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Potential Outdoor Cultivation of Green Microalgae Based on Response to Changing Temperatures and by Combining with Air Temperature Occurrence

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Abstract

In this study, our working hypothesis was to examine whether temperature alters biomass and metabolite production by microalgae according to strain. We also addressed whether it is possible to choose a strain suitable for growing in each season of a given region. A factorial experiment revealed a significant interaction between chlorophylls a and b (Chl a and Chl b), carotenoid/Chl (a + b) ratio, biomass and total lipid productivity of six green microalgae (four Chlorella spp., Chlorella sorokiniana and Neochloris oleoabundans) after 15 days at four temperatures. At 39/35 °C, two Chlorella sp. strains (IPR7115 and IPR7117) showed higher total carotenoids/Chl (a + b) (0.578 and 0.830), respectively. N. oleoabundans had the highest Chl a (8210 μg L−1) and Chl b (1909 μg L−1) at 19/15 °C and highest maximum dry biomass (2900 mg L−1), specific growth rate (0.538 day−1) and total lipids (1003 mg L−1) at 15/8 °C. We applied a method to infer the growth of these six green microalgae in outdoor ponds, as based on their response to changing temperatures and by combining with historical data on day/night air temperature occurrence for a given region. We conclude that the use of regionalized maps based on air temperature is a good strategy for predicting microalgal cultivation in outdoor ponds based on their features and tolerance to changing temperature.

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References

  1. Geider R, La Roche J (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37(1):1–17. https://doi.org/10.1017/S0967026201003456

    Article  Google Scholar 

  2. Renaud S, Parry D, Thinh L-V (1994) Microalgae for use in tropical aquaculture I: gross chemical and fatty acid composition of twelve species of microalgae from the northern territory, Australia. J Appl Phycol 6(3):337–345

    Article  CAS  Google Scholar 

  3. Wiltshire KH, Boersma M, Möller A, Buhtz H (2000) Extraction of pigments and fatty acids from the green alga Scenedesmus obliquus (Chlorophyceae). Aquat Ecol 34(2):119–126. https://doi.org/10.1023/a:1009911418606

    Article  CAS  Google Scholar 

  4. Abou-Shanab RAI, Ji M-K, Kim H-C, Paeng K-J, Jeon B-H (2013) Microalgal species growing on piggery wastewater as a valuable candidate for nutrient removal and biodiesel production. J Environ Manag 115(Supplement C):257–264. https://doi.org/10.1016/j.jenvman.2012.11.022

    Article  CAS  Google Scholar 

  5. Mehrabadi A, Farid MM, Craggs R (2017) Potential of five different isolated colonial algal species for wastewater treatment and biomass energy production. Algal Res 21:1–8. https://doi.org/10.1016/j.algal.2016.11.002

    Article  Google Scholar 

  6. Garcia-Gonzalez J, Sommerfeld M (2016) Biofertilizer and biostimulant properties of the microalga Acutodesmus dimorphus. J Appl Phycol 28(2):1051–1061. https://doi.org/10.1007/s10811-015-0625-2

    Article  PubMed  Google Scholar 

  7. Wuang SC, Khin MC, Chua PQD, Luo YD (2016) Use of Spirulina biomass produced from treatment of aquaculture wastewater as agricultural fertilizers. Algal Res 15:59–64. https://doi.org/10.1016/j.algal.2016.02.009

    Article  Google Scholar 

  8. Carver S, Hulatt C, Thomas D, Tuovinen O (2011) Thermophilic, anaerobic co-digestion of microalgal biomass and cellulose for H2 production. Biodegradation 22(4):805–814. https://doi.org/10.1007/s10532-010-9419-z

    Article  CAS  PubMed  Google Scholar 

  9. Yang J, Xu M, Zhang X, Hu Q, Sommerfeld M, Chen Y (2011) Life-cycle analysis on biodiesel production from microalgae: water footprint and nutrients balance. Bioresour Technol 102(1):159–165

    Article  CAS  PubMed  Google Scholar 

  10. Bayro-Kaiser V, Nelson N (2017) Microalgal hydrogen production: prospects of an essential technology for a clean and sustainable energy economy. Photosynth Res 133(1):49–62. https://doi.org/10.1007/s11120-017-0350-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Granata T (2017) Dependency of microalgal production on biomass and the relationship to yield and bioreactor scale-up for biofuels: a statistical analysis of 60+ years of algal bioreactor data. BioEnergy Res 10(1):267–287. https://doi.org/10.1007/s12155-016-9787-2

    Article  CAS  Google Scholar 

  12. Acién Fernández FG, Fernández Sevilla JM, Molina Grima E (2013) Photobioreactors for the production of microalgae. Rev Environ Sci Biotechnol 12(2):131–151. https://doi.org/10.1007/s11157-012-9307-6

    Article  CAS  Google Scholar 

  13. Chang J, Le K, Song X, Jiao K, Zeng X, Ling X, Shi T, Tang X, Sun Y, Lin L (2017) Scale-up cultivation enhanced arachidonic acid accumulation by red microalgae Porphyridium purpureum. Bioprocess Biosyst Eng 40(12):1763–1773. https://doi.org/10.1007/s00449-017-1831-x

    Article  CAS  PubMed  Google Scholar 

  14. Béchet Q, Moussion P, Bernard O (2017) Calibration of a productivity model for the microalgae Dunaliella salina accounting for light and temperature. Algal Res 21:156–160. https://doi.org/10.1016/j.algal.2016.11.001

    Article  Google Scholar 

  15. Ras M, Steyer J-P, Bernard O (2013) Temperature effect on microalgae: a crucial factor for outdoor production. Rev Environ Sci Biotechnol 12(2):153–164. https://doi.org/10.1007/s11157-013-9310-6

    Article  CAS  Google Scholar 

  16. Roleda MY, Slocombe SP, Leakey RJG, Day JG, Bell EM, Stanley MS (2013) Effects of temperature and nutrient regimes on biomass and lipid production by six oleaginous microalgae in batch culture employing a two-phase cultivation strategy. Bioresour Technol 129(1):439–449. https://doi.org/10.1016/j.biortech.2012.11.043

    Article  CAS  PubMed  Google Scholar 

  17. Srirangan S, Sauer M-L, Howard B, Dvora M, Dums J, Backman P, Sederoff H (2015) Interaction of temperature and photoperiod increases growth and oil content in the marine microalgae Dunaliella viridis. PLoS One 10(5):e0127562. https://doi.org/10.1371/journal.pone.0127562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Latala A (1991) Effects of salinity, temperature and light on the growth and morphology of green planktonie algae. Oceanologia 31:119–138

    Google Scholar 

  19. Bouterfas R, Belkoura M, Dauta A (2002) Light and temperature effects on the growth rate of three freshwater algae isolated from a eutrophic lake. Hydrobiologia 489:207–217

    Article  Google Scholar 

  20. Evens TJ, Niedz RP, Kirkpatrick GJ (2008) Temperature and irradiance impacts on the growth, pigmentation and photosystem II quantum yields of Haematococcus pluvialis (Chlorophyceae). J Appl Phycol 20(4):411–422. https://doi.org/10.1007/s10811-007-9277-1

    Article  CAS  Google Scholar 

  21. Sandnes JM, Källqvist T, Wenner D, Gislerød HR (2005) Combined influence of light and temperature on growth rates of Nannochloropsis oceanica: linking cellular responses to large-scale biomass production. J Appl Phycol 17(6):515–525. https://doi.org/10.1007/s10811-005-9002-x

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  23. Bold HC (1949) The morphology of Chlamydomonas chlamydogama sp. nov. Bull Torrey Bot Club 76(2):101–108

    Article  Google Scholar 

  24. Silva HR, Prete CEC, Zambrano F, de Mello VH, Tischer CA, Andrade DS (2016) Combining glucose and sodium acetate improves the growth of Neochloris oleoabundans under mixotrophic conditions. AMB Express 6(1):1–11. https://doi.org/10.1186/s13568-016-0180-5

    Article  CAS  Google Scholar 

  25. Kong W-B, Yang H, Cao Y-T, Song H, Hua S-F, Xia C-G (2013) Effect of glycerol and glucose on the enhancement of biomass, lipid and soluble carbohydrate production by Chlorella vulgaris in mixotrophic culture. Food Technol Biotechnol 51(1):62–69

    CAS  Google Scholar 

  26. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099

    Article  CAS  PubMed  Google Scholar 

  27. Ryckebosch E, Muylaert K, Foubert I (2012) Optimization of an analytical procedure for extraction of lipids from microalgae. J Am Oil Chem Soc 89(2):189–198. https://doi.org/10.1007/s11746-011-1903-z

    Article  CAS  Google Scholar 

  28. Jeffrey S, Humphrey G (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    Article  CAS  Google Scholar 

  29. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bulletin 167, 2nd edn. Fisheries Research Board of Canada, Ottawa

    Google Scholar 

  30. Thomas JB, Hammans JWK, Verwer W (1977) On the quantitative relationship between chlorophyll b and the chlorophyll a form ca685 in the light-harvesting pigment-protein complex of chloroplasts. Acta Bot Neerl 26(5):377–383. https://doi.org/10.1111/j.1438-8677.1977.tb00251.x

    Article  CAS  Google Scholar 

  31. Farr TG, Rosen PA, Caro E, Crippen R, Duren R, Hensley S, Kobrick M, Paller M, Rodriguez E, Roth L, Seal D, Shaffer S, Shimada J, Umland J, Werner M, Oskin M, Burbank D, Alsdorf D (2007) The shuttle radar topography mission. Rev Geophys 45(2):1–33

    Article  Google Scholar 

  32. Caviglione JH, Andrade DS, Colozzi Filho A (2014) Potencial climático para o cultivo de microalgas em sistemas abertos no estado do Paraná. In: Andrade DS, Filho AC (eds) Microalgas de águas continentais, vol 2. IAPAR, Londrina, pp 160–184

    Google Scholar 

  33. Urreta I, Ikaran Z, Janices I, Ibañez E, Castro-Puyana M, Castañón S, Suárez-Alvarez S (2014) Revalorization of Neochloris oleoabundans biomass as source of biodiesel by concurrent production of lipids and carotenoids. Algal Res 5:16–22. https://doi.org/10.1016/j.algal.2014.05.001

    Article  Google Scholar 

  34. de Winter L, Klok AJ, Cuaresma Franco M, Barbosa MJ, Wijffels RH (2013) The synchronized cell cycle of Neochloris oleoabundans and its influence on biomass composition under constant light conditions. Algal Res 2(4):313–320. https://doi.org/10.1016/j.algal.2013.09.001

    Article  Google Scholar 

  35. Del Campo JA, Rodríguez H, Moreno J, Vargas MÁ, Rivas J, Guerrero MG (2004) Accumulation of astaxanthin and lutein in Chlorella zofingiensis (Chlorophyta). Appl Microbiol Biotechnol 64(6):848–854. https://doi.org/10.1007/s00253-003-1510-5

    Article  CAS  PubMed  Google Scholar 

  36. Andrade D, Matos Md, Goes Kd, Gatti IdA, Silva Md, Scherer A (2014) Produção de proteínas e pigmentos pelas microalgas da coleção IPR In: DS A, A CF (eds) Microalgas de águas continentais Produção de biomassa e coprodutos. IAPAR, Londrina, pp 387–410

  37. Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60(1):43–73. https://doi.org/10.1023/a:1006297731456

    Article  CAS  Google Scholar 

  38. Rise M, Cohen E, Vishkautsan M, Cojocaru M, Gottlieb HE, Arad S (1994) Accumulation of secondary carotenoids in Chlorella zofingiensis. J Plant Physiol 144(3):287–292. https://doi.org/10.1016/S0176-1617(11)81189-2

    Article  CAS  Google Scholar 

  39. Chinnasamy S, Ramakrishnan B, Bhatnagar A, Das KC (2009) Biomass production potential of a wastewater alga Chlorella vulgaris ARC 1 under elevated levels of CO2 and temperature. Int J Mol Sci 10(2):518–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yang G-j, Luan Z-q, Zhou X-h, Mei Y (2010) The researching of the effect of temperature on Chlorella growth and content of dissolved oxygen and content of chlorophyll. Math Phys Fish Sci 8:68–74

    Google Scholar 

  41. Angelo EE, Andrade DS, Colozzi Filho A (2014) Cultivo não-fotoautotrófico de microalgas: uma visão geral. Semina: Ciênc Biol Saúde 35(2):125. https://doi.org/10.5433/1679-0367.2014v35n2p125

    Article  Google Scholar 

  42. Teoh M-L, Phang S-M, Chu W-L (2013) Response of Antarctic, temperate, and tropical microalgae to temperature stress. J Appl Phycol 25(1):285–297. https://doi.org/10.1007/s10811-012-9863-8

    Article  CAS  Google Scholar 

  43. Kessler E (1985) Upper limits of temperature for growth in Chlorella (Chlorophyceae). Plant Syst Evol 151(1):67–71. https://doi.org/10.1007/bf02418020

    Article  Google Scholar 

  44. Ugwu CU, Aoyagi H, Uchiyama H (2007) Influence of irradiance, dissolved oxygen concentration, and temperature on the growth of Chlorella sorokiniana. Photosynthetica 45(2):309–311. https://doi.org/10.1007/s11099-007-0052-y

    Article  Google Scholar 

  45. Aleya L, Dauta A, Reynolds CS (2011) Endogenous regulation of the growth-rate responses of a spring-dwelling strain of the freshwater alga, Chlorella minutissima, to light and temperature. Eur J Protistol 47(4):239–244. https://doi.org/10.1016/j.ejop.2011.05.003

    Article  PubMed  Google Scholar 

  46. González-Fernández C, Mahdy A, Ballesteros I, Ballesteros M (2016) Impact of temperature and photoperiod on anaerobic biodegradability of microalgae grown in urban wastewater. Int Biodeterior Biodegrad 106:16–23. https://doi.org/10.1016/j.ibiod.2015.09.016

    Article  Google Scholar 

  47. Xin L, Hong-ying H, Yu-ping Z (2011) Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature. Bioresour Technol 102(3):3098–3102. https://doi.org/10.1016/j.biortech.2010.10.055

    Article  CAS  Google Scholar 

  48. Yoshimura T, Okada S, Honda M (2013) Culture of the hydrocarbon producing microalga Botryococcus braunii strain Showa: optimal CO2, salinity, temperature, and irradiance conditions. Bioresour Technol 133:232–239. https://doi.org/10.1016/j.biortech.2013.01.095

    Article  CAS  PubMed  Google Scholar 

  49. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306

    Article  CAS  PubMed  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. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232. https://doi.org/10.1016/j.rser.2009.07.020

    Article  CAS  Google Scholar 

  52. Hu H, Gao K (2006) Response of growth and fatty acid compositions of Nannochloropsis sp. to environmental factors under elevated CO2 concentration. Biotechnol Lett 28(13):987–992. https://doi.org/10.1007/s10529-006-9026-6

    Article  CAS  PubMed  Google Scholar 

  53. Patterson GW (1970) Effect of culture temperature on fatty acid composition of Chlorella sorokiniana. Lipids 5(7):597–600. https://doi.org/10.1007/bf02531336

    Article  CAS  PubMed  Google Scholar 

  54. Han F, Wang W, Li Y, Shen G, Wan M, Wang J (2013) Changes of biomass, lipid content and fatty acids composition under a light–dark cyclic culture of Chlorella pyrenoidosa in response to different temperature. Bioresour Technol 132:182–189. https://doi.org/10.1016/j.biortech.2012.12.175

    Article  CAS  PubMed  Google Scholar 

  55. Converti A, Casazza AA, Ortiz E, Perego PD, Borghi M (2009) Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem Eng Process 48:1146–1151. https://doi.org/10.1016/j.cep.2009.03.006

    Article  CAS  Google Scholar 

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Acknowledgements

L. A. Maroubo acknowledges MSc. scholarship from the National Council for the Improvement of Higher Education (CAPES). D.S. Andrade is also a research fellow of CNPq (312996/2017-9).

Funding

The study was partially supported by Conselho Nacional de Desenvolvimento Científico (CNPq) project (407297/2013-8).

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Authors and Affiliations

  1. Centro de Ciências Exatas, Programa de Pós-Graduação em Bioenergia, Universidade Estadual de Londrina (UEL), Rodovia Celso Garcia Cid, Km 320, P.O. Box 6001, Londrina, Parana, 86051-980, Brazil

    Lucas Alves Maroubo

  2. Instituto Agronômico do Parana, (IAPAR), Rodovia Celso Garcia Cid, Km 375, P.O. Box 10030, Londrina, Parana, 86047-902, Brazil

    Lucas Alves Maroubo, Diva S. Andrade, João Henrique Caviglione, Gisele Milani Lovato & Getulio Takashi Nagashima

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  1. Lucas Alves Maroubo
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  2. Diva S. Andrade
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  3. João Henrique Caviglione
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  4. Gisele Milani Lovato
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  5. Getulio Takashi Nagashima
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Contributions

DSA, LAM and JHC did the conception and design of the study. LAM, GTN, JHC and GML performed acquisition of data. Analysis and interpretation of the data were done by all authors. All authors have reviewed and approved the manuscript for publication.

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Correspondence to Diva S. Andrade.

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The authors declare no conflict of interest. Mention of trade names or commercial products in this paper is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the authors.

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Maroubo, L.A., Andrade, D.S., Caviglione, J.H. et al. Potential Outdoor Cultivation of Green Microalgae Based on Response to Changing Temperatures and by Combining with Air Temperature Occurrence. Bioenerg. Res. 11, 748–762 (2018). https://doi.org/10.1007/s12155-018-9931-2

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