Degradation and transformation of all-trans-retinoic acid in seawater: implications on its fate and risk in the marine environment
Katie Wan Yee Yeung A B , Guang-Jie Zhou
A B and Kenneth Mei Yee Leung A *
A State Key Laboratory of Marine Pollution and Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China.
B The Swire Institute of Marine Science and School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China.
Environmental Chemistry 19(4) 228-235 https://doi.org/10.1071/EN22053
Submitted: 18 May 2022 Accepted: 23 August 2022 Published: 25 October 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Environmental context. Excessive amounts of retinoic acids (RAs), the main derivatives of vitamin A, cause developmental abnormalities in animals, yet information on their fate in the marine environment is limited. This study investigated the degradation of all-trans-RA in seawater and found that over 90% was degraded and transformed in unfiltered natural seawater within 24 h. The results provide essential insights on the fate and risks of RAs in marine environments.
Rationale. Retinoic acids (RAs) are crucial to the development of various animals. However, exposure to excessive concentrations of RAs can lead to teratogenic effects in aquatic species during their developmental stages. Some urbanised coastal marine environments receive a large amount of partially treated wastewater effluent and occasionally suffer from algal bloom incidents, both of which are considered important sources of RAs in the marine environment. Yet information on degradation and transformation of RAs in seawater is currently unavailable for assessment of their environmental risk. This study, therefore, aimed to investigate the degradation and transformation of all-trans-RA (at-RA), which is the most abundant and widely distributed RA in the marine environment.
Methodology. A laboratory experiment was conducted to examine the degradation and transformation of at-RA in six different types of seawater (i.e. artificial seawater, unfiltered and filtered natural seawater, each with or without autoclave treatment). Degradation and transformation products of at-RA were analysed using high-performance liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS).
Results. The experiment showed that at-RA could be instantly degraded and transformed into other isomers such as 9-cis-RA and 13-cis-RA when entering seawater. Over 80% of at-RA was degraded in the first 48 h regardless of the type of seawater.
Discussion. The presence of microorganisms and suspended organic matters could jointly facilitate the degradation and removal of at-RA from the water column. Further investigation is encouraged to reveal the influence of other factors (e.g. temperature, solar radiation, aeration) on the transformation and degradation of at-RA in seawater.
Keywords: environmental fate, half-life, natural seawater, retinoic acids, retinoids, speciation, transformation, degradation, vitamin A.
References
Barua AB, Furr HC (1998) Properties of retinoids. In ‘Retinoid Protocols’ edited by Redfern CPF. pp. 3–28. (Humana Press)Batley GE (2004). Chemistry – More than a one-line item. Environmental Chemistry 1, 8–9.
| Chemistry – More than a one-line item.Crossref | GoogleScholarGoogle Scholar |
Collins MD, Mao GE (1999). Teratology of retinoids. Annual Review of Pharmacology and Toxicology 39, 399–430.
| Teratology of retinoids.Crossref | GoogleScholarGoogle Scholar |
Cotham Jr WE, Bidleman TF (1989). Degradation of malathion, endosulfan, and fenvalerate in seawater and seawater/sediment microcosms. Journal of Agricultural and Food Chemistry 37, 824–828.
| Degradation of malathion, endosulfan, and fenvalerate in seawater and seawater/sediment microcosms.Crossref | GoogleScholarGoogle Scholar |
Defo MA, Spear PA, Couture P (2014). Consequences of metal exposure on retinoid metabolism in vertebrates: A review. Toxicology Letters 225, 1–11.
| Consequences of metal exposure on retinoid metabolism in vertebrates: A review.Crossref | GoogleScholarGoogle Scholar |
Degitz SJ, Kosian PA, Makynen EA, Jensen KM, Ankley GT (2000). Stage- and species-specific developmental toxicity of all-trans retinoic acid in four native North American ranids and Xenopus laevis. Toxicological Sciences 57, 264–274.
| Stage- and species-specific developmental toxicity of all-trans retinoic acid in four native North American ranids and Xenopus laevis.Crossref | GoogleScholarGoogle Scholar |
Herrmann K (1995). Teratogenic effects of retinoic acid and related substances on the early development of the zebrafish (Brachydanio rerio) as assessed by a novel scoring system. Toxicology in Vitro 9, 267–283.
| Teratogenic effects of retinoic acid and related substances on the early development of the zebrafish (Brachydanio rerio) as assessed by a novel scoring system.Crossref | GoogleScholarGoogle Scholar |
Horiguchi T, Ohta Y, Nishikawa T, Shiraishi F, Shiraishi H, Morita M (2008). Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera. Cell Biology and Toxicology 24, 553–562.
| Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera.Crossref | GoogleScholarGoogle Scholar |
Inoue D, Sawada K, Wada Y, Sei K, Ike M (2013). Removal characteristics of retinoic acids and 4-oxo-retinoic acids in wastewater by activated sludge treatment. Water Science and Technology 67, 2868–2874.
| Removal characteristics of retinoic acids and 4-oxo-retinoic acids in wastewater by activated sludge treatment.Crossref | GoogleScholarGoogle Scholar |
(1983). Nomenclature of retinoids: Recommendations 1981. Archives of Biochemistry and Biophysics 224, 728–731.
| Nomenclature of retinoids: Recommendations 1981.Crossref | GoogleScholarGoogle Scholar |
Jonas A, Buranova V, Scholz S, Fetter E, Novakova K, Kohoutek J, Hilscherova K (2014). Retinoid-like activity and teratogenic effects of cyanobacterial exudates. Aquatic Toxicology 155, 283–290.
| Retinoid-like activity and teratogenic effects of cyanobacterial exudates.Crossref | GoogleScholarGoogle Scholar |
Kang J-H, Kondo F (2005). Bisphenol A degradation in seawater is different from that in river water. Chemosphere 60, 1288–1292.
| Bisphenol A degradation in seawater is different from that in river water.Crossref | GoogleScholarGoogle Scholar |
Murayama A, Suzuki T, Matsui M (1997). Photoisomerization of retinoic acids in ethanol under room light: A warning for cell biological study of geometrical isomers of retinoids. Journal of Nutritional Science and Vitaminology 43, 167–176.
| Photoisomerization of retinoic acids in ethanol under room light: A warning for cell biological study of geometrical isomers of retinoids.Crossref | GoogleScholarGoogle Scholar |
National Center for Biotechnology Information (NCBI) (2022) PubChem Compound Summary for CID 444795, Tretinoin. Available at https://pubchem.ncbi.nlm.nih.gov/compound/Tretinoin
Ross SA, McCaffery PJ, Drager UC, De Luca LM (2000). Retinoids in embryonal development. Physiological Reviews 80, 1021–1054.
| Retinoids in embryonal development.Crossref | GoogleScholarGoogle Scholar |
Sehnal L, Procházková T, Smutná M, Kohoutek J, Lepšová-Skácelová O, Hilscherová K (2019). Widespread occurrence of retinoids in water bodies associated with cyanobacterial blooms dominated by diverse species. Water Research 156, 136–147.
| Widespread occurrence of retinoids in water bodies associated with cyanobacterial blooms dominated by diverse species.Crossref | GoogleScholarGoogle Scholar |
Smutná M, Priebojová J, Večerková J, Hilscherová K (2017). Retinoid-like compounds produced by phytoplankton affect embryonic development of Xenopus laevis. Ecotoxicology and Environmental Safety 138, 32–38.
| Retinoid-like compounds produced by phytoplankton affect embryonic development of Xenopus laevis.Crossref | GoogleScholarGoogle Scholar |
van Breemen RB, Nikolic D, Xu X, Xiong Y, van Lieshout M, West CE, Schilling AB (1998). Development of a method for quantitation of retinol and retinyl palmitate in human serum using high-performance liquid chromatography–atmospheric pressure chemical ionization–mass spectrometry. Journal of Chromatography A 794, 245–251.
| Development of a method for quantitation of retinol and retinyl palmitate in human serum using high-performance liquid chromatography–atmospheric pressure chemical ionization–mass spectrometry.Crossref | GoogleScholarGoogle Scholar |
Wu X, Jiang J, Wan Y, Giesy JP, Hu J (2012). Cyanobacteria blooms produce teratogenic retinoic acids. Proceedings of the National Academy of Sciences 109, 9477–9482.
| Cyanobacteria blooms produce teratogenic retinoic acids.Crossref | GoogleScholarGoogle Scholar |
Yeung KWY, Zhou G-J, Hilscherová K, Giesy JP, Leung KMY (2020). Current understanding of potential ecological risks of retinoic acids and their metabolites in aquatic environments. Environment International 136, 105464
| Current understanding of potential ecological risks of retinoic acids and their metabolites in aquatic environments.Crossref | GoogleScholarGoogle Scholar |
Yeung KWY, Zhou G-J, Ruan Y, Lam PKS, Leung KMY (2021). Occurrence of retinoic acids and their metabolites in sewage and their removal efficiencies by chemically enhanced primary treatment and secondary biological treatment. Chemosphere 280, 130745
| Occurrence of retinoic acids and their metabolites in sewage and their removal efficiencies by chemically enhanced primary treatment and secondary biological treatment.Crossref | GoogleScholarGoogle Scholar |
Yeung KWY, Ho KKY, Zhou G-J, Ruan Y, Lam PKS, Leung KMY (2022a). Spatiotemporal variations of retinoic acids and their metabolites in the marine environment of Hong Kong. Marine Pollution Bulletin 181, 113878
| Spatiotemporal variations of retinoic acids and their metabolites in the marine environment of Hong Kong.Crossref | GoogleScholarGoogle Scholar |
Yeung KWY, Lai RWS, Zhou G-J, Leung KMY (2022b). Concentration-response of six marine species to all-trans-retinoic acid and its ecological risk to the marine environment. Ecotoxicology and Environmental Safety 235, 113455
| Concentration-response of six marine species to all-trans-retinoic acid and its ecological risk to the marine environment.Crossref | GoogleScholarGoogle Scholar |
Ying GG, Kookana RS (2003). Degradation of five selected endocrine-disrupting chemicals in seawater and marine sediment. Environmental Science & Technology 37, 1256–1260.
| Degradation of five selected endocrine-disrupting chemicals in seawater and marine sediment.Crossref | GoogleScholarGoogle Scholar |
Zhen H, Wu X, Hu J, Xiao Y, Yang M, Hirotsuji J, Nishikawa J-I, Nakanishi T, Ike M (2009). Identification of retinoic acid receptor agonists in sewage treatment plants. Environmental Science & Technology 43, 6611–6616.
| Identification of retinoic acid receptor agonists in sewage treatment plants.Crossref | GoogleScholarGoogle Scholar |
Zhou G-J, Li XY, Leung KMY (2019). Retinoids and oestrogenic endocrine disrupting chemicals in saline sewage treatment plants: Removal efficiencies and ecological risks to marine organisms. Environment International 127, 103–113.
| Retinoids and oestrogenic endocrine disrupting chemicals in saline sewage treatment plants: Removal efficiencies and ecological risks to marine organisms.Crossref | GoogleScholarGoogle Scholar |
Zhou G-J, Ho KKY, Ip JCH, Liu S, Hu J, Giesy JP, Leung KMY (2021). Insights into the influence of natural retinoic acids on imposex induction in female marine gastropods in the coastal environment. Environmental Science & Technology Letters 8, 1002–1008.
| Insights into the influence of natural retinoic acids on imposex induction in female marine gastropods in the coastal environment.Crossref | GoogleScholarGoogle Scholar |
