Skip to main content
SpringerLink
Log in

A new isolate cold-adapted Ankistrodesmus sp. OR119838: influence of light, temperature, and nitrogen concentration on growth characteristics and biochemical composition using the two-stage cultivation strategy

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

Natural-based chemicals from microalgae such as lipids and pigments are the interests in industries and the bioeconomy. Cold-adapted Ankistrodesmus sp. OR119838, an isolated strain from Cheshmeh–Sabz Lake in northeastern Iran, was cultivated using a two-stage culture strategy under different environmental conditions. With doubling the nitrate concentration at the vegetative stage (170 mg/L) and increasing the light intensity (180 µmol photons/m2/s) the highest specific growth rate (0.61 ± 0.02 per day) and biomass productivity (121.1 ± 7.2 mg/L/day) were observed at 25 °C. In the optimal growth condition Chl a and Chl b contents of Ankistrodesmus sp. OR119838 reached the highest amount (11.07 ± 0.14 and 11.23 ± 0.29 µg/mL, respectively) at 25 °C. While carotenoid content correlated negatively with optimum biomass productivity (− 0.708) and had the best value (12.23 ± 0.29 µg/mL) in nitrogen deficiency (42 mg/L) and intense light conditions (180 µmol photons/m2/s) at 15 °C. Lipid content was increased with declined nitrate concentration (42 mg/L), high light intensity, and 180 µmol photons/m2/s at 25 °C. The highest percentage of polyunsaturated fatty acids (71.94%) and α-linolenic acid (57.73 ± 6.63%) was observed in conditions with 170 mg/L nitrate concentration and low light intensity (40 µmol photons/m2/ s) at the low temperature (15 °C). While saturated fatty acids content (43.27%) and palmitic acid reached the highest amount under 40 µmol photons/m2/s, 42 mg/L nitrate at 25 °C (35.02 ± 5.33%). Biomass productivity of Ankistrodesmus sp. OR119838, as a cold-adapted strain, decreased by only 8.2% with a 10-degree decline in temperature. Therefore, this strain has good potential to grow in open ponds by tolerating the daily temperature fluctuations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated during the current study are available from the corresponding authors upon request.

References

  1. Ferreira de Oliveira AP, Bragotto APA (2022) Microalgae-based products: Food and public health. Futur Foods 6:100157. https://doi.org/10.1016/j.fufo.2022.100157

    Article  CAS  Google Scholar 

  2. Dolganyuk V, Belova D, Babich O et al (2020) Microalgae: A promising source of valuable bioproducts. Biomolecules 10:1153. https://doi.org/10.3390/biom10081153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Mehariya S, Goswami RK, Karthikeysan OP, Verma P (2021) Microalgae for high-value products: a way towards green nutraceutical and pharmaceutical compounds. Chemosphere 280:130553. https://doi.org/10.1016/j.chemosphere.2021.130553

    Article  CAS  PubMed  Google Scholar 

  4. Remize M, Brunel Y, Silva J et al (2021) Microalgae n-3 PUFAs production and use in food and feed industries. Mar Drugs 19:113. https://doi.org/10.3390/md19020113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Tang DYY, Yew GY, Koyande AK et al (2020) Green technology for the industrial production of biofuels and bioproducts from microalgae: a review. Environ Chem Lett 18:1967–1985. https://doi.org/10.1007/s10311-020-01052-3

    Article  CAS  Google Scholar 

  6. Varela JC, Pereira H, Vila M, León R (2015) Production of carotenoids by microalgae: achievements and challenges. Photosynth Res 125:423–436. https://doi.org/10.1007/s11120-015-0149-2

    Article  CAS  PubMed  Google Scholar 

  7. Barkia I, Saari N, Manning SR (2019) Microalgae for high-value products towards human health and nutrition. Mar Drugs 17:304. https://doi.org/10.3390/md17050304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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) 10:1060. https://doi.org/10.3390/biology10101060

    Article  CAS  PubMed  Google Scholar 

  9. He Q, Yang H, Wu L, Hu C (2015) Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae. Bioresour Technol 191:219–228. https://doi.org/10.1016/j.biortech.2015.05.021

    Article  CAS  PubMed  Google Scholar 

  10. Krzemińska I, Piasecka A, Nosalewicz A et al (2015) Alterations of the lipid content and fatty acid profile of Chlorella protothecoides under different light intensities. Bioresour Technol 196:72–77. https://doi.org/10.1016/j.biortech.2015.07.043

    Article  CAS  PubMed  Google Scholar 

  11. Kurpan Nogueira DP, Silva AF, Araújo OQF, Chaloub RM (2015) Impact of temperature and light intensity on triacylglycerol accumulation in marine microalgae. Biomass Bioenerg 72:280–287. https://doi.org/10.1016/j.biombioe.2014.10.017

    Article  CAS  Google Scholar 

  12. Lamers P, van de Laak C, Kaasenbrood P et al (2010) Carotenoid and fatty acid metabolism in light-stressed Dunaliella Salina. Biotechnol Bioeng 106:638–648. https://doi.org/10.1002/bit.22725

    Article  CAS  PubMed  Google Scholar 

  13. Xie Y, Ho SH, Chen N et al (2013) Phototrophic cultivation of a thermo-tolerant Desmodesmus sp. for lutein production: effects of nitrate concentration, light intensity and fed-batch operation. Bioresour Technol. https://doi.org/10.1016/j.biortech.2013.06.064

    Article  PubMed  Google Scholar 

  14. Chodchoey K, Verduyn C (2012) Growth, fatty acid profile in major lipid classes and lipid fluidity of Aurantiochytrium mangroveiSK-02 As a function of growth temperature. Braz J Microbiol 43:187–200. https://doi.org/10.1590/S1517-838220120001000020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Sun XM, Ren L, Zhao Q et al (2018) Microalgae for the production of lipid and carotenoids: a review with focus on stress regulation and adaptation. Biotechnol Biofuels. https://doi.org/10.1186/s13068-018-1275-9

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lindberg A, Niemi C, Takahashi J et al (2022) Cold stress stimulates algae to produce value-added compounds. Bioresour Technol Rep 19:101145. https://doi.org/10.1016/j.biteb.2022.101145

    Article  CAS  Google Scholar 

  17. 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. Biotechnol Biofuels 10:60. https://doi.org/10.1186/s13068-017-0747-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Yang L, Chen J, Qin S et al (2018) Growth and lipid accumulation by different nutrients in the microalga Chlamydomonas reinhardtii. Biotechnol Biofuels. https://doi.org/10.1186/s13068-018-1041-z

    Article  PubMed  PubMed Central  Google Scholar 

  19. Potijun S, Yaisamlee C, Sirikhachornkit A (2021) Pigment production under cold stress in the Green Microalga Chlamydomonas reinhardtii. Agriculture. https://doi.org/10.3390/agriculture11060564

    Article  Google Scholar 

  20. Ali H, El-fayoumy E, Rasmy W 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 33:1–13. https://doi.org/10.1007/s10811-020-02308-9

    Article  CAS  Google Scholar 

  21. Sun H, Zhao W, Mao X et al (2018) High-value biomass from microalgae production platforms: strategies and progress based on carbon metabolism and energy conversion. Biotechnol Biofuels 11:227. https://doi.org/10.1186/s13068-018-1225-6

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  22. Rearte TA, Figueroa FL, Gómez-Serrano C et al (2020) Optimization of the production of lipids and carotenoids in the microalga Golenkinia aff. brevispicula. Algal Res 51:102004

    Article  Google Scholar 

  23. Mitra M, Patidar SK, Mishra S (2015) Integrated process of two stage cultivation of Nannochloropsis sp. for nutraceutically valuable eicosapentaenoic acid along with biodiesel. Bioresour Technol 193:363–369. https://doi.org/10.1016/j.biortech.2015.06.033

    Article  CAS  PubMed  Google Scholar 

  24. Rezaei A, Cheniany M, Ahmadzadeh H, Vaezi J (2023) Evaluation of lipid composition and growth parameters of cold-adapted microalgae under different conditions. BioEnergy Res. https://doi.org/10.1007/s12155-023-10626-2

    Article  Google Scholar 

  25. Campos M, Faria V, Teodoro T et al (2013) Evaluation of the capacity of the cyanobacterium Microcystis novacekii to remove atrazine from a culture medium. J Environ Sci Health B 48:101–107. https://doi.org/10.1080/03601234.2013.726891

    Article  CAS  PubMed  Google Scholar 

  26. Kong WB, Yang H, Cao YT et al (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 

  27. Zhu CJ, Lee YK (1997) Determination of biomass dry weight of marine microalgae. J Appl Phycol 9:189–194. https://doi.org/10.1023/A:1007914806640

    Article  Google Scholar 

  28. Nayek S, Choudhury I et al (2014) Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Res J Chem Sci 4:2231–2606

    Google Scholar 

  29. Lari Z, Abrishamchi P, Ahmadzadeh H, Soltani N (2019) Differential carbon partitioning and fatty acid composition in mixotrophic and autotrophic cultures of a new marine isolate Tetraselmis sp. KY114885. J Appl Phycol 31:201–210. https://doi.org/10.1007/s10811-018-1549-4

    Article  CAS  Google Scholar 

  30. Roshith CM, Meena DK, Manna RK et al (2018) Phytoplankton community structure of the Gangetic (Hooghly-Matla) estuary: Status and ecological implications in relation to eco-climatic variability. Flora 240:133–143. https://doi.org/10.1016/j.flora.2018.01.001

    Article  Google Scholar 

  31. Cao K, He M, Yang W et al (2016) The eurythermal adaptivity and temperature tolerance of a newly isolated psychrotolerant Arctic Chlorella sp. J Appl Phycol 28:877–888. https://doi.org/10.1007/s10811-015-0627-0

    Article  CAS  Google Scholar 

  32. Goldsborough LG, Robinson GGC (1996) 4 - Pattern in Wetlands**Contribution 248 from the University Field Station (Delta Marsh), University of Manitoba, Winnipeg. In: Stevenson RJ, Bothwell ML, Lowe RLBT-AE (eds) Aquatic ecology. Academic Press, San Diego, p. 77–117

  33. Valledor L, Furuhashi T, Hanak AM, Weckwerth W (2013) Systemic cold stress adaptation of Chlamydomonas reinhardtii. Mol Cell Proteomics 12:2032–2047. https://doi.org/10.1074/mcp.M112.026765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Cvetkovska M, Hüner NPA, Smith DR (2017) Chilling out: the evolution and diversification of psychrophilic algae with a focus on Chlamydomonadales. Polar Biol 40:1169–1184. https://doi.org/10.1007/s00300-016-2045-4

    Article  Google Scholar 

  35. Randhir A, Laird DW, Maker G et al (2020) Microalgae: a potential sustainable commercial source of sterols. Algal Res 46:101772. https://doi.org/10.1016/j.algal.2019.101772

    Article  Google Scholar 

  36. Kilham S, Kreeger D, Goulden C, Lynn S (1997) Effects of nutrient limitation on biochemical constituents of Ankistrodesmus falcatus. Freshw Biol 38:591–596. https://doi.org/10.1046/j.1365-2427.1997.00231.x

    Article  CAS  Google Scholar 

  37. Singh P, Guldhe A, Kumari S et al (2014) Investigation of combined effect of nitrogen, phosphorus and iron on lipid productivity of Ankistrodesmus falcatus KJ671624 using response surface methodology. Biochem Eng J. https://doi.org/10.1016/j.bej.2014.10.019

    Article  Google Scholar 

  38. Liyanaarachchi VC, Premaratne M, Ariyadasa TU et al (2021) Two-stage cultivation of microalgae for production of high-value compounds and biofuels: a review. Algal Res 57:102353. https://doi.org/10.1016/j.algal.2021.102353

    Article  Google Scholar 

  39. Ahn JW, Hwangbo K, Lee SY et al (2012) A new Arctic Chlorella species for biodiesel production. Bioresour Technol 125:340–343. https://doi.org/10.1016/j.biortech.2012.09.026

    Article  CAS  PubMed  Google Scholar 

  40. Li X, Wang X, Duan C et al (2020) Biotechnological production of astaxanthin from the microalga Haematococcus pluvialis. Biotechnol Adv 43:107602. https://doi.org/10.1016/j.biotechadv.2020.107602

    Article  CAS  PubMed  Google Scholar 

  41. Sansone C, Brunet C (2019) Promises and challenges of microalgal antioxidant production. Antioxidants 8:199. https://doi.org/10.3390/antiox8070199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Aziz MMA, Kassim KA, Shokravi Z et al (2020) Two-stage cultivation strategy for simultaneous increases in growth rate and lipid content of microalgae: a review. Renew Sustain Energy Rev 119:109621. https://doi.org/10.1016/j.rser.2019.109621

    Article  CAS  Google Scholar 

  43. Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167. https://doi.org/10.1016/S0167-7799(00)01433-5

    Article  CAS  PubMed  Google Scholar 

  44. Solovchenko AE, Khozin-Goldberg I, Didi-Cohen S et al (2008) Effects of light and nitrogen starvation on the content and composition of carotenoids of the green microalga Parietochloris incisa. Russ J Plant Physiol 55:455–462. https://doi.org/10.1134/S1021443708040043

    Article  CAS  Google Scholar 

  45. Morgan-Kiss RM, Priscu JC, Pocock T et al (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252. https://doi.org/10.1128/MMBR.70.1.222-252.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Solovchenko AE, Khozin-Goldberg I, Cohen Z, Merzlyak MN (2009) Carotenoid-to-chlorophyll ratio as a proxy for assay of total fatty acids and arachidonic acid content in the green microalga Parietochloris incisa. J Appl Phycol 21:361–366. https://doi.org/10.1007/s10811-008-9377-6

    Article  CAS  Google Scholar 

  47. Sforza E, Gris B, De Farias SC et al (2014) Effects of light on cultivation of scenedesmus obliquus in batch and continuous flat plate photobioreactor. Chem Eng Trans 38:211–216. https://doi.org/10.3303/CET1438036

    Article  Google Scholar 

  48. Aléman-Nava GS, Muylaert K, Cuellar Bermudez SP et al (2017) Two-stage cultivation of Nannochloropsis oculata for lipid production using reversible alkaline flocculation. Bioresour Technol 226:18–23. https://doi.org/10.1016/j.biortech.2016.11.121

    Article  CAS  PubMed  Google Scholar 

  49. Su C-H, Chien L-J, Gomes J et al (2011) Factors affecting lipid accumulation by Nannochloropsis oculata in a two-stage cultivation process. J Appl Phycol 23:903–908. https://doi.org/10.1007/s10811-010-9609-4

    Article  CAS  Google Scholar 

  50. Sun Z, Wei H, Zhou Z-G et al (2018) Screening of Isochrysis strains and utilization of a two-stage outdoor cultivation strategy for algal biomass and lipid production. Appl Biochem Biotechnol 185:1–18. https://doi.org/10.1007/s12010-018-2717-3

    Article  CAS  Google Scholar 

  51. Benavente-Valdés JR, Aguilar C, Contreras-Esquivel JC et al (2016) Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnol Rep 10:117–125. https://doi.org/10.1016/j.btre.2016.04.001

    Article  Google Scholar 

  52. Morales M, Aflalo C, Bernard O (2021) Microalgal lipids: a review of lipids potential and quantification for 95 phytoplankton species. Biomass Bioenerg 150:106108. https://doi.org/10.1016/j.biombioe.2021.106108

    Article  CAS  Google Scholar 

  53. Xiao Y, Zhang J, Cui J et al (2013) Metabolic profiles of Nannochloropsis oceanica IMET1 under nitrogen-deficiency stress. Bioresour Technol 130:731–738. https://doi.org/10.1016/j.biortech.2012.11.116

    Article  CAS  PubMed  Google Scholar 

  54. Liu X-J, Jiang Y, Chen F (2005) Fatty acid profile of the edible filamentous cyanobacterium Nostoc flagelliforme at different temperatures and developmental stages in liquid suspension culture. Process Biochem 40:371–377. https://doi.org/10.1016/j.procbio.2004.01.018

    Article  CAS  Google Scholar 

  55. Xia L, Song S, Hu C (2016) High temperature enhances lipid accumulation in nitrogen-deprived Scenedesmus obtusus XJ-15. J Appl Phycol 28:831–837. https://doi.org/10.1007/s10811-015-0636-z

    Article  CAS  Google Scholar 

  56. Jiang H, Gao K (2004) Effects of lowering temperature during culture on the production of polyunsaturated fatty acids in the marine diatom phaeodactylum tricornutum (bacillariophyceae). J Phycol. https://doi.org/10.1111/j.1529-8817.2004.03112.x

    Article  Google Scholar 

  57. Zheng Y, Xue C, Chen H et al (2020) Low-temperature adaptation of the snow alga chlamydomonas nivalis is associated with the photosynthetic system regulatory process. Front Microbiol. https://doi.org/10.3389/fmicb.2020.01233

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank prof.dr.ir. RH (Rene) Wijffels and prof.dr. MJ (Maria) Barbosa from Wageningen University, Netherlands, for using their fluorescence-activated cell sorting to isolate and purify strains.

Funding

Financial support was provided by Ferdowsi University of Mashhad (grant no. 3/45727).

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, 91779-48974, Iran

    Azar Rezaei, Monireh Cheniany & Jamil Vaezi

  2. Department of Chemistry, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, 91779-48974, Iran

    Hossein Ahmadzadeh

Authors
  1. Azar Rezaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monireh Cheniany
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hossein Ahmadzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jamil Vaezi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AR: conceptualization, methodology, investigation, formal analysis, writing-original draft. MC: supervision, conceptualization, resources, writing-review & editing. HA: supervision, conceptualization, resources, writing-review & editing. JV: methodology, writing-review.

Corresponding authors

Correspondence to Monireh Cheniany or Hossein Ahmadzadeh.

Ethics declarations

Conflict of interest

The authors declare there is no conflict of interest regarding the publication of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rezaei, A., Cheniany, M., Ahmadzadeh, H. et al. A new isolate cold-adapted Ankistrodesmus sp. OR119838: influence of light, temperature, and nitrogen concentration on growth characteristics and biochemical composition using the two-stage cultivation strategy. Bioprocess Biosyst Eng 47, 341–353 (2024). https://doi.org/10.1007/s00449-023-02964-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-023-02964-4

Keyword

Search

Navigation