Abstract
Crude oil spills imperil aquatic ecosystems globally, prompting innovative solutions such as microalgae-based bioremediation. The potential of Tetradesmus obliquus and Desmodesmus armatus for crude oil spill bioremediation is investigated in this study. Under mixotrophic conditions and varying crude oil concentrations (0.5 to 2%), both species showed decent resistance, sustaining growth, and adaptation at low crude oil exposure levels below 1%. Both algae exhibited peak growth rates at a 0.5% crude oil concentration. In T. obliquus, chlorophyll-a levels increased with 0.5% crude oil exposure, while chlorophyll-b and carotenoid levels remained fairly consistent. Conversely, D. armatus exhibited variable chlorophyll-a and carotenoid levels at the 0.5% crude oil concentration, accompanied by an uptick in chlorophyll-b levels. GC/MS analyses revealed that T. obliquus efficiently degraded aliphatic compounds like undecane, tridecane, and pentadecane. Additionally, T. obliquus outperformed D. armatus in degrading both aliphatic and aromatic hydrocarbons. The study identifies the modified Richards model efficacy for T. obliquus, while the Baranyi-Roberts model exhibited superiority for D. armatus as optimal for representing growth kinetics in response to crude oil exposure. This insight is crucial for tailored bioremediation strategies, emphasizing species-specific adaptability and concentration considerations. Overall, the study provides vital information for designing targeted approaches to address crude oil contamination challenges, contributing to effective environmental restoration in contaminated ecosystems.
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Abreu, A. P., Morais, R. C., Teixeira, J. A., & Nunes, J. (2022). A comparison between microalgal autotrophic growth and metabolite accumulation with heterotrophic, mixotrophic and photoheterotrophic cultivation modes. Renewable and Sustainable Energy Reviews, 159, 112247. https://doi.org/10.1016/j.rser.2022.112247
Ahmad, I. (2022). Microalgae–Bacteria Consortia: A review on the degradation of polycyclic aromatic hydrocarbons (PAHs). Arabian Journal for Science and Engineering, 47(1), 19–43. https://doi.org/10.1007/s13369-021-06236-9
Akaike, H. (1969). Fitting autoregressive models for prediction. Annals of the Institute of Statistical Mathematics, 21(1), 243–247. https://doi.org/10.1007/BF02532251
Almeda, R., Wambaugh, Z., Wang, Z., Hyatt, C., Liu, Z., & Buskey, E. J. (2013). Interactions between Zooplankton and crude oil: toxic effects and bioaccumulation of polycyclic aromatic hydrocarbons. Plos One, 8(6), 1–21. https://doi.org/10.1371/journal.pone.0067212
Ashraf, N., Ahmad, F., & Lu, Y. (2023). Synergy between microalgae and microbiome in polluted waters. Trends in Microbiology, 31(1), 9–21. https://doi.org/10.1016/j.tim.2022.06.004
Atlas, R., & Bragg, J. (2009). Bioremediation of marine oil spills: when and when not – the Exxon Valdez experience. Microbial Biotechnology, 2(2), 213–221. https://doi.org/10.1111/j.1751-7915.2008.00079.x
Bacaër, N. (2011). Verhulst and the logistic equation (1838). In A Short History of Mathematical Population Dynamics (pp. 35–39). Springer. https://doi.org/10.1007/978-0-85729-115-8_6
Banerjee, C., Singh, P. K., & Shukla, P. (2016). Microalgal bioengineering for sustainable energy development: Recent transgenesis and metabolic engineering strategies. Biotechnology Journal, 11(3), 303–314. https://doi.org/10.1002/biot.201500284
Baranyi, J., & Roberts, T. A. (1994). A dynamic approach to predicting bacterial growth in food. International Journal of Food Microbiology, 23(3–4), 277–294. https://doi.org/10.1016/0168-1605(94)90157-0
Borde, X., Guieysse, B., Delgado, O., Muoz, R., Hatti-Kaul, R., Nugier-Chauvin, C., Patin, H., & Mattiasson, B. (2003). Synergistic relationships in algal–bacterial microcosms for the treatment of aromatic pollutants. Bioresource Technology, 86(3), 293–300. https://doi.org/10.1016/S0960-8524(02)00074-3
Bretherton, L., Hillhouse, J., Kamalanathan, M., Finkel, Z. V., Irwin, A. J., & Quigg, A. (2020). Trait-dependent variability of the response of marine phytoplankton to oil and dispersant exposure. Marine Pollution Bulletin, 153, 110906. https://doi.org/10.1016/J.MARPOLBUL.2020.110906
Calderón-Delgado, I. C., Mora-Solarte, D. A., & Velasco-Santamaría, Y. M. (2019). Physiological and enzymatic responses of Chlorella vulgaris exposed to produced water and its potential for bioremediation. Environmental Monitoring and Assessment, 191(6), 399. https://doi.org/10.1007/s10661-019-7519-8
Cao, X., **ong, Y., Lund, J., Mao, J., & Christensen, K. (2013). The effects of microalgae characteristics on the bioremediation rate of emulsified oil. Journal of Emerging Investigations, 1–7 https://api.semanticscholar.org/CorpusID:51945946
Castillo, T., Ramos, D., García-Beltrán, T., Brito-Bazan, M., & Galindo, E. (2021). Mixotrophic cultivation of microalgae: An alternative to produce high-value metabolites. Biochemical Engineering Journal, 176, 108183. https://doi.org/10.1016/j.bej.2021.108183
Chatterjee, S. (2015). Oil spill cleanup: Role of environmental biotechnology. In G. Kaushik (Ed.), Applied Environmental Biotechnology: Present Scenario and Future Trends (pp. 129–143). Springer India. https://doi.org/10.1007/978-81-322-2123-4_9
Cohen, S., Stastny, P., & Sontheimer, R. D. (1986). Concurrence of subacute cutaneous lupus erythematosus and rheumatoid arthritis. Arthritis & Rheumatism, 29(3), 421–425. https://doi.org/10.1002/art.1780290318
Del Campo, J. A., García-González, M., & Guerrero, M. G. (2007). Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Applied Microbiology and Biotechnology, 74(6), 1163–1174. https://doi.org/10.1007/s00253-007-0844-9
Effendi Halmi, M., Abd Shukor, M. S., Johari, W. L. W., & Shukor, Y. (2014). Evaluation of several mathematical models for fitting the growth of the algae Dunaliella tertiolecta. Asian Journal of Plant Biology, 2, 1–6. https://doi.org/10.54987/ajpb.v2i1.81
El-Sheekh, M. M., Ghareib, M., & EL-Souod, G. A.-. (2012). Biodegradation of phenolic and polycyclic aromatic compounds by some algae and cyanobacteria. Journal of Bioremediation and Biodegradation, 03(01). https://doi.org/10.4172/2155-6199.1000133
El-Sheekh, M. M., & Hamouda, R. A. (2014). Biodegradation of crude oil by some cyanobacteria under heterotrophic conditions. Desalination and Water Treatment, 52(7–9), 1448–1454. https://doi.org/10.1080/19443994.2013.794008
El-Sheekh, M. M., Hamouda, R. A., & Nizam, A. A. (2013). Biodegradation of crude oil by Scenedesmus obliquus and Chlorella vulgaris growing under heterotrophic conditions. International Biodeterioration & Biodegradation, 82, 67–72. https://doi.org/10.1016/J.IBIOD.2012.12.015
Faisal, M., Nazlina Haiza, M. Y., Mohd, N., & Takriff, M. (2022). Growth kinetics determination using different mathematical models for microalgae Characium sp. UKM1, Chlorella sp. UKM2 and Coelastrella sp. UKM4. ASM Science Journal, 17, 1–12. https://doi.org/10.32802/asmscj.2022.930
Follett, C. L., Dutkiewicz, S., Ribalet, F., Zakem, E., Caron, D., Armbrust, E. V., & Follows, M. J. (2022). Trophic interactions with heterotrophic bacteria limit the range of Prochlorococcus. Proceedings of the National Academy of Sciences, 119(2). https://doi.org/10.1073/pnas.2110993118
Galieriková, A., & Materna, M. (2020). World seaborne trade with oil: One of main cause for oil spills? Transportation Research Procedia, 44, 297–304. https://doi.org/10.1016/J.TRPRO.2020.02.039
Gao, P., Guo, L., Zhao, Y., **, C., She, Z., & Gao, M. (2021). Enhancing microalgae growth and product accumulation with carbon source regulation: New perspective for the coordination between photosynthesis and aerobic respiration. Chemosphere, 278, 130435. https://doi.org/10.1016/j.chemosphere.2021.130435
Ghasemi, Y., Rasoul-Amini, S., & Fotooh-Abadi, E. (2011). The biotransformation, biodegradation, and bioremediation of organic compounds by microalgae 1. Journal of Phycology, 47(5), 969–980. https://doi.org/10.1111/j.1529-8817.2011.01051.x
Ghodrati, M., Kosari-Nasab, M., Zarrini, G., & Movafeghi, A. (2020). Crude oil contamination enhances the lipoxygenase gene expression in the green microalga Scenedesmus dimorphu. Biointerface Research in Applied Chemistry, 11(4), 11431–11439. https://doi.org/10.33263/BRIAC114.1143111439
Gouma, S., Fragoeiro, S., Bastos, A. C., & Magan, N. (2014). Bacterial and fungal bioremediation strategies. Microbial Biodegradation and Bioremediation, 302–323. https://doi.org/10.1016/B978-0-12-800021-2.00013-3
Hamouda, R. A. E. F., Sorour, N. M., & Yeheia, D. S. (2016). Biodegradation of crude oil by Anabaena oryzae, Chlorella kessleri and its consortium under mixotrophic conditions. International Biodeterioration & Biodegradation, 112, 128–134. https://doi.org/10.1016/J.IBIOD.2016.05.001
Hamza, S. A., Wahba, H. M. F., & Hegazy, M. M. (2013). Assessment of handgrip strength variables in a population of egyptian elderly. Middle East Journal of Age and Ageing, 10(3), 19–23. https://doi.org/10.5742/MEJAA.2013.103247
Hanief, S., Prasakti, L., Pradana, Y., Cahyono, R., & Budiman, A. (2020). Growth kinetic of Botryococcus braunii microalgae using logistic and gompertz models. AIP Conference Proceedings, 2296, 20065. https://doi.org/10.1063/5.0030459
Hong, Y., Hu, H. Y., **e, X., & Li, F. M. (2008). Responses of enzymatic antioxidants and non-enzymatic antioxidants in the cyanobacterium Microcystis aeruginosa to the allelochemical ethyl 2-methyl acetoacetate (EMA) isolated from reed (Phragmites communis). Journal of Plant Physiology, 165(12), 1264–1273. https://doi.org/10.1016/J.JPLPH.2007.10.007
Islam, M. S., Senaha, I., Rahman, M. M., Yoda, Y., & Saha, B. B. (2022). Mathematical modelling and statistical optimization of fast cultivation of Agardhiella subulata: response surface methodology. Energy Nexus, 7, 100115. https://doi.org/10.1016/j.nexus.2022.100115
Kalhor, A., Movafeghi, A., Mohammadi-Nassab, A. D., Abedi, E., & Bahrami, A. (2017). Potential of the green alga Chlorella vulgaris for biodegradation of crude oil hydrocarbons. Marine Pollution Bulletin, 123. https://doi.org/10.1016/j.marpolbul.2017.08.045
Praveen, K., Sudharsanam, A., Natarajan, R., & Sambasivam, K. (2018). Biochemical responses from biomass of isolated Chlorella sp., under different cultivation modes: Non-linear modelling of growth kinetics. Brazilian Journal of Chemical Engineering, 35, 489–496. https://doi.org/10.1590/0104-6632.20180352s20170188
Lam, M., Lee, K. T., Khoo, C. G., Uemura, Y., & Lim, J.-W. (2016). Growth kinetic study of chlorella vulgaris using lab-scale and pilot-scale photobioreactor: Effect of CO2 concentration. Journal of Engineering Science and Technology, 11, 93–107 https://api.semanticscholar.org/CorpusID:214587228
Li, H., & Meng, F. (2023). Efficiency, mechanism, influencing factors, and integrated technology of biodegradation for aromatic compounds by microalgae: A review. Environmental Pollution, 335, 122248. https://doi.org/10.1016/j.envpol.2023.122248
Liu, X., Duan, S., Li, A., Xu, N., Cai, Z., & Hu, Z. (2009). Effects of organic carbon sources on growth, photosynthesis, and respiration of Phaeodactylum tricornutum. Journal of Applied Phycology, 21(2), 239–246. https://doi.org/10.1007/s10811-008-9355-z
Ma, X., & Jian, W. (2023). Growth conditions and growth kinetics of Chlorella vulgaris cultured in domestic sewage. Sustainability, 15(3). https://doi.org/10.3390/su15032162
Mohd, N., Yasin, N. H. M., & Takriff, M. S. (2021). Predictive growth model of indigenous green microalgae (Scenedesmus sp. UKM9) in palm oil mill effluent (POME). IOP Conference Series: Materials Science and Engineering, 1051(1), 12070. https://doi.org/10.1088/1757-899X/1051/1/012070
Munoz, R., Guieysse, B., & Mattiasson, B. (2003). Phenanthrene biodegradation by an algal-bacterial consortium in two-phase partitioning bioreactors. Applied Microbiology and Biotechnology, 61, 261–267. https://doi.org/10.1007/s00253-003-1231-9
Okoh, A. (2006). Biodegradation alternative in the cleanup of petroleum hydrocarbon pollutants. Microbiology and Molecular Biology Reviews: MMBR, 1, 38–50 https://api.semanticscholar.org/CorpusID:59474293
Oudot, J. (2000). Biodégradabilité du fuel de l’Erika. Comptes Rendus de l’Académie Des Sciences - Series III - Sciences de La Vie, 323(11), 945–950. https://doi.org/10.1016/S0764-4469(00)01247-6
Pimda, W., & Bunnag, S. (2015). Growth performance and biodegradation of waste motor oil by Nostoc piscinale strain TISTR 8401 in the presence of heavy metals and nutrients as co-contaminants. Journal of the Taiwan Institute of Chemical Engineers, 53, 74–79. https://doi.org/10.1016/j.jtice.2015.02.030
Prince, R. C., Elmendorf, D. L., Lute, J. R., Hsu, C. S., Haith, C. E., Senius, J. D., Dechert, G. J., Douglas, G. S., & Butler, E. L. (1994). 17.alpha.(H)-21.beta.(H)-hopane as a conserved internal marker for estimating the biodegradation of crude oil. Environmental Science & Technology, 28(1), 142–145. https://doi.org/10.1021/es00050a019
Rahman, M. M., Muttakin, M., Pal, A., Shafiullah, A. Z., & Saha, B. B. (2019). A statistical approach to determine optimal models for IUPAC-classified adsorption isotherms. Energies, 12(23). https://doi.org/10.3390/en12234565
Rambabu, K., Avornyo, A., Gomathi, T., Thanigaivelan, A., Show, P. L., & Banat, F. (2023). Phycoremediation for carbon neutrality and circular economy: Potential, trends, and challenges. Bioresource Technology, 367, 128257. https://doi.org/10.1016/j.biortech.2022.128257
Richards, F. J. (1959). A flexible growth function for empirical use. Journal of Experimental Botany, 10(2), 290–301. https://doi.org/10.1093/jxb/10.2.290
Senger, H. (1970). Charakterisierung einer Synchronkultur von Scenedesmus obliquus, ihrer potentiellen Photosyntheseleistung und des Photosynthese-Quotienten wahrend des Entwicklungscyclus. Planta, 243–266.
Seo, J.-S., Keum, Y.-S., & Li, Q. X. (2009). Bacterial degradation of aromatic compounds. International Journal of Environmental Research and Public Health, 6(1), 278–309. https://doi.org/10.3390/ijerph6010278
Serri, N. A., Anbalagan, L., Norafand, N. Z., Kassim, M. A., & Abu Mansor, M. S. (2020). Preliminary study on the growth of Tetraselmis suecica in centred-light photobioreactor (CLPBR). IOP Conference Series: Materials Science and Engineering, 716(1), 012008. https://doi.org/10.1088/1757-899X/716/1/012008
Sisman-Aydin, G. (2022). Comparative study on phycoremediation performance of three native microalgae for primary-treated municipal wastewater. Environmental Technology & Innovation, 28, 102932. https://doi.org/10.1016/j.eti.2022.102932
Sousa, C. A., Sousa, H., Vale, F., & Simões, M. (2021). Microalgae-based bioremediation of wastewaters - Influencing parameters and mathematical growth modelling. Chemical Engineering Journal, 425, 131412. https://doi.org/10.1016/J.CEJ.2021.131412
Subashchandrabose, S. R., Ramakrishnan, B., Megharaj, M., Venkateswarlu, K., & Naidu, R. (2013). Mixotrophic cyanobacteria and microalgae as distinctive biological agents for organic pollutant degradation. Environment International, 51, 59–72. https://doi.org/10.1016/j.envint.2012.10.007
Surendhiran, D., Vijay, M., Sivaprakash, B., & Sirajunnisa, A. (2015). Kinetic modeling of microalgal growth and lipid synthesis for biodiesel production. 3. Biotech, 5(5), 663–669. https://doi.org/10.1007/s13205-014-0264-3
Tjørve, K. M., & Tjørve, E. (2017). The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family. Plos One, 12(6), 1–17. https://doi.org/10.1371/journal.pone.0178691
Trivedi, J., Singh, J., Atray, N., Ray, S. S., & Agrawal, D. (2019). Development of a non-linear growth model for predicting temporal evolution of Scenedesmus obliquus with varying irradiance. Bioprocess and Biosystems Engineering, 42(12), 2047–2054. https://doi.org/10.1007/s00449-019-02194-7
Ugya, Y. A., Hasan, D. B., Tahir, S. M., Imam, T. S., Ari, H. A., & Hua, X. (2021). Microalgae biofilm cultured in nutrient-rich water as a tool for the phycoremediation of petroleum-contaminated water. International Journal of Phytoremediation, 23(11), 1175–1183. https://doi.org/10.1080/15226514.2021.1882934
Wetherell, D. F. (1961). Culture of fresh water algae in enriched natural sea water. Physiologia Plantarum, 14(1), 1–6. https://doi.org/10.1111/j.1399-3054.1961.tb08131.x
Yang, J. S., Rasa, E., Tantayotai, P., Scow, K. M., Yuan, H. L., & Hristova, K. R. (2011). Mathematical model of Chlorella minutissima UTEX2341 growth and lipid production under photoheterotrophic fermentation conditions. Bioresource Technology, 102(3), 3077–3082. https://doi.org/10.1016/J.BIORTECH.2010.10.049
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Abbas Mohamed: conceptualization, investigation, methodology, writing—review and editing. Cunhao Du: investigation, writing—review and editing. Lixiao Ni: supervision, writing—review and editing.
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Abbas, M., Ni, L. & Du, C. Exploring Hydrocarbon Degradation Capacity and Mathematical Modeling of Mixotrophic Growth Kinetics in Tetradesmus obliquus and Desmodesmus armatus for Crude Oil Bioremediation. Water Air Soil Pollut 235, 165 (2024). https://doi.org/10.1007/s11270-024-06958-0
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DOI: https://doi.org/10.1007/s11270-024-06958-0