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Comparative Response of Marine Microalgae to H2O2-Induced Oxidative Stress

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Abstract

There have been growing interests in the biorefining of bioactive compounds from marine microalgae, including pigments, omega-3 fatty acids or antioxidants for use in the nutraceutical and cosmetic sectors. This study focused on the comparative responses of five marine microalgal species from different lineages, including the dinoflagellate Amphidinium carterae, chlorophyte Brachiomonas submarina, diatom Stauroneis sp., haptophyte Diacronema sp. and rhodophyte Rhodella violacea, to exposure during their batch growth to hydrogen peroxide (H2O2). A. carterae returned an enhanced signal with the DPPH assay (8.8 µmol Trolox eq/g DW) when exposed to H2O2, which was associated with reduced pigment yields and increased proportions in saturated C16 and C18 fatty acids. B. submarina showed enhanced antioxidant response upon exposure to H2O2 with the DPPH assay (10 µmol Trolox eq/g DW), a threefold decrease in lutein (from 2.3 to 0.8 mg/g) but a twofold increase in chlorophyll b (up to 30.0 mg/g). Stauroneis sp. showed a downward response for the antioxidant assays, but its pigment yields did not vary significantly from the control. Diacronema sp. showed reduced antioxidant response and fucoxanthin content (from 4.0 to 0.2 mg/g) when exposed to 0.5 mM H2O2. R. violacea exposed to H2O2 returned enhanced antioxidant activity and proportions of EPA but was not significantly impacted in terms of pigment content. Results indicate that H2O2 can be used to induce stress and initiate metabolic changes in microalgae. The responses were however species-specific, which would require further dosage optimisation to modulate the yields of specific metabolites in individual species.

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References

  1. Bhalamurugan, G. L., Orsat, V., & Lefsrud, M. (2018). Valuable bioproducts obtained from microalgal biomass and their commercial applications: A review. Environmental Engineering Research, 23(3), 229–241.

    Article  Google Scholar 

  2. Khan, M. I., Shin, J. H., & Kim, J. D. (2018). The promising future of microalgae: Current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microbial Cell Factories, 17, 1–21.

    Article  Google Scholar 

  3. Abida, H., Ruchaud, S., Rios, L., Humeau, A., Probert, I., De Vargas, C., Bach, S., & Bowler, C. (2013). Bioprospecting marina plankton. Marine Drugs, 11(11), 4594–4611.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Fu, W., Nerlson, D. R., Yi, Z., Khraiwesh, B., Jijakli, K., Chaiboonchoe, A., Alzahmi, A., Al-khairy, D., Brynjolfsson, S., & Salehi-Ashtiani, K. (2017). Chapter 6 - Bioactive compounds from microalgae: Current development and prospects. Studies in Natural Products Chemistry, 54, 199–225.

    Article  CAS  Google Scholar 

  5. Sansone, C., & Brunet, C. (2019). Promises and challenges of microalgal antioxidant production. Antioxidants, 8(7), 199.

    Article  CAS  PubMed Central  Google Scholar 

  6. Vavilala, S. L., Gawde, K. K., Sinha, M., & D’Souza, J. S. (2015). Programmed cell death is induced by hydrogen peroxide but not by excessive ionic stress of sodium chloride in the unicellular green alga Chlamydomonas reinhardtii. European Journal of Phycology, 50(4), 422–438.

    Article  CAS  Google Scholar 

  7. Di Meo, F., Cuciniello, R., Margarucci, S., Bergamo, P., Petillo, O., Peluso, G., Filosa, S., & Crispi, S. (2020). Ginkgo biloba prevents oxidative stress-induced apoptosis blocking p53 activation in neuroblastoma cells. Antioxidants, 9(4), 279.

    Article  PubMed Central  Google Scholar 

  8. Ngo, D. N., Kim, M. M., & Kim, S. K. (2006). Chitin oligosaccharides inhibit oxidative stress in live cells. Carbohydrate Polymers, 74, 228–234.

    Article  Google Scholar 

  9. Lobo, V., Patil, A., Phatak, A., & Chandra, N. (2010). Free radicals, antioxidants and functional foods: Impact on human health. Pharmacognosy Reviews, 4(8), 118–126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Uttara, B., Singh, A. V., Zamboni, P., & Mahajan, R. (2009). Oxidative stress and neurodegenerative diseases: A review of upstream and downstream antioxidant therapeutic options. Current Neuropharmacology, 7(1), 65–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Pham-Huy, L. A., He, H., & Pham-Huy, C. (2008). Free radicals, antioxidants in disease and health. International Journal of Biomedical Sciences, 4(2), 89–96.

    CAS  Google Scholar 

  12. Sun, X. M., Ren, L. J., Zhao, Q. Y., Ji, X. J., & Huang, H. (2018). Microalgae for the production of lipid and carotenoids: A review with focus on stress regulation and adaptation. Biotechnology for Biofuels, 11, 272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Levasseur, W., Perré, P., & Pozzobon, V. (2020). A review of high value-added molecules production by microalgae in light of the classification. Biotechnology Advances, 41, 107545.

    Article  CAS  PubMed  Google Scholar 

  14. Archer, L., McGee, D., Parkes, R., Paskuliakova, A., McCoy, G. R., Adamo, G., Cusimano, A., Bongiovanni, A., Gillespie, E., & Touzet, N. (2021). Antioxidant bioprospecting in microalgae: Characterisation of the potential of two marine heterokonts from Irish waters. Applied Biochemistry and Biotechnology, 193, 981–997.

    Article  CAS  PubMed  Google Scholar 

  15. Murthy, K. N. C., Vanitha, A., Rajesha, J., Mahadeva Swamy, M., Sowmya, P. R., & Ravishankar, G. A. (2005). In vivo antioxidant activity of carotenoids from Dunaliella salina – A green microalga. Life Sciences, 76(12), 1381–1390.

    Article  CAS  Google Scholar 

  16. Haoujar, I., Cacciola, F., Abrini, J., Mangraviti, D., Giuffrida, D., Majdoub, Y. O. E., Kounnoun, A., Miceli, N., Taviano, M. F., Mondello, L., Rigano, F., & Senhaji, N. S. (2019). The contribution of carotenoids, phenolic compounds, and flavonoids to the antioxidative properties of marine microalgae isolated from Mediterranean Morocco. Molecules, 24(22), 4037.

    Article  CAS  PubMed Central  Google Scholar 

  17. Le Goff, M., Le Ferrec, E., Mayer, C., Mimouni, V., Lagadic-Gossman, D., Schoefs, B., & Ulmann, L. (2019). Microalgal carotenoids and phytosterols regulate biochemical mechanisms involved in human health and disease prevention. Biochimie, 167, 106–118.

    Article  PubMed  Google Scholar 

  18. Kouhestani, S., Jafari, A., & Babei, P. (2018). Kaempferol attenuates cognitive deficit via regulating oxidative stress and neuroinflammation in an ovariectomized rat model of sporadic dementia. Neural Regeneration Research, 13(10), 1827–1832.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Robertson, R., Guihéneuf, F., Bahar, B., Schmid, M., Stengel, D. B., Fiztgerald, G. F., Ross, R. P., & Stanton, C. (2015). The anti-inflammatory effect of algae-derived lipid extracts on lipopolysaccharide (LPS)-stimulated human THP-1 macrophages. Marine Drugs, 13(8), 5402–5424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Begum, H., Yusoff, F. M., Banerjee, S., Khatoon, H., & Shariff, M. (2016). Availability and utilization of pigments from microalgae. Food Science & Nutrition, 56(13), 2209–2222.

    CAS  Google Scholar 

  21. Greque de Morais, M., da Silva Vaz, B., Greque de Morais, E., & Vieira Costa, A. (2015). Biologically active metabolites synthesized by microalgae. BioMed Research International, 2015, 835761.

    Google Scholar 

  22. Pérez-Pérez, M. E., Lemaire, S. D., & Crespo, J. L. (2012). Reactive oxygen species and autophagy in plants and algae. Plant Physiology, 160(1), 156–164.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Burch, A. R., & Franz, A. K. (2016). Combined nitrogen limitation and hydrogen peroxide treatment enhances neutral lipid accumulation in the marine diatom Phaeodactylum tricornutum. Bioresource Technology, 219, 559–565.

    Article  CAS  PubMed  Google Scholar 

  24. Ahmed, F., & Schenk, P. M. (2017). UV-C radiation increases sterol production in the microalga Pavlova lutheri. Phytochemistry, 139, 25–32.

    Article  CAS  PubMed  Google Scholar 

  25. Anand, V., Kashyap, M., Sharma, M. P., & Bala, K. (2021). Impact of hydrogen peroxide on microalgae cultivated in varying salt-nitrate-phosphate conditions. Journal of Environmental Chemical Engineering, 9, 105824.

    Article  Google Scholar 

  26. Qiao, T., Zhao, Y., Zhong, D., & Yu, X. (2021). Hydrogen peroxide and salinity stress act synergistically to enhance lipids production in microalga by regulating reactive oxygen species and calcium. Algal Research, 53, 102017.

    Article  Google Scholar 

  27. McGee, D., Archer, L., Paskuliakova, A., Mc Coy, G., Fleming, G. T. A., Gillespie, E., & Touzet, N. (2018). Rapid chemotaxonomic profiling for the identification of high-value carotenoids in microalgae. Journal of Applied Phycology, 30, 385–399.

    Article  CAS  Google Scholar 

  28. Guillard, R. L., & Ryther, J. H. (1962). Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Canadian Journal of Microbiology, 8, 2.

    Article  Google Scholar 

  29. Nakamura, J., Purvis, E. R., & Swenberg, J. A. (2003). Micromolar concentrations of hydrogen peroxide induce oxidative DNA lesions more efficiently than millimolar concentrations in mammalian cells. Nucleic Acids Research, 31(6), 1790–1795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Guillard, R. L. (1975), in Culture of marine invertebrate animals: Culture of phytoplankton for feeding marine invertebrates (Smith W. L. and Chanley M. H, ed.), Springer, pp. 29–60.

  31. McGee, D., Archer, L., Fleming, G. T. A., Gillespie, E., & Touzet, N. (2020). Influence of spectral intensity and quality of LED lighting on photoacclimation, carbon allocation and high-value pigments in microalgae. Photosynthesis Research, 143(1), 67–80.

    Article  CAS  PubMed  Google Scholar 

  32. Mayers, J. J., Flynn, K. J., & Shields, R. J. (2013). Rapid determination of bulk microalgal biochemical composition by Fourier-transform infrared spectroscopy. Bioresource Technology, 148, 215–220.

    Article  CAS  PubMed  Google Scholar 

  33. Liu, J. Y., Zeng, L. H., & Ren, Z. H. (2019). Recent application of spectroscopy for the detection of microalgae life information: A review. Applied Spectroscopy Reviews, 55(1), 26–59.

    Article  Google Scholar 

  34. Kenny, O., Brunton, N. P., and Smyth, T. J. (2015), in Natural products from marine algae: In vitro protocols for measuring the antioxidant capacity of algal extracts. (Stengel D. B. and Connan S., ed.), Humana Press, pp 375–402.

  35. Egeland, E. S., Garrido, J. L., Clementson, L., Andersen, K., Thomas, C. S., Zapata, M., et al. (2011). in Phytoplankton pigments: Characterisation. In S. Roy, C. A. Llewellyn, E. S. Egeland, & G. Johnsen (Eds.), chemotaxonomy and applications in oceanography: Data sheets aiding identification of phytoplankton carotenoids and chlorophylls (pp. 6665–6822). Cambridge University Press.

    Google Scholar 

  36. Ryckebosch, E., Bruneel, C., Termote-Verhalle, R., Goiris, K., Muylaert, K., & Foubert, I. (2014). Nutritional evaluation of microalgae oils rich in omega-3 long chain polyunsaturated fatty acids as an alternative for fish oil. Food Chemistry, 160, 393–400.

    Article  CAS  PubMed  Google Scholar 

  37. Chokshi, K., Pancha, I., Ghosh, A., & Mishra, S. (2017). Nitrogen starvation-induced cellular crosstalk of ROS-scavenging antioxidants and phytohormone enhanced the biofuel potential of green microalga Acutodesmus dimorphus. Biotechnology for Biofuels, 10, 60.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Pérez-López, P., Gonzalez-Garcia, S., Jeffreys, C., Agathos, S. N., Mchugh, E., Walsh, D. J., Murray, P. M., Moane, S., Fijoo, G., & Moreira, M. T. (2014). Life cycle assessment of the production of the red antioxidant carotenoid astaxanthin by microalgae: From lab to pilot scale. Journal of Cleaner Production, 64, 332–344.

    Article  Google Scholar 

  39. Randhawa, V., Thakkear, M., & Wei, L. (2012). Applicability of hydrogen peroxide in brown tide control – Culture and microcosm studies. Plos One, 7(10), e47844.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Van Creveld, S. G., Rosenwasser, S., Schatz, D., Koren, I., & Vardi, A. (2015). Early perturbation in mitochondria redox homeostasis in response to environmental stress predicts cell fate in diatoms. ISME Journal, 9, 385–395.

    Article  Google Scholar 

  41. Shi, T., Wang, L., Zhang, Z., Sun, X., & Huang, H. (2020). Stresses as first-line tools for enhancing lipid and carotenoid production in microalgae. Front. Bioeng. Biotechnol., 8, 610.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Assunção, M. F. G., Amaral, R., Martins, C. B., Ferreira, J. D., Ressureição, S., Dias Santos, S., & Verejão, J. M. T. B. (2017). Screening microalgae as potential sources of antioxidants. Journal of Applied Phycology, 29, 865–877.

    Article  Google Scholar 

  43. Yang, J., Ou, X., Zhang, X., Zhou, Z., & Ma, L. (2017). Effect of different solvents on the measurement of phenolics and antioxidant activity of mulberry (Morus atropurpurea Roxb.) with accelerated solvent extraction. Food Science, 82(3), 604–612.

    Article  Google Scholar 

  44. Sadeer, N. B., Montesano, D., Albrizio, S., Zengin, G., & Mahomoodally, M. F. (2020). The versatility of antioxidant assays in food science and safety–Chemistry, applications, strengths and limitations (review). Antioxidants, 9, 709.

    Article  CAS  Google Scholar 

  45. Yang, C., Zhang, L., Zhang, H., Sun, Q., Ronghua, L., Li, J., Wu, L., & Tsao, R. (2017). Rapid and efficient conversion of all-E-astaxanthin to 9Z- and 13Z-isomers and assessment of their stability and antioxidant activities. Journal of Agriculture and Food Chemistry, 65(4), 818–826.

    Article  CAS  Google Scholar 

  46. Monteiro, G. C., Minatel, I. O., Pimentel, A. J., Gomez-Gomez, H. A., De Camargo, J. P., Pereira Diamante, M. S., Basilio, L. S., Tecchio, M. A., & Pace Pereira Lima, G. (2021). Bioactive compounds and antioxidant capacity of grape pomace flours. LWT, 135, 110053.

    Article  CAS  Google Scholar 

  47. Selvamuthukumaran, M., & Shi, J. (2017). Recent advances in extraction of antioxidants from plant by-products processing industries. FQS, 1(1), 61–81.

    CAS  Google Scholar 

  48. Banskota, A. H., Sperker, S., Stefanova, R., McGinn, P. J., & O’Leary, S. (2019). Antioxidant properties and lipid composition of selected microalgae. Journal of Applied Phycology, 31, 309–318.

    Article  CAS  Google Scholar 

  49. Li, H., Cheng, K., Wong, C., Fan, K., Chen, F., & Jiang, Y. (2007). Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chemistry, 102, 771–776.

    Article  CAS  Google Scholar 

  50. Schieler, B. M., Brown, M. V., Coolen, M. J. L., Fredricks, H., Van Mooy, B. A. S., Hirsh, D. J., & Bidle, K. D. (2019). Nitric oxide production and antioxidant function during viral infection of coccolithophore Emiliania huxleyi. ISME Journal, 13, 1019–1031.

    Article  CAS  Google Scholar 

  51. Fimbres-Olivarria, D., Carvajal-Milland, E., Lopez-Elias, H. A., Martinez-Robinson, K. G., Miranda-Baeza, A., Martinez-Cordova, L. R., & Valdez-Holguin, J. E. (2018). Chemical characterization and antioxidant activity of sulphated polysaccharides from Navicula sp. Food Hydrocolloids, 75, 229–236.

    Article  CAS  Google Scholar 

  52. Deng, X. Y., Cheng, J., Hu, X. L., Li, D., & Gao, K. (2017). Biological effects of TiO2 and CeO2 nanoparticles on the growth, photosynthetic activity, and unicellular components of a marine diatom Phaeodactylum tricornutum. Science of the Total Environment, 575, 87–96.

    Article  CAS  Google Scholar 

  53. Wang, J., Zhang, X., Chen, Y., Sommerfeld, M., & Hu, Q. (2008). Toxicity assessment of manufactured nanomaterials using the unicellular green alga Chlamydomonas reinhardtii. Chemosphere, 73, 1121–1128.

    Article  CAS  PubMed  Google Scholar 

  54. Pospíšil, P. (2016). Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Frontiers in Plant Science, 7, 1950.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Zhang, Y., He, D., Chang, F., Dang, C., & Fu, J. (2021). Combined effects of sulfamethoxazole and erythromycin on a freshwater microalga, Raphidocelis subcapitata: Toxicity and oxidative stress. Antibiotics, 10(5), 576.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Xiong, J. Q., Kurade, M. B., Patil, D. V., Min, J., & Jeon, B. H. (2017). Biodegradation and metabolic fate of levofloxacin via freshwater green alga, Scenedesmus obliquus in synthetic saline wastewater. Algal Research, 25, 54–61.

    Article  Google Scholar 

  57. Latowski, D., Kuczyńska, P., & Strzałka, K. (2013). Xanthophyll cycle – A mechanism protecting plants against oxidative stress. Redox Report, 16(2), 78–90.

    Article  PubMed Central  Google Scholar 

  58. Domeregue, F., Lerchl, J., Zähringer, U., & Heinz, E. (2002). Cloning and functional characterization of Phaeodactylum tricornutum front-end desaturases involved in eicopentaenoic acid biosynthesis. European Journal of Biochemistry, 269, 4105–4113.

    Article  Google Scholar 

  59. Vigor, C., Oger, C., Reversat, G., Rocher, A., Zhou, B., Linares-Maurizi, A., Guy, A., Bultel-Poncé, V., Galano, J. M., Vercauteren, J., Durand, T., Potin, P., Tonon, T., & Lebanc, C. (2020). Isoprostaoid profiling of marine microalgae. Biomolecules, 10, 1073.

    Article  CAS  PubMed Central  Google Scholar 

  60. Vigor, C., Reversat, G., Rocher, A., Oger, C., Galano, J. M., Vercauteren, J., Durand, T., Tonon, T., Leblanc, C., & Potin, P. (2018). Isoprostanoids quantitative profiling of marine red and brown macroalgae. Food Chemistry, 268, 452–462.

    Article  CAS  PubMed  Google Scholar 

  61. Lupette, J., Jaussaud, A., Vigor, C., Oger, C., Galano, J. M., Reversat, G., Vercauteren, J., Jouhet, J., Durand, T., & Marechal, E. (2018). Non-enzymatic synthesis of bioactive isoprostanoids in the diatom Phaeodactylum following oxidative stress. Plant Physiology, 178, 1344–1357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

The authors acknowledge financial support from the VES4US project funded by the European Union’s Horizon 2020 research and innovation program under grant Agreement No 801338.

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MEB, GTAF and NT developed the experimental design. MEB conducted all experiments and analyses and led the drafting of the manuscript. RP, DF, AA, TC, HH and AMD provided technical support and helped with the FTIR, AOX, HPLC and GC–MS methods. All authors contributed to editing and finalising the manuscript.

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Correspondence to Maria Elena Barone.

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Research Highlights

• Comparative response to H2O2 treatment assessed for 5 microalgal species from different lineages.

• Results showed an enhanced antioxidant response for Rhodella violacea and an overall reduction for the other species.

• Pigment yield reduction was observed for most species except for chlorophyll b, which was enhanced in Brachiomonas submarina.

• Species-specific variations in the proportions of fatty acids were observed.

• Principal component analysis clearly separated the H2O2-treated Rhodella violacea set from the others, with higher antioxidant response and proportions of EPA.

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Barone, M.E., Parkes, R., Herbert, H. et al. Comparative Response of Marine Microalgae to H2O2-Induced Oxidative Stress. Appl Biochem Biotechnol 193, 4052–4067 (2021). https://doi.org/10.1007/s12010-021-03690-x

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