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Gamma Radiation as a Pretreatment for Co-extraction of Lipids and Astaxanthin in Haematococcus pluvialis

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Abstract

The study aimed to apply gamma radiation as a cell pretreatment method for lipid extraction and for obtaining astaxanthin from residual biomass of Haematococcus pluvialis. Factor 1 of the two-factor experimental design was represented by cell pretreatment methods: biomass with chloroform:methanol under ultrasound (BCMU), biomass with chloroform:methanol under γ radiation (BCMR), dry biomass under γ radiation (DBR), and control (without pretreatment). Factor 2 considered the vegetative and cystic phases. Cultivation was performed in a mixotrophic system, and biomass was collected in both phases, centrifuged, lyophilized, and submitted to cell pretreatment and lipid extraction. Lipid content and FAMEs were evaluated comparing pretreatment methods and life cycle phases. Total lipid content was higher with the BCMR method in the vegetative (18% DW) and cystic (14% DW) phases. Gamma radiation combined with organic solvent was more efficient for increasing lipid yield, and DBR had a lipid yield similar to BCMU. FAME content differed between phases and pretreatments for most fatty acids, mainly C16:0, C16:1, C18:1n9c, C18:2n6c, C18:2n6t, and C18:3n3. The predominance of saturated or low unsaturated fatty acids makes H. pluvialis, in both phases, suitable for biofuel production. The preservation of astaxanthin from residual cystic biomass was observed when submitted to the DBR method, with a concentration similar to the raw biomass (1.5% DW). Gamma radiation in dry biomass has an antioxidant effect. Therefore, the lipid extraction method preceded by gamma irradiation was efficient for vegetative and cystic cells of H. pluvialis and contributed to the preservation of astaxanthin from residual cystic biomass.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Mota GCP, Moraes LBS, Oliveira CYB, Oliveira DWS, Abreu JL, Dantas DMM, Gálvez AO (2022) Astaxanthin from Haematococcus pluvialis: processes, applications, and market. Prep Biochem Biotechnol 52(5):598–609. https://doi.org/10.1080/10826068.2021.1966802

    Article  CAS  PubMed  Google Scholar 

  2. Ding W, Zhao Y, Xu JW, Zhao P, Li T, Ma H, Yu X (2018) Melatonin: a multifunctional molecule that triggers defense responses against high light and nitrogen starvation stress in Haematococcus pluvialis. J Agric Food Chem 66(29):7701–7711. https://doi.org/10.1021/acs.jafc.8b02178

    Article  CAS  PubMed  Google Scholar 

  3. Xie S, Fang W, Wei D, Liu Y, Yin P, Niu J, Tian L (2018) Dietary supplementation of Haematococcus pluvialis improved the immune capacity and low salinity tolerance ability of post-larval white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 80:452–457. https://doi.org/10.1016/j.fsi.2018.06.039

    Article  CAS  PubMed  Google Scholar 

  4. Ahmed EA, Mohamed HE, Abd El-Salam HS (2022) In vitro antimicrobial activity of astaxanthin crude extract from Haematococcuspluvialis. Egypt J Aquat Biol 26:95–106. https://doi.org/10.21608/EJABF.2022.224854

    Article  Google Scholar 

  5. Alateyah N, Ahmad SMS, Gupta I, Fouzat A, Thaher MI, Das P, Al Moustafa A-E, Ouhtit A (2022) Haematococcus pluvialis microalgae extract inhibits proliferation, invasion, and induces apoptosis in breast cancer cells. Front Nutr 9:882956. https://doi.org/10.3389/fnut.2022.882956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Shah M, Mahfuzur R, Liang Y, Cheng J, Daroch M (2016) Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Front Plant Sci 7:531. https://doi.org/10.3389/fpls.2016.00531

    Article  PubMed  PubMed Central  Google Scholar 

  7. Saha SK, Mchugh E, Hayes J, Moane S, Walsh D, Murray P (2013) Effect of various stress-regulatory factors on biomass and lipid production in microalga Haematococcus pluvialis. Bioresour Technol 128:118–124. https://doi.org/10.1016/j.biortech.2012.10.049

    Article  CAS  PubMed  Google Scholar 

  8. Nishshanka GKSH, Liyanaarachchi VC, Nimarshana PHV, Ariyadasa TU, Chang JS (2022) Haematococcus pluvialis: a potential feedstock for multiple-product biorefining. J Clean Prod 344:131103. https://doi.org/10.1016/j.jclepro.2022.131103

  9. Karpagam R, Jawaharraj K, Gnanam R (2021) Review on integrated biofuel production from microalgal biomass through the outset of transesterification route: a cascade approach for sustainable bioenergy. Sci Total Environ 766:144236. https://doi.org/10.1016/j.scitotenv.2020.144236

    Article  CAS  PubMed  Google Scholar 

  10. Shuba ES, Kifle D (2018) Microalgae to biofuels: promising alternative and renewable energy, review. Renew Sust Energ Rev 81:743–755. https://doi.org/10.1016/j.rser.2017.08.042

    Article  CAS  Google Scholar 

  11. Correa DF, Beyer HL, Possingham HP, Fargione JE, Hill JD, Schenk PM (2021) Microalgal biofuel production at national scales: reducing conflicts with agricultural lands and biodiversity within countries. Energy 215:119033. https://doi.org/10.1016/j.energy.2020.119033

    Article  Google Scholar 

  12. Foteinis S, Antoniadis-Gavriil A, Tsoutsos T (2018) Life cycle assessment of algae-to-biodiesel shallow pond production systems in the Mediterranean: influence of species, pond type, by (co)-product valorisation and electricity mix. Biofuel Bioprod Biorefin 4:542–558. https://doi.org/10.1002/bbb.1871

    Article  CAS  Google Scholar 

  13. El-Sheekh MM, Gheda SF, El-Sayed AEKB, Abo Shady AM, El-Sheikh ME (2019) Schagerl M (2019) Outdoor cultivation of the green microalga Chlorella vulgaris under stress conditions as a feedstock for biofuel. Environ Sci Pollut Res 26:18520–18532. https://doi.org/10.1007/s11356-019-05108-y

    Article  CAS  Google Scholar 

  14. Enamala M, Enamala S, Chavali M, Donepudi J, Yadavalli R, Kolapalli B, Aradhyula T, Velpuri J, Kuppam C (2018) Production of biofuels from microalgae-a review on cultivation, harvesting, lipid extraction, and numerous applications of microalgae. Renew Sustain Energy Rev 94:49–68. https://doi.org/10.1016/j.rser.2018.05.012

    Article  CAS  Google Scholar 

  15. Ramluckan K, Moodley K, Bux F (2014) An evaluation of the efficacy of using selected solvents for the extraction of lipids from algal biomass by the Soxhlet extraction method. Fuel 116:103–108. https://doi.org/10.1016/j.fuel.2013.07.118

    Article  CAS  Google Scholar 

  16. Onumaegbu C, Mooney J, Alaswad A, Olabi A (2018) Pretreatment methods for production of biofuel from microalgae biomass. Renew Sustain Energy Rev 93:16–26. https://doi.org/10.1016/j.rser.2018.04.015

    Article  CAS  Google Scholar 

  17. Hagen C, Siegmund S, Braune W (2002) Ultrastructural and chemical changes in the cell wall of Haematococcus pluvialis (Volvocales, Chlorophyta) during aplanospore formation. Eur J Phycol 37(2):217–226. https://doi.org/10.1017/S0967026202003669

    Article  Google Scholar 

  18. Kim B, Lee SY, Narasimhan AL, Kim S, Oh YK (2022) Cell disruption and astaxanthin extraction from Haematococcus pluvialis: recent advances. Bioresour Technol 343:126124. https://doi.org/10.1016/j.biortech.2021.126124

    Article  CAS  PubMed  Google Scholar 

  19. Sankaran R, Cruz RAP, Pakalapati H, Show PL, Ling TC, Chen WH, Tao Y (2020) Recent advances in the pretreatment of microalgal and lignocellulosic biomass: a comprehensive review. Bioresour Technol 298:122476. https://doi.org/10.1016/j.biortech.2019.122476

    Article  CAS  PubMed  Google Scholar 

  20. Hassan SS, Williams GA, Jaiswal AK (2018) Emerging technologies for the pretreatment of lignocellulosic biomass. Bioresour Technol 262:310–318. https://doi.org/10.1016/j.biortech.2018.04.099

    Article  CAS  PubMed  Google Scholar 

  21. Kassim MA, Khalil HPSA, Serri NA, Kassim MHM, Syakir MI, Aprila NS, Dungani R (2016) Irradiation pretreatment of tropical biomass and biofiber for biofuel production. In: Monteiro W (ed) Radiation effects in materials, 1st edn. IntechOpen, Croatia, pp 329–338. https://dx.doi.org/10.5772/62728

  22. Subhash GV, Rajvanshi M, Kumar GRK, Sagaram US, Prasad V, Govindachary S, Dasgupta S (2022) Challenges in microalgal biofuel production: a perspective on techno economic feasibility under biorefinery stratagem. Bioresour Technol 343:126155. https://doi.org/10.1016/j.biortech.2021.126155

    Article  CAS  Google Scholar 

  23. Chia SR, Chew KW, Show PL, Yap YJ, Ong HC, Ling TC, Chang JS (2018) Analysis of economic and environmental aspects of microalgae biorefinery for biofuels production: a review. Biotechnol J 13(6):1700618. https://doi.org/10.1002/biot.201700618

    Article  CAS  Google Scholar 

  24. Chew KW, Yap JY, Show PL, Suan NH, Juan JC, Ling TC, Chang JS (2017) Microalgae biorefinery: high value products perspectives. Bioresour Technol 229:53–62. https://doi.org/10.1016/j.biortech.2017.01.006

    Article  CAS  PubMed  Google Scholar 

  25. Chen J, Li J, Dong W, Zhang X, Tyagi RD, Drogui P, Surampalli RY (2018) The potential of microalgae in biodiesel production. Renew Sust Energ Rev 90:336–346. https://doi.org/10.1016/j.rser.2018.03.073

    Article  Google Scholar 

  26. Marinho YF, Malafaia CB, de Araújo KS, da Silva TD, dos Santos APF, de Moraes LB, Gálvez AO (2021) Evaluation of the influence of different culture media on growth, life cycle, biochemical composition, and astaxanthin production in Haematococcus pluvialis. Aquac Int 29(2):757–778. https://doi.org/10.1007/s10499-021-00655-z

    Article  CAS  Google Scholar 

  27. Silva DLB, de Moraes LBS, Oliveira CYB, da Silva Campos CVF, de Souza BR, Gálvez AO (2022) Influence of culture medium on growth and protein production by Haematococcus pluvialis. Acta Sci Technol 44:e59590–e59590. https://doi.org/10.4025/actascitechnol.v44i1.59590

    Article  Google Scholar 

  28. Bligh E, Dyer W (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  29. de Araújo KS, Siqueira SM, dos Santos LD, Malafaia CB, Barbosa MO (2019) A preliminary study of the physico-chemical properties and fatty acid profile of five palm oil genotypes cultivated in Northeast of Brazil. J Env Anal Progr 4(4):251–256. https://doi.org/10.24221/jeap.4.4.2019.2632.251-256

    Article  Google Scholar 

  30. Dong S, Huang Y, Zhang R, Wang S, Liu Y (2014) Four different methods comparison for extraction of astaxanthin from green alga Haematococcus pluvialis. Sci World J. https://doi.org/10.1155/2014/694305

    Article  Google Scholar 

  31. R Core Team (2021) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. Available at https://www.R-project.org/. Accessed 13 July 2021

  32. Chekanov K, Lobakova E, Selyakh I, Semenova L, Sidorov R, Solovchenko A (2014) Accumulation of astaxanthin by a new Haematococcus pluvialis strain BM1 from the White Sea coastal rocks (Russia). Mar Drugs 12(8):4504–4520. https://doi.org/10.3390/md12084504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rizwan M, Mujtaba G, Memon S, Lee K, Rashid N (2018) Exploring the potential of microalgae for new biotechnology applications and beyond: a review. Renew Sustain Energy Rev 92:394–404. https://doi.org/10.1016/j.rser.2018.04.034

    Article  Google Scholar 

  34. Wang SB, Hu Q, Sommerfeld M, Chen F (2004) Cell wall proteomics of the green alga Haematococcus pluvialis (Chlorophyceae). Proteomics 4(3):692–708. https://doi.org/10.1002/pmic.200300634

    Article  CAS  PubMed  Google Scholar 

  35. Praveenkumar R, Lee K, Lee J, Oh YK (2015) Breaking dormancy: an energy-efficient means of recovering astaxanthin from microalgae. Green Chem 17(2):1226–1234. https://doi.org/10.1039/C4GC01413H

    Article  CAS  Google Scholar 

  36. Singh R, Singh D, Singh A (2016) Radiation sterilization of tissue allografts: a review. World J Radiol 8(4):55. https://doi.org/10.4329/wjr.v8.i4.355

    Article  Google Scholar 

  37. Li QM, Li XJ, Xiong XY, Hu QL, Tan XH, Wang KQ, Su XJ (2016) Analysis of degradation products and structural characterization of giant reed and Chinese silvergrass pretreated by 60Co-γ irradiation. Ind Crops Prod 83:307–315. https://doi.org/10.4329/wjr.v8.i4.355

    Article  CAS  Google Scholar 

  38. Torun M (2017) Radiation pretreatment of biomass. In: Sun Y, Chmielewski A (eds) Applications of ionizing radiation in materials processing, 2nd edn. Institute of Nuclear Chemistry and Technology, Warszawa, pp 447–460

  39. Cheng J, Li K, Yang Z, Zhou J, Cen K (2016) Enhancing the growth rate and astaxanthin yield of Haematococcus pluvialis by nuclear irradiation and high concentration of carbon dioxide stress. Bioresour Technol 204:49–54. https://doi.org/10.1016/j.biortech.2015.12.076

    Article  CAS  PubMed  Google Scholar 

  40. Torun M, Abbasova D, Solpan D, Güven O (2014) Caffeine degradation in water by gamma irradiation, zonation and zonation/gamma irradiation. Nukleonika 59(1):25–35. https://doi.org/10.2478/nuka-2014-0004

    Article  CAS  Google Scholar 

  41. Bhat NA, Wani IA, Hamdani AM, Gani A, Masoodi FA (2016) Physicochemical properties of whole wheat flour as affected by gamma irradiation. LWT- Food Sci Technol 71:175–183. https://doi.org/10.1016/j.lwt.2016.03.024

    Article  CAS  Google Scholar 

  42. Gao Y, Nagy B, Liu X, Simándi B, Wang Q (2009) Supercritical CO2 extraction of lutein esters from marigold (Tagetes erecta L) enhanced by ultrasound. J Supercrit Fluids 49(3):345–350. https://doi.org/10.1016/j.supflu.2009.02.006

    Article  CAS  Google Scholar 

  43. Lee SY, Cho JM, Chang YK, Oh YK (2017) Cell disruption and lipid extraction for microalgal biorefineries: a review. Bioresour Technol 244:1317–1328. https://doi.org/10.1016/j.biortech.2017.06.038

    Article  CAS  PubMed  Google Scholar 

  44. Adam F, Abert-Vian M, Peltier G, Chemat F (2012) “Solvent-free” ultrasound-assisted extraction of lipids from fresh microalgae cells: a green, clean and scalable process. Bioresour Technol 114:457–465. https://doi.org/10.1016/j.biortech.2012.02.096

    Article  CAS  PubMed  Google Scholar 

  45. Natarajan R, Ang W, Chen X, Voigtmann M, Lau R (2014) Lipid releasing characteristics of microalgae species through continuous ultrasonication. Bioresour Technol 158:7–11. https://doi.org/10.1016/j.biortech.2014.01.146

    Article  CAS  PubMed  Google Scholar 

  46. Zou TB, Jia Q, Li HW, Wang CX, Wu HF (2013) Response surface methodology for ultrasound-assisted extraction of astaxanthin from Haematococcus pluvialis. Mar Drugs 11(5):1644–1655. https://doi.org/10.3390/md11051644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Khoo KS, Chew KW, Yew GY, Manickam S, Ooi CW, Show PL (2020) Integrated ultrasound-assisted liquid biphasic flotation for efficient extraction of astaxanthin from Haematococcuspluvialis. Ultrason Sonochem 67:105052. https://doi.org/10.1016/j.ultsonch.2020.105052

    Article  CAS  PubMed  Google Scholar 

  48. Bilbao S, Damiani C, Salvador G, Leonardi P (2016) Haematococcus pluvialis as a source of fatty acids and phytosterols: potential nutritional and biological implications. J Appl Phycol 28(6):3283–3294. https://doi.org/10.1007/s10811-016-0899-z

    Article  CAS  Google Scholar 

  49. Nigam PS, Singh A (2011) Production of liquid biofuels from renewable resources. Prog Energy Combust Sci 37(1):52–68. https://doi.org/10.1016/j.pecs.2010.01.003

    Article  CAS  Google Scholar 

  50. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54(4):621–639. https://doi.org/10.1111/j.1365-313X.2008.03492.x

    Article  CAS  PubMed  Google Scholar 

  51. Khawory M, Sain A, Rosli M, Ishak M, Noordin M, Wahab H (2020) Effects of gamma radiation treatment on three different medicinal plants: microbial limit test, total phenolic content, in vitro cytotoxicity effect and antioxidant assay. Appl Radiat Isot 157:109013. https://doi.org/10.1016/j.apradiso.2019.109013

    Article  CAS  PubMed  Google Scholar 

  52. Zhao L, Zhao G, Chen F, Wang Z, Wu J, Hu X (2006) Different effects of microwave and ultrasound on the stability of (all-E)-astaxanthin. J Agric Food Chem 54(21):8346–8351. https://doi.org/10.1021/jf061876d

    Article  CAS  PubMed  Google Scholar 

  53. Deora NS, Misra NN, Deswal A, Mishra HN, Cullen PJ, Tiwari BK (2013) Ultrasound for improved crystallisation in food processing. Food Eng Rev 5:36–44. https://doi.org/10.1007/s12393-012-9061-0

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank the Foundation for Science and Technology of the State of Pernambuco (FACEPE) for the aid granted to Laenne Moraes [14722.01/16] and the National Council for Scientific and Technological Development (CNPq) for the aid granted to Alfredo Gálvez [PQ 308063/2019-8] and Ranilson Bezerra [PQ 307107/2019-1] and the Northeast Strategic Technologies Center (CETENE) for its availability to carry out the analyses.

Funding

This work was supported by the Foundation for Science and Technology of the State of Pernambuco (FACEPE) (grant number 14722.01/16 to Laenne Moraes) and the National Council for Scientific and Technological Development (CNPq) (grant numbers PQ 308063/2019–8 to Alfredo Gálvez and PQ 307107/2019–1 to Ranilson Bezerra).

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Writing — original draft preparation, Laenne Moraes; conceptualization, Laenne Moraes, Carolina Malafaia, Yllana Marinho, and Ranilson Bezerra; investigation, Laenne Moraes, Géssica Mota, Carolina Malafaia, and Túlio Silva; methodology, Laenne Moraes, Carolina Malafaia, Antônio Oliveira, and Ana Melo; formal analysis, Laenne Moraes, Túlio Silva, and Antônio Oliveira; writing — review and editing, Carolina Malafaia, Yllana Marinho, and Alfredo Gálvez; resources, Ranilson Bezerra, Alfredo Gálvez, and Ana Melo; supervision, Ranilson Bezerra and Danielli Dantas; and project administration, Ranilson Bezerra.

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Correspondence to Laenne Barbara S. de Moraes.

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de Moraes, L.B.S., Malafaia, C.B., da Silva, T.D. et al. Gamma Radiation as a Pretreatment for Co-extraction of Lipids and Astaxanthin in Haematococcus pluvialis. Bioenerg. Res. 16, 1841–1850 (2023). https://doi.org/10.1007/s12155-022-10531-0

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