Photocatalyst (TiO2) as an enhancer: an attempt to enhance the production of carotenoids and lipids with the combined oxidative stresses in Coelastrella sp. M60

Abstract

Microalgae are important biological resources which attract the researchers for the production of valuable products like bio-energy and value-added products. In this study, enhanced accumulation of carotenoids and lipids was obtained from Coelastrella sp. M60 which was grown at 40 °C, along with different stress conditions (nitrogen starvation, salinity and TiO2). The results clearly indicate that osmotic stress and nitrogen starvation along with high temperature had induced the yield of zeaxanthin (13.15 mg/g DCW) and the lipid content (39.51 ± 5.13%). Further, it was also observed that TiO2 combined with other stresses had induced the increased accumulation of astaxanthin and zeaxanthin up to 1.16 and 0.51 fold on the 10th day of cultivation. On the contrary, TiO2, along with other stress conditions had influenced the biomass production up to 1.16 fold than the control, but no detectable increase in lipid content was observed. Thus, for the first time it is reported that by employing combined stress factors such as high temperature, nitrogen starvation and 3% salinity had resulted in significant improvement in zeaxanthin production in the foresaid microalgae. Further, it was also noticed that the Coelastrella sp. M60 had accumulated the carotenoids and lipids under TiO2 along with other oxidative stress conditions within the short duration.

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References

  1. Bramley PM (2000) Is lycopene beneficial to human health? Phytochemistry 54:233–236. https://doi.org/10.1016/s0031-9422(00)00103-5

    CAS  Article  Google Scholar 

  2. Chen L, Zhou L, Liu Y, Deng S, Wu H, Wang G (2012) Toxicological effects of nanometer titanium dioxide (nano-TiO2) on Chlamydomonas reinhardtii. Ecotoxicol Environ Saf 84:155–162. https://doi.org/10.1016/j.ecoenv.2012.07.019

    CAS  Article  Google Scholar 

  3. Deng X, Cheng J, Hu X, Wang L, Li D, Gao K (2017) Science of the total environment biological effects of TiO2 and CeO2 nanoparticles on the growth, photosynthetic activity, and cellular components of a marine diatom Phaeodactylum tricornutum. Sci Total Environ 575:87–96. https://doi.org/10.1016/j.scitotenv.2016.10.003

    CAS  Article  Google Scholar 

  4. Dere S, Gunes T, Sivaci R (1998) Spectrophotometric determination of chlorophyll a, b and total carotenoid contents of some algae species using different solvents. Trends J Bot 22:13–17

    Google Scholar 

  5. Fazelian N, Yousefzadi M, Movafeghi A (2020) Algal response to metal oxide nanoparticles: analysis of growth, protein content, and fatty acid composition. Bioenergy Res. https://doi.org/10.1007/s12155-020-10099-7

    Article  Google Scholar 

  6. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  Article  Google Scholar 

  7. Griffiths MJ, Harrison STL (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507. https://doi.org/10.1007/s10811-008-9392-7

    CAS  Article  Google Scholar 

  8. Hall S, Bradley T, Moore JT, Kuykindall T, Minella L (2009) Acute and chronic toxicity of nano-scale TiO2 particles to freshwater fish, cladocerans, and green algae, and effects of organic and inorganic substrate on TiO2 toxicity. Nanotoxicol 3(2):91–97. https://doi.org/10.1080/17435390902788078

    CAS  Article  Google Scholar 

  9. Haynes VN, Ward JE, Russell BJ, Agrios AG (2017) Photocatalytic effects of titanium dioxide nanoparticles on aquatic organisms—current knowledge and suggestions for future research. Aquat Toxicol 185:138–148. https://doi.org/10.1016/j.aquatox.2017.02.012

    CAS  Article  Google Scholar 

  10. Henriques M, Silva A, Rocha J (2007) Extraction and quantiication of pigments from a marine microalga: a simple and reproducible method. Commun Curr Res Educ Top Appl Microbiol 2:586–593

    Google Scholar 

  11. Ho SH, Chen CNN, Lai YY, Lu WB, Chang JS (2014) Exploring the high lipid production potential of a thermotolerant microalga using statistical optimization and semi-continuous cultivation. Bioresour Technol 163:128–135. https://doi.org/10.1016/j.biortech.2014.04.028

    CAS  Article  Google Scholar 

  12. Hong ME, Hwang SK, Chang WS, Kim BW, Lee J, Sim SJ (2015) Enhanced autotrophic astaxanthin production from Haematococcus pluvialis under high temperature via heat stress-driven Haber–Weiss reaction. Appl Microbiol Biotechnol 99:5203–5215. https://doi.org/10.1007/s00253-015-6440-5

    CAS  Article  Google Scholar 

  13. Hu CW, Chuang LT, Yu PC, Chen CNN (2013) Pigment production by a new thermotolerant microalga Coelastrella sp. F50. Food Chem 138:2071–2078. https://doi.org/10.1016/j.foodchem.2012.11.133

    CAS  Article  Google Scholar 

  14. Huang W, Lin Y, He M, Gong Y, Huang J (2018) Induced high-yield production of zeaxanthin, lutein, and β-carotene by a mutant of Chlorella zofingiensis. J Agric Food Chem 66:891–897. https://doi.org/10.1021/acs.jafc.7b05400

    CAS  Article  Google Scholar 

  15. Iswarya V, Sharma V, Chandrasekaran N, Mukherjee A (2017) Impact of tetracycline on the toxic effects of titanium dioxide (TiO2) nanoparticles towards the freshwater algal species, Scenedesmus obliquus. Aquat Toxicol 193:168–177. https://doi.org/10.1016/j.aquatox.2017.10.023

    CAS  Article  Google Scholar 

  16. Ji J, Long Z, Lin D (2011) Toxicity of oxide nanoparticles to the green algae Chlorella sp. Chem Eng J 170:525–530. https://doi.org/10.1016/j.cej.2010.11.026

    CAS  Article  Google Scholar 

  17. Kang NK, Lee B, Choi GG, Moon M, Park MS, Lim JK, Yang JW (2014) Enhancing lipid productivity of Chlorella vulgaris using oxidative stress by TiO2 nanoparticles. Korean J Chem Eng 31:861–867. https://doi.org/10.1007/s11814-013-0258-6

    CAS  Article  Google Scholar 

  18. Karpagam R, Raj KJ, Ashokkumar B, Varalakshmi P (2015) Characterization and fatty acid profiling in two fresh water microalgae for biodiesel production: lipid enhancement methods and media optimization using response surface methodology. Bioresour Technol 188:177–184. https://doi.org/10.1016/j.biortech.2015.01.053

    CAS  Article  Google Scholar 

  19. Karpagam R, Jawaharraj K, Ashokkumar B, Sridhar J, Varalakshmi P (2018) Unraveling the lipid and pigment biosynthesis in Coelastrella sp. M-60: genomics-enabled transcript profiling. Algal Res 29:277–289. https://doi.org/10.1016/j.algal.2017.11.031

    Article  Google Scholar 

  20. Khalid M (2020) Nanotechnology and chemical engineering as a tool to bioprocess microalgae for its applications in therapeutics and bioresource management. Crit Rev Biotechnol 40:46–63. https://doi.org/10.1080/07388551.2019.1680599

    Article  Google Scholar 

  21. Khan I, Saeed K, Khan I (2019) Nanoparticles: properties, applications and toxicities. Arab J Chem 12:908–931. https://doi.org/10.1016/j.arabjc.2017.05.011

    CAS  Article  Google Scholar 

  22. Li F, Liang Z, Zheng X, Zhao W, Wu M, Wang Z (2015) Toxicity of nano-TiO2 on algae and the site of reactive oxygen species production. Aquat Toxicol 158:1–13. https://doi.org/10.1016/j.aquatox.2014.10.014

    CAS  Article  Google Scholar 

  23. Liang SX, Wong LS, Dhanapa AC (2020) Toxicity of metals and metallic nanoparticles on nutritional properties of microalgae. Water Air Soil Pollut 231(2):52. https://doi.org/10.1007/s11270-020-4413-5

    CAS  Article  Google Scholar 

  24. Matouke MM, Elewa DT, Abdullahi K (2018) Binary effect of titanium dioxide nanoparticles (nTio2) and phosphorus on microalgae (Chlorella ‘Ellipsoides Gerneck, 1907). Aquat Toxicol 198:40–48

    CAS  Article  Google Scholar 

  25. Mcgee D, Archer L, Fleming GTA, Gillespie E, Touzet N, Lutein L (2020) Influence of spectral intensity and quality of LED lighting on photoacclimation, carbon allocation and high-value pigments in microalgae. Photosynth Res 143:67–80. https://doi.org/10.1007/s11120-019-00686-x

    CAS  Article  Google Scholar 

  26. Middepogu A, Hou J, Gao X, Lin D (2018) Effect and mechanism of TiO2 nanoparticles on the photosynthesis of Chlorella pyrenoidosa. Ecotoxicol Environ Saf 161:497–506. https://doi.org/10.1016/j.ecoenv.2018.06.027

    CAS  Article  Google Scholar 

  27. Minhas AK, Hodgson P, Barrow CJ, Adholeya A (2016) A review on the assessment of stress conditions for simultaneous production of microalgal lipids and carotenoids. Front Microbiol 7:1–19. https://doi.org/10.3389/fmicb.2016.00546

    Article  Google Scholar 

  28. Mulders, Kim JM (2014) Phototrophic pigment production with microalgae: a review https://doi.org/10.13140/RG.2.1.2104.8804

  29. Paliwal C, Mitra M, Bhayani K, Bharadwaj SVV, Ghosh T, Dubey S, Mishra S (2017) Abiotic stresses as tools for metabolites in microalgae. Bioresour Technol 244:1216–1226. https://doi.org/10.1016/j.biortech.2017.05.058

    CAS  Article  Google Scholar 

  30. Peller JR, Whitman RL, Griffith S, Harris P, Peller C, Scalzitti J (2007) TiO2 as a photocatalyst for control of the aquatic invasive alga, cladophora, under natural and artificial light cladophora, under natural and artificial light. J Photochem Photobiol 186:212–217. https://doi.org/10.1016/j.jphotochem.2006.08.009

    CAS  Article  Google Scholar 

  31. Petit AN, Eullaffroy P, Debenest T, Gagne F (2010) Toxicity of PAMAM dendrimers to Chlamydomonas reinhardtii. Aquat Toxicol 100:187–193. https://doi.org/10.1016/j.aquatox.2010.01.019

    CAS  Article  Google Scholar 

  32. Pugkaew W, Meetam M, Yokthongwattana K, Leeratsuwan N (2019) Effects of salinity changes on growth, photosynthetic activity, biochemical composition, and lipid productivity of marine microalga Tetraselmis suecica. J Appl Phycol 31(2):969–979. https://doi.org/10.1007/s10811-018-1619-7

    CAS  Article  Google Scholar 

  33. Recht L, Töpfer N, Batushansky A, Sikron N, Gibon Y, Fait A, Nikoloski Z, Boussiba S, Zarka A (2014) Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis. J Biol Chem 289:30387–30403. https://doi.org/10.1074/jbc.M114.555144

    CAS  Article  Google Scholar 

  34. Remias D, Lutz C (2007) Characterisation of esterified secondary carotenoids and of their isomers in green algae: a HPLC approach. Algol Stud 124:85–94. https://doi.org/10.1127/1864-1318/2007/0124-0085

    CAS  Article  Google Scholar 

  35. Ren HY, Dai YQ, Kong F, Xing D, Zhao L, Ren NQ, Ma J, Liu BF (2020) Enhanced microalgal growth and lipid accumulation by addition of different nanoparticles under xenon lamp illumination. Bioresour Technol 297:122409. https://doi.org/10.1016/j.biortech.2019.122409

    CAS  Article  Google Scholar 

  36. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61. https://doi.org/10.1099/00221287-111-1-1

    Article  Google Scholar 

  37. Rodriguez-Amaya DB, Kimura M (2004) Harvestplus Handbook for Carotenoid Analysis, International Food Policy Research Institute (IFPRI) and International Center for Tropical Agriculture (CIAT), Washington DC and Cali, 2004. http://ebrary.ifpri.org/cdm/singleitem/collection/p15738coll2/id/125148/rec/25

  38. Saeki K, Aburai N, Aratani S, Miyashita H, Abe K (2016) Salt-stress and plant hormone-like responses for selective reactions of esterified xanthophylls in the aerial microalga Coelastrella sp. KGU-Y002. J Appl Phycol. https://doi.org/10.1007/s10811-016-0911-7

    Article  Google Scholar 

  39. Schuler LM, Santos T, Pereira H, Duarte P, Gangadhar KN (2020) Improved production of lutein and β-carotene by thermal and light intensity upshifts in the marine microalga Tetraselmis sp. CTP4 45. Algal Res 45:101732. https://doi.org/10.1016/j.algal.2019.101732

    Article  Google Scholar 

  40. Singh D, Puri M, Wilkens S, Mathur AS, Tuli DK, Barrow CJ (2013) Characterization of a new zeaxanthin producing strain of Chlorella saccharophila isolated from New Zealand marine waters. Bioresour Technol 143:308–314. https://doi.org/10.1016/j.biortech.2013.06.006

    CAS  Article  Google Scholar 

  41. Singh D, Barrow CJ, Mathur AS, Tuli DK, Puri M (2015) Optimization of zeaxanthin and β-carotene extraction from Chlorella saccharophila isolated from New Zealand marine waters. Biocatal Agric Biotechnol 4:166–173. https://doi.org/10.1016/j.bcab.2015.02.001

    Article  Google Scholar 

  42. Stark WJ, Stoessel PR, Wohlleben W, Hafner A (2015) Industrial applications of nanoparticles. Chem Soc Rev 44:5793–5805. https://doi.org/10.1039/c4cs00362d

    CAS  Article  Google Scholar 

  43. Subhash GV, Rohit MV, Devi MP, Swamy YV, Mohan SV (2014) Temperature induced stress influence on biodiesel productivity during mixotrophic microalgae cultivation with wastewater. Bioresour Technol 169:789–793. https://doi.org/10.1016/j.biortech.2014.07.019

    CAS  Article  Google Scholar 

  44. Thiagarajan V, Pavani M, Archanaa S, Seenivasan R, Chandrasekaran N, Suraishkumar GK, Mukherjee A (2019) Diminishing bioavailability and toxicity of P25 TiO2 NPs during continuous exposure to marine algae Chlorella sp. Chemosphere 233:363–372. https://doi.org/10.1016/j.chemosphere.2019.05.270

    CAS  Article  Google Scholar 

  45. Ugya AY, Imam TS, Li A, Ma J, Hua X (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

    CAS  Article  Google Scholar 

  46. Wan C, Chen BL, Zhao XQ, Bai FW (2019) Stress response of microalgae and its manipulation for development of robust strains. Microalgae Biotechnol Dev Biofuel Wastewater Treat. https://doi.org/10.1007/978-981-13-2264-8_5

    Article  Google Scholar 

  47. Xie Y, Lu K, Zhao X, Ma R, Chen J, Ho SH (2019) Manipulating nutritional conditions and salinity-gradient stress for enhanced lutein production in marine microalga Chlamydomonas sp. Biotechnol J 14(4):1800380. https://doi.org/10.1002/biot.201800380

    CAS  Article  Google Scholar 

  48. Xu D (2012) Salt-induced osmotic stress for lipid overproduction in batch culture of Chlorella vulgaris. Afr J Biotechnol 11:7072–7078. https://doi.org/10.5897/AJB11.3670

    CAS  Article  Google Scholar 

  49. Zhang XL, Yan S, Tyagi RD, Surampalli RY (2013) Biodiesel production from heterotrophic microalgae through transesterification and nanotechnology application in the production. Renew Sustain Energy Rev 26:216–223. https://doi.org/10.1016/j.rser.2013.05.061

    CAS  Article  Google Scholar 

  50. Zhang Z, Sun D, Mao X, Liu J, Chen F (2016) The crosstalk between astaxanthin, fatty acids and reactive oxygen species in heterotrophic Chlorella zofingiensis. Algal Res 19:178–183. https://doi.org/10.1016/j.algal.2016.08.015

    Article  Google Scholar 

  51. Zhang J, Li Q, Zhang M, You Y, Wang Yu, Wang Yu-hua (2019) Enhancement of carotenoid biosynthesis in Phaffia rhodozyma PR106 under stress conditions. Biosci Biotechnol Biochem 00:1–11. https://doi.org/10.1080/09168451.2019.1650633

    CAS  Article  Google Scholar 

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Acknowledgements

Authors thankfully acknowledge DST-PURSE, DST-FIST, UGC-SAP, UGC-UPE and Central Instrumentation facility of Madurai Kamaraj University, Madurai, for providing the instrumentation facilities.

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Correspondence to Perumal Varalakshmi.

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Pushpalatha, S., Sangeetha, R., Ariraman, S. et al. Photocatalyst (TiO2) as an enhancer: an attempt to enhance the production of carotenoids and lipids with the combined oxidative stresses in Coelastrella sp. M60. Clean Techn Environ Policy 23, 41–53 (2021). https://doi.org/10.1007/s10098-020-01879-y

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Keywords

  • Lipids
  • Microalgae
  • Nanoparticle
  • Pigments
  • TiO2
  • Zeaxanthin