A novel Oocystis algal strain enables highly efficient simultaneous biodegradation of bisphenol A and carbon capture in seawater

Abstract

The removal of bisphenol A (BPA) in seawater using microalgae is still a challenge due to the low removal efficiency and weak tolerance. A novel Oocystis algal strain was isolated for BPA removal with an efficiency (> 98%) over two times higher than that of the common microalgae Chlorella (42.8%). The maximal carbon capture rate of Oocystis was 0.16 g/(L·d) which was much higher than that of Chlorella (0.06 g/(L·d)). The BPA removal fitted a first-order kinetic model and Oocystis showed a maximum removal rate of 29.80 μg/(L·d) at a BPA concentration of 2000 μg/L. The new Oocystis strain had a wide range of pH adaptability for BPA removal. The sharp increase in peroxidase (POD) activity indicated its involvement in BPA degradation. Transcriptome analysis showed that BPA mainly affected the photosynthesis-related genes while the engagement of glutathione POD in the BPA biodegradation was confirmed. BPA could also serve as growth promoter for Oocystis during the removal process, which subsequently enhanced the growth and carbon capture. BPA could be removed by the Oocystis strain through hydroxylation, demethylation, and conjugation. The Oocystis strain still maintained high BPA removal efficiency (100%) and carbon capture rate (0.2 g/(L·d)) in the pilot-scale tailwater treatment system, illustrating microalgal processes were efficient for marine pollution control. This study also provides new ideas for developing low-cost carbon capture technologies to achieve the goal of carbon neutrality.

Graphical abstract

Keywords

Oocystis / Micropollutant / Stress response / Degradation / Transcriptome analysis / Carbon capture

Highlight

	● Oocystis obtained high BPA removal rate and carbon capture rate.
	● SOD/POD activity of the Oocystis was much higher than that of the Chlorella .
	● The engagement of POD and photosynthesis damage occurred during BPA biodegradation.
	● BPA could serve as growth promoter for Oocystis during the BPA removal process.
	● BPA was mainly removed through hydroxylation, demethylation, and conjugation.

References

[1] Azizullah A, Khan S, Gao G, Gao K S. (2022). The interplay between bisphenol A and algae: a review. Journal of King Saud University - Science, 34(5): 102050

[2] Bai L L, Liu X, Wu Y Q, Wang C L, Wang C H, Jiang H L. (2024). Ecological determinants of 17α-ethynylestradiol biodegradation: unveiling unique microbial community assemblages in lake sediments under nitrate or sulfate reduction. Journal of Cleaner Production, 446: 141400

[3] Barber J, Nield J, Morris E P, Zheleva D, Hankamer B. (1997). The structure, function and dynamics of photosystem two. Physiologia Plantarum, 100(4): 817–827

[4] Ben Ali R, Ben Ouada S, Leboulanger C, Ammar J, Sayadi S, Ben Ouada H. (2021). Bisphenol A removal by the Chlorophyta Picocystis sp.: optimization and kinetic study. International Journal of Phytoremediation, 23(8): 818–828

[5] Ben Ouada S, Ben Ali R, Leboulanger C, Ben Ouada H, Sayadi S. (2018a). Effect of bisphenol A on the extremophilic microalgal strain Picocystis sp. (Chlorophyta) and its high BPA removal ability. Ecotoxicology and Environmental Safety, 158: 1–8

[6] Ben Ouada S, Ben Ali R, Leboulanger C, Zaghden H, Choura S, Ben Ouada H, Sayadi S. (2018b). Effect and removal of bisphenol A by two extremophilic microalgal strains (Chlorophyta). Journal of Applied Phycology, 30(3): 1765–1776

[7] Cai Z Q, Hao X D, Sun X B, Du P H, Liu W, Fu J. (2019). Highly active WO₃@anatase-SiO₂ aerogel for solar-light-driven phenanthrene degradation: mechanism insight and toxicity assessment. Water Research, 162: 369–382

[8] Cao C S, Wang J Z, Yu X Y, Zhang Y Q, Zhu L Y. (2020). Photodegradation of seven bisphenol analogues by Bi₅O₇I/UiO-67 heterojunction: relationship between the chemical structures and removal efficiency. Applied Catalysis B: Environmental, 277: 119222

[9] Carbó M, Chaturvedi P, Álvarez A, Pineda-Cevallos D, Ghatak A, González P R, Cañal M J, Weckwerth W, Valledor L. (2023). Ferroptosis is the key cellular process mediating bisphenol A responses in Chlamydomonas and a promising target for enhancing microalgae-based bioremediation. Journal of Hazardous Materials, 448: 130997

[10] Chen D, Kannan K, Tan H L, Zheng Z G, Feng Y L, Wu Y, Widelka M. (2016). Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity: a review. Environmental Science & Technology, 50(11): 5438–5453

[11] Diao Z H, Dong F X, Yan L, Chen Z L, Qian W, Kong L J, Zhang Z W, Zhang T, Tao X Q, Du J J. . (2020). Synergistic oxidation of Bisphenol A in a heterogeneous ultrasound-enhanced sludge biochar catalyst/persulfate process: reactivity and mechanism. Journal of Hazardous Materials, 384: 121385

[12] Drira M, Ben Mohamed J, Ben Hlima H, Hentati F, Michaud P, Abdelkafi S, Fendri I. (2021). Improvement of Arabidopsis thaliana salt tolerance using a polysaccharidic extract from the brown algae Padina pavonica. Algal Research, 56: 102324

[13] Duarte J H, de Morais E G, Radmann E M, Costa J A V. (2017). Biological CO₂ mitigation from coal power plant by Chlorella fusca and Spirulina sp. Bioresource Technology, 234: 472–475

[14] Eio E J, Kawai M, Niwa C, Ito M, Yamamoto S, Toda T. (2015). Biodegradation of bisphenol A by an algal-bacterial system. Environmental Science and Pollution Research, 22(19): 15145–15153

[15] Eltoukhy A, Jia Y, Nahurira R, Abo-Kadoum M A, Khokhar I, Wang J H, Yan Y C. (2020). Biodegradation of endocrine disruptor bisphenol A by Pseudomonas putida strain YC-AE1 isolated from polluted soil, Guangdong, China. BMC Microbiology, 20(1): 11

[16] Fu W X, Li X E, Yang Y R, Song D H. (2023). Enhanced degradation of bisphenol A: influence of optimization of removal, kinetic model studies, application of machine learning and microalgae-bacteria consortia. Science of the Total Environment, 858: 159876

[17] GuillardR R L (1975). Culture of phytoplankton for feeding marine invertebrates. In: Smith W L, Chanley M H, eds. Culture of Marine Invertebrate Animals. Boston: Springer, 29–60

[18] Ha G S, Sim M G, Jeon B H, Baek G. (2025). Bioremediation of perfluorooctanoic acid using microalgae with a transcriptomic approach. Journal of Hazardous Materials, 488: 137508

[19] Haddad J J, Harb H L. (2005). L-γ-Glutamyl-L-cysteinyl-glycine (glutathione; GSH) and GSH-related enzymes in the regulation of pro- and anti-inflammatory cytokines: a signaling transcriptional scenario for redox(y) immunologic sensor(s)?. Molecular Immunology, 42(9): 987–1014

[20] Helal M, Liu M, Chen H H, Fang M L, Qiu W H, Kjeldsen F, Tollefsen K E, Thiyagarajan V, Holbech H, Xu E G. (2024). Multi-omics in nanoplastic research: a spotlight on aquatic life. Frontiers of Environmental Science & Engineering, 18(11): 133

[21] HerreraMRoca M (2023). Microalgal chlorophylls for food/feed applications. In: Jacob-Lopes E, Queiroz M I, Maroneze M M, Zepka L Q, eds. Handbook of Food and Feed from Microalgae. London: Academic Press, 147–160

[22] Hou S Y, Yang P. (2022). BPA biodegradation driven by isolated strain SQ-2 and its metabolism mechanism elucidation. Biochemical Engineering Journal, 185: 108540

[23] Ifuku K, Ido K, Sato F. (2011). Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex. Journal of Photochemistry and Photobiology B: Biology, 104(1−2): 158–164

[24] Im J, Löffler F E. (2016). Fate of bisphenol A in terrestrial and aquatic environments. Environmental Science & Technology, 50(16): 8403–8416

[25] Ji M K, Kabra A N, Choi J, Hwang J H, Kim J R, Abou-Shanab R A I, Oh Y K, Jeon B H. (2014). Biodegradation of bisphenol A by the freshwater microalgae Chlamydomonas mexicana and Chlorella vulgaris. Ecological Engineering, 73: 260–269

[26] Jia D Q, Li Q Z, Hanna K, Mailhot G, Brigante M. (2021). Efficient removal of estrogenic compounds in water by Mn^III-activated peroxymonosulfate: mechanisms and application in sewage treatment plant water. Environmental Pollution, 288: 117728

[27] Khan N G, Correia J, Adiga D, Rai P S, Dsouza H S, Chakrabarty S, Kabekkodu S P. (2021). A comprehensive review on the carcinogenic potential of bisphenol A: clues and evidence. Environmental Science and Pollution Research, 28(16): 19643–19663

[28] Kyrila G, Katsoulas A, Schoretsaniti V, Rigopoulos A, Rizou E, Doulgeridou S, Sarli V, Samanidou V, Touraki M. (2021). Bisphenol A removal and degradation pathways in microorganisms with probiotic properties. Journal of Hazardous Materials, 413: 125363

[29] Li M Q, Luo R, Wang C H, Zhang M, Zhang W X, Klu P K, Yan Y B, Qi J W, Sun X Y, Wang L J. . (2019). Iron-tannic modified cotton derived Fe⁰/graphitized carbon with enhanced catalytic activity for bisphenol A degradation. Chemical Engineering Journal, 372: 774–784

[30] Liao C, Kannan K (2012). Determination of free and conjugated forms of bisphenol A in human urine and serum by liquid chromatography: tandem mass spectrometry. Environmental Science & Technology, 46(9): 5003–5009

[31] Li R, Chen G Z, Tam N F Y, Luan T G, Shin P K S, Cheung S G, Liu Y. (2009). Toxicity of bisphenol A and its bioaccumulation and removal by a marine microalga Stephanodiscus hantzschii. Ecotoxicology and Environmental Safety, 72(2): 321–328

[32] Lin J W, Hu Y Y, Wang L X, Liang D H, Ruan X, Shao S C. (2020). M88/PS/Vis system for degradation of bisphenol A: environmental factors, degradation pathways, and toxicity evaluation. Chemical Engineering Journal, 382: 122931

[33] Liu M, Huang X H, Li C L, Gu B H. (2020). Study on the uptake of dissolved nitrogen by Oocystis borgei in prawn (Litopenaeus vannamei) aquaculture ponds and establishment of uptake model. Aquaculture International, 28(4): 1445–1458

[34] Loffredo E, Traversa A, Senesi N. (2012). Biodecontamination of water from bisphenol A using ligninolytic fungi and the modulation role of humic acids. Ecotoxicology and Environmental Safety, 79: 288–293

[35] LouatiIDammak MNasriRBelbahriLNasriM AbdelkafiSMechichi T (2019). Biodegradation and detoxification of bisphenol A by bacteria isolated from desert soils. 3 Biotech, 9(6): 228

[36] Lu J, Wu J, Stoffella P J, Wilson P C. (2015). Uptake and distribution of bisphenol A and nonylphenol in vegetable crops irrigated with reclaimed water. Journal of Hazardous Materials, 283: 865–870

[37] Lu J, Wu J, Zhang C, Wang J H, He X. (2024). Occurrence and possible sources of antibiotic resistance genes in seawater of the South China Sea. Frontiers of Environmental Science & Engineering, 18(9): 108

[38] Lu J, Zhang C, Wu J. (2022). Removal of steroid hormones from mariculture system using seaweed Caulerpa lentillifera. Frontiers of Environmental Science & Engineering, 16(2): 15

[39] Ma Y X, Yan F, An L L, Shen W D, Tang T T, Li Z H, Dai R H. (2023). Transcriptome analysis of changes in M. aeruginosa growth and microcystin production under low concentrations of ethinyl estradiol. Science of the Total Environment, 859: 160226

[40] May M J, Vernoux T, Leaver C, van Montagu M, Inzé D. (1998). Glutathione homeostasis in plants: implications for environmental sensing and plant development. Journal of Experimental Botany, 49(321): 649–667

[41] Niavarani Z, Breite D, Yasir M, Sedlarik V, Prager A, Schönherr N, Abel B, Gläser R, Schulze A. (2024). Removal of endocrine disrupting chemicals from water through urethane functionalization of microfiltration membranes via electron beam irradiation. Frontiers of Environmental Science & Engineering, 18(4): 45

[42] Nzayisenga J C, Farge X, Groll S L, Sellstedt A. (2020). Effects of light intensity on growth and lipid production in microalgae grown in wastewater. Biotechnology for Biofuels, 13(1): 4

[43] Perez-Garcia O, Escalante F M E, de-Bashan L E, Bashan Y. (2011). Heterotrophic cultures of microalgae: metabolism and potential products. Water Research, 45(1): 11–36

[44] Popelkova H, Yocum C F. (2011). PsbO, the manganese-stabilizing protein: analysis of the structure–function relations that provide insights into its role in photosystem II. Journal of Photochemistry and Photobiology B: Biology, 104(1−2): 179–190

[45] Ruiz J, Wijffels R H, Dominguez M, Barbosa M J. (2022). Heterotrophic vs autotrophic production of microalgae: bringing some light into the everlasting cost controversy. Algal Research, 64: 102698

[46] Swiatek M, Kuras R, Sokolenko A, Higgs D, Olive J, Cinque G, Müller B, Eichacker L A, Stern D B, Bassi R. . (2001). The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. The Plant Cell, 13(6): 1347–1368

[47] Usman M, Ahmed A, Ji Z J, Yu B, Shen Y Q, Cong H L. (2021). Environmentally friendly fabrication of new β-Cyclodextrin/ZrO₂ nanocomposite for simultaneous removal of Pb(II) and BPA from water. Science of the Total Environment, 784: 147207

[48] Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M. (2006). Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety, 64(2): 178–189

[49] Wang R, Diao P P, Chen Q, Wu H, Xu N, Duan S S. (2017). Identification of novel pathways for biodegradation of bisphenol A by the green alga Desmodesmus sp. WR1, combined with mechanistic analysis at the transcriptome level. Chemical Engineering Journal, 321: 424–431

[50] Wei S J, Zhuang G J, Cheng L R J, Wang S B. (2022). The proliferation rule of Microcystis aeruginosa under different initial pH conditions and its influence on the pH value of the environment. Environmental Science and Pollution Research, 29(10): 13835–13844

[51] Wu J, Lu J, Wu J. (2022). Adsorption and desorption of steroid hormones on saline soil. Frontiers of Environmental Science & Engineering, 16(11): 140

[52] Xiong J K, An T C, Li G Y, Peng P A. (2017). Accelerated biodegradation of BPA in water-sediment microcosms with Bacillus sp. GZB and the associated bacterial community structure. Chemosphere, 184: 120–126

[53] Xiong J K, Li G Y, An T C, Zhang C S, Wei C H. (2016a). Emission patterns and risk assessment of polybrominated diphenyl ethers and bromophenols in water and sediments from the Beijiang River, South China. Environmental Pollution, 219: 596–603

[54] Xiong J Q, Kurade M B, Abou-Shanab R A I, Ji M K, Choi J, Kim J O, Jeon B H. (2016b). Biodegradation of carbamazepine using freshwater microalgae Chlamydomonas mexicana and Scenedesmus obliquus and the determination of its metabolic fate. Bioresource Technology, 205: 183–190

[55] Zhang A H, Fang S H, Xi H, Huang J K, Li Y F, Ma G Y, Zhang J F. (2023a). Highly efficient and selective removal of phosphate from wastewater of sea cucumber aquaculture for microalgae culture using a new adsorption-membrane separation-coordinated strategy. Frontiers of Environmental Science & Engineering, 17(10): 120

[56] Zhang C, Lu J, Wu J. (2021). Enhanced removal of phenolic endocrine disrupting chemicals from coastal waters by intertidal macroalgae. Journal of Hazardous Materials, 411: 125105

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

[58] Zhang G S, Wang Y, Jiang J H, Yang S. (2017). Bisphenol A removal by submerged macrophytes and the contribution of epiphytic microorganisms to the removal process. Bulletin of Environmental Contamination and Toxicology, 98(6): 770–775

[59] Zhang H G, Du L, Xing J J, Wei G L, Quan X. (2023b). Electro-conductive crosslinked polyaniline/carbon nanotube nanofiltration membrane for electro-enhanced removal of bisphenol A. Frontiers of Environmental Science & Engineering, 17(5): 59

[60] Zhang L Y, Yang G J, Hasan H A, Fan J, Ji B. (2023c). Adaptation mechanisms of microalgal-bacterial granular sludge to outdoor light-limited conditions. Environmental Research, 239: 117244

[61] Zhao H D, Liu M, Yang J J, Chen Y Y, Fang M L. (2023). Time-dependent metabolomics uncover dynamic metabolic adaptions in MCF-7 cells exposed to bisphenol A. Frontiers of Environmental Science & Engineering, 17(1): 4

[62] Zheng R, Zhang K, Kong L R, Liu S T. (2024). Research progress and prospect of low-carbon biological technology for nitrate removal in wastewater treatment. Frontiers of Environmental Science & Engineering, 18(7): 80

RIGHTS & PERMISSIONS

Higher Education Press