Removal of steroid hormones from mariculture system using seaweed Caulerpa lentillifera

Abstract

•Steroid hormones could be removed efficiently from mariculture system using seaweed;

• Caulerpa lentillifera was the most efficient seaweed for removal of steroid hormones;

• More than 90% of E₂ or EE₂ were removed within 12 h using Caulerpa lentillifera;

• The removal included the rapid biosorption and the slow bio-accumulation;

•The hormones and nutrients in mariculture wastewater could be simultaneously removed.

The removal of steroid hormones from the mariculture system using seaweeds (Caulerpa lentillifera, Ulva pertusa, Gracilaria lemaneiformis, and Codium fragile) was investigated. The results illustrated that both 17β-estradiol (E₂) and 17α-ethinylestradiol (EE₂) could be removed by the seaweeds at different levels, and the Caulerpa lentillifera was the most efficient one. More than 90% of E₂ or EE₂ at concentration of 10 μg/L was removed by Caulerpa lentillifera within 12 h. Processes including initial quick biosorption, the following slow accumulation, and biodegradation might explain the removal mechanisms of E₂/EE₂ by Caulerpa lentillifera. E₂/EE₂ removal was positively related to the nutrient level and the initial concentration of steroid hormone. A significant linear relationship for E₂ and EE₂ existed between the initial pollutant concentration and the average removal rate. The highest removal kinetic constant (k) value was obtained at 30°C as 0.34 /h for E₂ and at 20°C as 0.28 /h for EE₂, demonstrating the promising application potential of Caulerpa lentillifera in the water purification of the industrialized mariculture system with relatively high water temperature. Simultaneous and efficient removal of E₂ and EE₂ by Caulerpa lentillifera was still achieved after 3 cycles in the pilot-scale experiment. The steroid hormones and nutrients in mariculture wastewater could also be simultaneously removed using Caulerpa lentillifera. These findings demonstrated that Caulerpa lentillifera was the promising seaweed for the removal of steroid hormones in mariculture systems.

Graphical abstract

Keywords

Phycoremediation / Steroid hormones / Seaweed / Mariculture / Caulerpa lentillifera

References

[1] Bennett J L, Mackie A L, Park Y, Gagnon G A (2018). Advanced oxidation processes for treatment of 17β-estradiol and its metabolites in aquaculture wastewater. Aquacultural Engineering, 83: 40–46

[2] Cahill P L, Hurd C L, Lokman M (2010). Keeping the water clean-Seaweed biofiltration outperforms traditional bacterial biofilms in recirculating aquaculture. Aquaculture (Amsterdam, Netherlands), 306(1–4): 153–159

[3] Cheng Q, Jiang Y, Jin Z, Hui C, Xu L, Zhou Q, Zhao Y, Du L, Jiang H (2020). Enhanced excretion of extracellular polymeric substances associated with nonylphenol tolerance in Dictyosphaerium sp. Journal of Hazardous Materials, 395: 122644

[4] Dobson G T, Duy N D Q, Paul N A, Southgate P C (2020). Assessing potential for integrating sea grape (Caulerpa lentillifera) culture with sandfish (Holothuria scabra) and Babylon snail (Babylonia areolata) co-culture. Aquaculture (Amsterdam, Netherlands), 522: 735153

[5] Gong L, Zhang S, Chen D, Liu K, Lu J (2018). Response of biofilms-leaves of two submerged macrophytes to high ammonium. Chemosphere, 192: 152–160

[6] Good C, Davidson J, Earley R L, Lee E, Summerfelt S (2014). The Impact of water exchange rate and treatment processes on water-borne hormones in recirculation aquaculture systems containing sexually maturing Atlantic salmon salmo salar. Journal of Aquaculture Research & Development, 05(05): 1–7

[7] Guo H, Yao J, Sun Z, Duan D (2015a). Effect of temperature, irradiance on the growth of the green alga Caulerpa lentillifera (Bryopsidophyceae, Chlorophyta). Journal of Applied Phycology, 27(2): 879–885

[8] Guo H, Yao J T, Sun Z M, Duan D L (2015b). Effects of salinity and nutrients on the growth and chlorophyll fluorescence of Caulerpa lentillifera. Chinese Journal of Oceanology and Limnology, 33(2): 410–418

[9] Hom-Diaz A, Llorca M, Rodríguez-Mozaz S, Vicent T, Barceló D, Blánquez P (2015). Microalgae cultivation on wastewater digestate: β-estradiol and 17α-ethynylestradiol degradation and transformation products identification. Journal of Environmental Management, 155: 106–113

[10] Huang B, Tang J, He H, Gu L, Pan X (2019). Ecotoxicological effects and removal of 17β-estradiol in chlorella algae. Ecotoxicology and Environmental Safety, 174: 377–383

[11] Kakinuma M, Coury D A, Kuno Y, Itoh S, Kozawa Y, Inagaki E, Yoshiura Y, Amano H (2006). Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Marine Biology, 149(1): 97–106

[12] Liu W, Chen Q, He N, Sun K, Sun D, Wu X, Duan S (2018). Removal and biodegradation of 17β-estradiol and diethylstilbestrol by the freshwater microalgae Raphidocelis subcapitata. International Journal of Environmental Research and Public Health, 15(3): 452–465

[13] Lu J, Lin Y, Wu J, Zhang C (2020f). Continental-scale spatial distribution, sources, and health risks of heavy metals in seafood: challenge for the water-food-energy nexus sustainability in coastal regions? Environmental Science and Pollution Research International,

[14] Lu J, Sun Q, Wu J, Zhu G (2020e). Enhanced ozonation of antibiotics using magnetic Mg(OH)₂ nanoparticles made through magnesium recovery from discarded bischofite. Chemosphere, 238: 124694

[15] Lu J, Wu J, Wu J, Zhang C, Luo Y (2020g). Adsorption and desorption of steroid hormones by microplastics in seawater. Bulletin of Environmental Contamination and Toxicology,

[16] Lu J, Wu J, Zhang C, Zhang Y (2020c). Possible effect of submarine groundwater discharge on the pollution of coastal water: Occurrence, source, and risks of endocrine disrupting chemicals in coastal groundwater and adjacent seawater influenced by reclaimed water irrigation. Chemosphere, 250: 126323

[17] Lu J, Wu J, Zhang C, Zhang Y, Lin Y, Luo Y (2018). Occurrence, distribution, and ecological-health risks of selected antibiotics in coastal waters along the coastline of China. Science of the Total Environment, 644: 1469–1476

[18] Lu J, Zhang C, Wu J, Zhang Y, Lin Y (2020b). Seasonal distribution, risks, and sources of endocrine disrupting chemicals in coastal waters: Will these emerging contaminants pose potential risks in marine environment at continental-scale? Chemosphere, 247: 125907

[19] Lu J, Zhang Y, Wu J, Wang J (2020a). Nitrogen removal in recirculating aquaculture water with high dissolved oxygen conditions using the simultaneous partial nitrification, anammox and denitrification system. Bioresource Technology, 305: 123037

[20] Lu J, Zhang Y, Wu J, Wang J, Cai Y (2020d). Fate of antibiotic resistance genes in reclaimed water reuse system with integrated membrane process. Journal of Hazardous Materials, 382: 121025

[21] Miklos D B, Hartl R, Michel P, Linden K G, Drewes J E, Hubner U (2018). UV/H₂O₂ process stability and pilot-scale validation for trace organic chemical removal from wastewater treatment plant effluents. Water Research, 136: 169–179

[22] Mota V C, Martins C I M, Eding E H, Canário A V M, Verreth J A J (2014). Steroids accumulate in the rearing water of commercial recirculating aquaculture systems. Aquacultural Engineering, 62: 9–16

[23] Neori A, Chopin T, Troell M, Buschmann A H, Kraemer G P, Halling C, Shpigel M, Yarish C (2004). Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture (Amsterdam, Netherlands), 231(1–4): 361–391

[24] Ocharoen Y, Boonphakdee C, Boonphakdee T, Shinn A P, Moonmangmee S (2018). High levels of the endocrine disruptors bisphenol-A and 17β-estradiol detected in populations of green mussel, Perna viridis, cultured in the Gulf of Thailand. Aquaculture (Amsterdam, Netherlands), 497: 348–356

[25] Park Y, Alayafi A, Bennett J L, Malloy D, Smith P M, Ross N W, Gagnon G A, Donaldson A A (2019). Modeling the fate of dietary 17B-estradiol and its metabolites in an American eel (Anguilla rostrata) recirculating aquaculture system. Aquacultural Engineering, 86: 101995

[26] Simerský R, Novák O, Morris D A, Pouzar V, Strnad M (2009). Identification and quantification of several mammalian steroid hormones in plants by UPLC-MS/MS. Journal of Plant Growth Regulation, 28(2): 125–136

[27] Solé A, Matamoros V (2016). Removal of endocrine disrupting compounds from wastewater by microalgae co-immobilized in alginate beads. Chemosphere, 164: 516–523

[28] Teoh M L, Chu W L, Phang S M (2010). Effect of temperature change on physiology and biochemistry of algae: A review. Malaysian Journal of Science, 29(2): 82–97

[29] Wang J, Lu J, Zhang Y, Wu J, Zhang C, Yu X, Zhang Z, Liu H, Wang W (2018). High-throughput sequencing analysis of the microbial community in coastal intensive mariculture systems. Aquacultural Engineering, 83: 93–102

[30] Wang Y, Sun Q, Li Y, Wang H, Wu K, Yu C P (2019). Biotransformation of estrone, 17β-estradiol and 17α-ethynylestradiol by four species of microalgae. Ecotoxicology and Environmental Safety, 180: 723–732

[31] Weber S, Leuschner P, Kämpfer P, Dott W, Hollender J (2005). Degradation of estradiol and ethinyl estradiol by activated sludge and by a defined mixed culture. Applied Microbiology and Biotechnology, 67(1): 106–112

[32] Yokoyama H, Ishihi Y (2010). Bioindicator and biofilter function of Ulva spp. (Chlorophyta) for dissolved inorganic nitrogen discharged from a coastal fish farm—potential role in integrated multi-trophic aquaculture. Aquaculture (Amsterdam, Netherlands), 310(1-2): 74–83

[33] Zhang C, Lu J, Wu J, Luo Y (2019). Phycoremediation of coastal waters contaminated with bisphenol A by green tidal algae Ulva prolifera. Science of the Total Environment, 661: 55–62

[34] Zhang M, Lu J, He Y, Wilson P C (2016). Photocatalytic degradation of polybrominated diphenyl ethers in pure water system. Frontiers of Environmental Science & Engineering, 10(2): 229–235

[35] Zhang Y, Habteselassie M Y, Resurreccion E P, Mantripragada V, Peng S, Bauer S, Colosi L M (2014). Evaluating removal of steroid estrogens by a model alga as a possible sustainability benefit of hypothetical integrated algae cultivation and wastewater treatment systems. ACS Sustainable Chemistry & Engineering, 2(11): 2544–2553

RIGHTS & PERMISSIONS

Higher Education Press