene (OC) and ethylhexyl salicylate (ES) at 50 µg/L. Based on the overall coral response, we hypothesize that steroid 14 mediates coral response to stress. OC also specifically altered mitochondrial function at this concentration and above, while ES triggered a stress/inflammatory response at 300 µg/L and above as witnessed by the significant increases in the concentrations of polyunsaturated fatty acids, lysophosphatidylcholines and lysophosphatidylethanolamines. Benzophenone-3 increased the concentration of compound 14 at 2 mg/L, while the concentration of stress marker remained unchanged upon exposition to the other solar filters tested. Also, our results seemed to refute earlier suggestions that platelet-activating factor is involved in the coral inflammatory response. Coral reefs are experiencing an unprecedented planet-wide decline 1. This decline has been attributed to several anthropogenic factors, including global warming, overfishing, and pollution. Widely used for skin protection against cancer, solar filters are regularly released in the sea from populated coastal zones or in sites dedicated to touristic activities including a bathing zone. Nonetheless, the impacts of solar filters on corals have been relatively understudied to date. An early article from Danovaro and coworkers 2 demonstrated that solar filters can induce coral bleaching by promoting viral infections. More recently, it was shown that several UV filters in the benzophenone class, along with octocrylene (OC), exert direct detrimental effects on corals 3-7. Additionally, it has been shown that other ingredients in sunscreens and cosmetics exacerbate the toxicity of the UV filters OC and octinoxate 8 , while Fel et al. reported that many UV filters, including OC have little or no effect on corals 9. According to Downs et al., benzophenone-3 (BP3) induced concentration-dependent planulae coral bleaching, DNA-AP lesions, ossification of the planula, and planulae mortality, and these adverse effects were exacerbated by light 3. In our previous work, we compared the metabolomic profiles of exposed and unexposed corals and demonstrated that OC triggers mitochondrial dysfunction that results in the accumulation of acylcarnitines 7. Also of great concern were both the accumulation of OC derivatives in coral tissues and the concentration at which the toxicity was detected. In a 1-week exposure experiment, 19 OC derivatives were found in the coral tissue, and the response-inducing concentration was 50 µg/L, a concentration only 5 to 10 times higher than the highest environmental concentrations reported in the literature 10,11. Since wild corals are exposed to solar filters for longer periods of time, it has been hypothesized that OC does impact corals ...

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Metabolomics Reveal That Octocrylene Accumulates in Pocillopora damicornis Tissues as Fatty Acid Conjugates and Triggers Coral Cell Mitochondrial Dysfunction

Cited by 63 publications

References 28 publications

Effect of 10 UV Filters on the Brine Shrimp Artemia salina and the Marine Microalga Tetraselmis sp.

Effect of 10 UV Filters on the Brine Shrimp Artemia salina and the Marine Microalga Tetraselmis sp.

A polyp-on-chip for coral long-term culture

A unique approach to monitor stress in coral exposed to emerging pollutants

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