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Induction of antioxidant activities of Arthrospira platensis and Chlorella vulgaris by modified culture conditions

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Abstract

Microalgae are considered a promising source for obtaining natural compounds with strong antioxidant activity. Despite the great progress made in this field, there is still need for further studies applying simple and cost-effective modifications to reveal their full potential and enhance antioxidant properties. Arthrospira platensis and Chlorella vulgaris are some of the most common cells studied for this purpose. In this study, it was aimed to develop a bioprocess for the enhancement of antioxidant properties of these two microalgae by evaluating the effect of different culture conditions. With this aim, the impacts of light intensity/reactive oxygen species and nitrogen sources/reactive oxygen species were evaluated for the A. platensis and C. vulgaris cells, respectively. Results showed that the antioxidant potential of A. platensis was found to be correlated with the phycocyanin and total phenolic content of cells, and 80 µmol photons m−2 s−1 light intensity induced antioxidant activity in a two-step cultivation mode. For C. vulgaris cells, maximum antioxidant activities of 68.10 ± 1.51% and 75.68 ± 0.66% were obtained in cultures with NH4Cl (0.016% (w/v)) for DPPH and ABTS assays, respectively. The applied oxidative stress factors exhibited different effects on the antioxidant activities of the cells because of their cellular morphologies and changing mechanisms of reactive oxygen species. These outcomes show the potential of applied modifications on cells and suggest a promising route to enhance antioxidant activities of microalgae for further research.

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The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Sharifi-Rad M, Anil Kumar NV, Zucca P et al (2020) Lifestyle, oxidative stress, and antioxidants: back and forth in the pathophysiology of chronic diseases. Front Physiol 11:694. https://doi.org/10.3389/fphys.2020.00694

    Article  PubMed  PubMed Central  Google Scholar 

  2. Chandra P, Sharma RK, Arora DS (2020) Antioxidant compounds from microbial sources: a review. Food Res Int 129:108849. https://doi.org/10.1016/j.foodres.2019.108849

    Article  CAS  PubMed  Google Scholar 

  3. Li Z, Yang S, Zhou Z et al (2021) Enhancement of lipid production in Desmodesmus intermedius Z8 by ultrasonic stimulation coupled with nitrogen and phosphorus stress. Biochem Eng J 172:108061. https://doi.org/10.1016/j.bej.2021.108061

    Article  CAS  Google Scholar 

  4. Aklakur M (2018) Natural antioxidants from sea: a potential industrial perspective in aquafeed formulation. Rev Aquac 10:385–399. https://doi.org/10.1111/raq.12167

    Article  Google Scholar 

  5. Lourenço SC, Moldão-Martins M, Alves VD (2019) Antioxidants of natural plant origins: From sources to food industry applications. Molecules 24:4132. https://doi.org/10.3390/molecules24224132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ma R, Wang B, Chua ET et al (2020) Comprehensive utilization of marine microalgae for enhanced co-production of multiple compounds. Mar Drugs 18:467. https://doi.org/10.3390/md18090467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Archer L, McGee D, Parkes R et al (2021) Antioxidant bioprospecting in microalgae: Characterisation of the potential of two marine heterokonts from Irish Waters. Appl Biochem Biotechnol 193:981–997. https://doi.org/10.1007/s12010-020-03467-8

    Article  CAS  PubMed  Google Scholar 

  8. Martinez-Frances E, Carlos EO (2018) Cyanobacteria and microalgae in the production of valuable bioactive compounds. Microalgal biotechnology. InTech, pp 105–115

    Google Scholar 

  9. Ugya AY, Imam TS, Li A et al (2020) Antioxidant response mechanism of freshwater microalgae species to reactive oxygen species production: a mini review. Chem Ecol 36:174–193. https://doi.org/10.1080/02757540.2019.1688308

    Article  CAS  Google Scholar 

  10. Gauthier MR, Senhorinho GNA, Scott JA (2020) Microalgae under environmental stress as a source of antioxidants. Algal Res 52:102104. https://doi.org/10.1016/j.algal.2020.102104

    Article  Google Scholar 

  11. Rastogi RP, Madamwar D, Nakamoto H, Incharoensakdi A (2020) Resilience and self-regulation processes of microalgae under UV radiation stress. J Photochem Photobiol C Photochem Rev 43:100322. https://doi.org/10.1016/j.jphotochemrev.2019.100322

    Article  CAS  Google Scholar 

  12. Markou G, Nerantzis E (2013) Microalgae for high-value compounds and biofuels production: a review with focus on cultivation under stress conditions. Biotechnol Adv 31:1532–1542. https://doi.org/10.1016/j.biotechadv.2013.07.011

    Article  CAS  PubMed  Google Scholar 

  13. Vuppaladadiyam AK, Prinsen P, Raheem A et al (2018) Microalgae cultivation and metabolites production: a comprehensive review. Biofuels, Bioprod Biorefining 12:304–324. https://doi.org/10.1002/bbb.1864

    Article  CAS  Google Scholar 

  14. Raja R, Coelho A, Hemaiswarya S et al (2018) Applications of microalgal paste and powder as food and feed: an update using text mining tool. Beni-Suef Univ J Basic Appl Sci 7:740–747. https://doi.org/10.1016/j.bjbas.2018.10.004

    Article  Google Scholar 

  15. Han P, Li J, Zhong H et al (2021) Anti-oxidation properties and therapeutic potentials of spirulina. Algal Res 55:102240. https://doi.org/10.1016/j.algal.2021.102240

    Article  Google Scholar 

  16. Wu Q, Liu L, Miron A et al (2016) (2016) The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview. Arch Toxicol 908(90):1817–1840. https://doi.org/10.1007/S00204-016-1744-5

    Article  Google Scholar 

  17. Raji AA, Alaba PA, Yusuf H et al (2018) Fishmeal replacement with Spirulina Platensis and Chlorella vulgaris in African catfish (Clarias gariepinus) diet: Effect on antioxidant enzyme activities and haematological parameters. Res Vet Sci 119:67–75. https://doi.org/10.1016/j.rvsc.2018.05.013

    Article  CAS  PubMed  Google Scholar 

  18. Zhou J, Wang M, Bäuerl C et al (2023) The impact of liquid-pressurized extracts of Spirulina, Chlorella and Phaedactylum tricornutum on in vitro antioxidant, antiinflammatory and bacterial growth effects and gut microbiota modulation. Food Chem 401:134083. https://doi.org/10.1016/j.foodchem.2022.134083

    Article  CAS  PubMed  Google Scholar 

  19. Georgiopoulou I, Tzima S, Louli V, Magoulas K (2023) Process optimization of microwave-assisted extraction of chlorophyll, carotenoid and phenolic compounds from chlorella vulgaris and comparison with conventional and supercritical fluid extraction. Appl Sci 13:2740. https://doi.org/10.3390/app13042740

    Article  CAS  Google Scholar 

  20. Zarrouk C (1966) Contribution à l’étude d’une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et photosynthese de Spirulina maxima Geitler

  21. Erdoğan A, Karataş AB, Demirel Z, Conk Dalay M (2022) Purification of fucoxanthin from the diatom Amphora capitellata by preparative chromatography after its enhanced productivity via oxidative stress. J Appl Phycol 34:301–309. https://doi.org/10.1007/s10811-021-02625-7

    Article  CAS  Google Scholar 

  22. Aslanbay Guler B, Deniz I, Demirel Z, Imamoglu E (2020) Evaluation of scale-up methodologies and computational fluid dynamics simulation for fucoxanthin production in airlift photobioareactor. Asia-Pacific J Chem Eng 15:e2532. https://doi.org/10.1002/APJ.2532

    Article  CAS  Google Scholar 

  23. Minyuk G, Sidorov R, Solovchenko A (2020) Effect of nitrogen source on the growth, lipid, and valuable carotenoid production in the green microalga Chromochloris zofingiensis. J Appl Phycol 32:923–935. https://doi.org/10.1007/s10811-020-02060-0

    Article  CAS  Google Scholar 

  24. Khazi MI, Demirel Z, Conk Dalay M (2018) Evaluation of growth and phycobiliprotein composition of cyanobacteria isolates cultivated in different nitrogen sources. J Appl Phycol 30:1513–1523. https://doi.org/10.1007/s10811-018-1398-1

    Article  CAS  Google Scholar 

  25. Fu W, Gudmundsson O, Feist AM et al (2012) Maximizing biomass productivity and cell density of Chlorella vulgaris by using light-emitting diode-based photobioreactor. J Biotechnol 161:242–249. https://doi.org/10.1016/j.biotech.2012.07.004

    Article  CAS  PubMed  Google Scholar 

  26. Song C, Wei Y, Sun J et al (2020) Biodegradation and metabolic fate of thiamphenicol via Chlorella sp. UTEX1602 and L38. Bioresour Technol. https://doi.org/10.1016/j.biortech.2019.122320

    Article  PubMed  Google Scholar 

  27. Kuda T, Tsunekawa M, Hishi T, Araki Y (2005) Antioxidant properties of dried `kayamo-nori’, a brown alga Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). Food Chem 89:617–622. https://doi.org/10.1016/j.foodchem.2004.03.020

    Article  CAS  Google Scholar 

  28. Choochote W, Suklampoo L, Ochaikul D (2014) Evaluation of antioxidant capacities of green microalgae. J Appl Phycol 26:43–48. https://doi.org/10.1007/s10811-013-0084-6

    Article  CAS  Google Scholar 

  29. Boukhris S, Athmouni K, Hamza-Mnif I et al (2017) The potential of a brown microalga cultivated in high salt medium for the production of high-value compounds. Biomed Res Int. https://doi.org/10.1155/2017/4018562

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ali HEA, El-fayoumy EA, Rasmy WE et al (2021) Two-stage cultivation of Chlorella vulgaris using light and salt stress conditions for simultaneous production of lipid, carotenoids, and antioxidants. J Appl Phycol 33:227–239. https://doi.org/10.1007/s10811-020-02308-9

    Article  CAS  Google Scholar 

  31. Rosero-Chasoy G, Rodríguez-Jasso RM, Aguilar CN et al (2022) Growth kinetics and quantification of carbohydrate, protein, lipids, and chlorophyll of Spirulina platensis under aqueous conditions using different carbon and nitrogen sources. Bioresour Technol 346:126456. https://doi.org/10.1016/j.biortech.2021.126456

    Article  CAS  PubMed  Google Scholar 

  32. Chaiklahan R, Chirasuwan N, Srinorasing T et al (2022) Enhanced biomass and phycocyanin production of Arthrospira (Spirulina) platensis by a cultivation management strategy: Light intensity and cell concentration. Bioresour Technol 343:126077. https://doi.org/10.1016/j.biortech.2021.126077

    Article  CAS  PubMed  Google Scholar 

  33. Markou G, Kougia E, Kefalogianni I et al (2019) Effect of glycerol concentration and light intensity on growth and biochemical composition of Arthrospira (Spirulina) Platensis: a study in semi-continuous mode with non-aseptic conditions. Appl Sci 9:4703. https://doi.org/10.3390/app9214703

    Article  CAS  Google Scholar 

  34. Kepekçi RA, Saygideger SD (2012) Enhancement of phenolic compound production in Spirulina platensis by two-step batch mode cultivation. J Appl Phycol 24:897–905. https://doi.org/10.1007/s10811-011-9710-3

    Article  CAS  Google Scholar 

  35. Maltsev Y, Maltseva K, Kulikovskiy M, Maltseva S (2021) Influence of light conditions on microalgae growth and content of lipids, carotenoids, and fatty acid composition. Biology (Basel) 10:1–24. https://doi.org/10.3390/biology10101060

    Article  CAS  Google Scholar 

  36. Oliveira CYB, Oliveira CDL, Prasad R et al (2021) A multidisciplinary review of Tetradesmus obliquus: a microalga suitable for large-scale biomass production and emerging environmental applications. Rev Aquac 13:1594–1618. https://doi.org/10.1111/raq.12536

    Article  Google Scholar 

  37. Ma R, Thomas-Hall SR, Chua ET et al (2018) LED power efficiency of biomass, fatty acid, and carotenoid production in Nannochloropsis microalgae. Bioresour Technol 252:118–126. https://doi.org/10.1016/j.biortech.2017.12.096

    Article  CAS  PubMed  Google Scholar 

  38. Erdoğan A, Karataş AB, Demir D et al (2023) Manipulation in culture conditions of Nanofrustulum shiloi for enhanced Fucoxanthin production and isolation by preparative chromatography. Molecules 28:1988

    Article  PubMed  PubMed Central  Google Scholar 

  39. Martínez-Sanz M, Garrido-Fernández A, Mijlkovic A et al (2020) Composition and rheological properties of microalgae suspensions: Impact of ultrasound processing. Algal Res 49:101960. https://doi.org/10.1016/j.algal.2020.101960

    Article  Google Scholar 

  40. Matsudo MC, Bezerra RP, Sato S et al (2009) Repeated fed-batch cultivation of Arthrospira (Spirulina) platensis using urea as nitrogen source. Biochem Eng J 43:52–57. https://doi.org/10.1016/j.bej.2008.08.009

    Article  CAS  Google Scholar 

  41. Dobrev GT, Pishtiyski IG, Stanchev VS, Mircheva R (2007) Optimization of nutrient medium containing agricultural wastes for xylanase production by Aspergillus niger B03 using optimal composite experimental design. Bioresour Technol 98:2671–2678. https://doi.org/10.1016/j.biortech.2006.09.022

    Article  CAS  PubMed  Google Scholar 

  42. Cejas L, Romano N, Moretti A et al (2017) Malt sprout, an underused beer by-product with promising potential for the growth and dehydration of lactobacilli strains. J Food Sci Technol 54:4464–4472. https://doi.org/10.1007/s13197-017-2927-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. da Silva Ferreira V, Sant’ Anna C (2017) Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-016-2181-6

    Article  PubMed  Google Scholar 

  44. Machado L, Carvalho G, Pereira RN (2022) Effects of innovative processing methods on microalgae cell wall: prospects towards digestibility of protein-rich biomass. Biomass 2:80–102. https://doi.org/10.3390/biomass2020006

    Article  CAS  Google Scholar 

  45. Gao L, Li D, Gao F et al (2015) Hydroxyl radical-aided thermal pretreatment of algal biomass for enhanced biodegradability. Biotechnol Biofuels 8:1–11. https://doi.org/10.1186/s13068-015-0372-2

    Article  CAS  Google Scholar 

  46. Wei D, Chen F, Chen G et al (2008) Enhanced production of lutein in heterotrophic Chlorella protothecoides by oxidative stress. Sci China, Ser C Life Sci 51:1088–1093. https://doi.org/10.1007/s11427-008-0145-2

    Article  CAS  Google Scholar 

  47. Liu JG, Hou CW, Lee SY et al (2011) Antioxidant effects and UVB protective activity of Spirulina (Arthrospira platensis) products fermented with lactic acid bacteria. Process Biochem 46:1405–1410. https://doi.org/10.1016/j.procbio.2011.03.010

    Article  CAS  Google Scholar 

  48. Xie Y, Jin Y, Zeng X et al (2015) Fed-batch strategy for enhancing cell growth and C-phycocyanin production of Arthrospira (Spirulina) platensis under phototrophic cultivation. Bioresour Technol 180:281–287. https://doi.org/10.1016/J.BIORTECH.2014.12.073

    Article  CAS  PubMed  Google Scholar 

  49. Lee SH, Lee JE, Kim Y, Lee SY (2016) The production of high purity phycocyanin by Spirulina platensis using light-emitting diodes based two-stage cultivation. Appl Biochem Biotechnol 178:382–395. https://doi.org/10.1007/s12010-015-1879-5

    Article  CAS  PubMed  Google Scholar 

  50. Oliveira CYB, Abreu JL, Santos EP et al (2022) Light induces peridinin and docosahexaenoic acid accumulation in the dinoflagellate Durusdinium glynnii. Appl Microbiol Biotechnol 106:6263–6276. https://doi.org/10.1007/s00253-022-12131-6

    Article  CAS  PubMed  Google Scholar 

  51. Shanthi G, Premalatha M, Anantharaman N (2018) Effects of l-amino acids as organic nitrogen source on the growth rate, biochemical composition and polyphenol content of Spirulina platensis. Algal Res 35:471–478. https://doi.org/10.1016/j.algal.2018.09.014

    Article  Google Scholar 

  52. Esen M, Öztürk Ürek R (2014) Nitrate and iron nutrition effects on some nitrate assimilation enzymes and metabolites in Spirulina platensis. Turkish J Biol 38:690–700. https://doi.org/10.3906/biy-1405-37

    Article  CAS  Google Scholar 

  53. Manirafasha E, Murwanashyaka T, Ndikubwimana T et al (2018) Enhancement of cell growth and phycocyanin production in Arthrospira (Spirulina) platensis by metabolic stress and nitrate fed-batch. Bioresour Technol 255:293–301. https://doi.org/10.1016/J.BIORTECH.2017.12.068

    Article  CAS  PubMed  Google Scholar 

  54. Khalil ZI, Asker MMS, El-Sayed S, Kobbia IA (2010) Effect of pH on growth and biochemical responses of Dunaliella bardawil and Chlorella ellipsoidea. World J Microbiol Biotechnol 26:1225–1231. https://doi.org/10.1007/s11274-009-0292-z

    Article  CAS  PubMed  Google Scholar 

  55. Liaqat F, Khazi MI, Bahadar A et al (2023) Mixotrophic cultivation of microalgae for carotenoid production. Rev Aquac 15:35–61. https://doi.org/10.1111/raq.12700

    Article  Google Scholar 

  56. Floegel A, Kim DO, Chung SJ et al (2011) Comparison of ABTS/DPPH assays to measure antioxidant capacity in popular antioxidant-rich US foods. J Food Compos Anal 24:1043–1048. https://doi.org/10.1016/j.jfca.2011.01.008

    Article  CAS  Google Scholar 

  57. Park WS, Kim HJ, Li M et al (2018) Two classes of pigments, carotenoids and c-phycocyanin, in spirulina powder and their antioxidant activities. Molecules 23:1–11. https://doi.org/10.3390/molecules23082065

    Article  CAS  Google Scholar 

  58. Finamore A, Palmery M, Bensehaila S, Peluso I (2017) Antioxidant, immunomodulating, and microbial-modulating activities of the sustainable and ecofriendly Spirulina. Oxid Med Cell Longev. https://doi.org/10.1155/2017/3247528

    Article  PubMed  PubMed Central  Google Scholar 

  59. Mtaki K, Kyewalyanga MS, Mtolera MSP (2020) Assessment of antioxidant contents and free radical-scavenging capacity of chlorella vulgaris cultivated in low cost media. Appl Sci 10:8611. https://doi.org/10.3390/app10238611

    Article  CAS  Google Scholar 

  60. Conde T, Lopes D, Łuczaj W et al (2022) Algal lipids as modulators of skin disease: a critical review. Metabolites. https://doi.org/10.3390/metabo12020096

    Article  PubMed  PubMed Central  Google Scholar 

  61. Conde TA, Neves BF, Couto D et al (2021) Microalgae as sustainable bio-factories of healthy lipids: Evaluating fatty acid content and antioxidant activity. Mar Drugs 19:1–20. https://doi.org/10.3390/md19070357

    Article  CAS  Google Scholar 

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Acknowledgements

This study was a part of Cost Action CA17120 and the authors would like to thank the Scientific and Technological Research Council of Turkey (TUBITAK) with the project number 120M111 for the financial support.

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Türkiye Bilimsel ve Teknolojik Araştırma Kurumu, 120M111

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BAG: Conceptualization, Methodology, Investigation, Writing–original draft. ZD: Conceptualization, Resources. EI: Conceptualization, Methodology, Writing–review & editing.

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Correspondence to Bahar Aslanbay Guler.

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Aslanbay Guler, B., Demirel, Z. & Imamoglu, E. Induction of antioxidant activities of Arthrospira platensis and Chlorella vulgaris by modified culture conditions. Bioprocess Biosyst Eng 47, 275–287 (2024). https://doi.org/10.1007/s00449-023-02963-5

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