Physiological Properties of Photoautotrophic Microalgae and Cyanobacteria Relevant to Industrial Biomass Production

  • Mikio Tsuzuki
  • Katsuhiko OkadaEmail author
  • Haruna Isoda
  • Masayuki Hirano
  • Tetsuo Odaka
  • Hirotaka Saijo
  • Risa Aruga
  • Hiroki Miyauchi
  • Shoko FujiwaraEmail author
Original Article


Photoautotrophic mass culture of microalgae is currently under investigation for social implementation, since such organisms are anticipated to be resources of alternative fuels and materials for reducing global warming. Production scale-up of culture systems and economy balance are great barriers for practical usage. In order to develop new culture systems such as attachment on solid surfaces or biofilms, we investigated various characteristics of photosynthesis in Chlorella, not only in liquid but also on filter membranes. In aquatic cultures, the photosynthetic rate was almost the same as the specific exponential growth rate at over 32 °C, suggesting that highly efficient cell growth was achieved at that temperature. The algal cells could fix about 50 mmol carbons per mole photons, at cloudy-day-level light intensities, which result to produce 1.2 g dry cell weight in calculation. Moreover, Chlorella could grow on a membrane surface at almost the same rate as in liquid. Similar tolerance to water deficiency was observed in a cyanobacterium, Synechocystis, in which gene expression responded in 30 min after the stress. Such a tolerance was also observed in other species of microalgae and cyanobacteria in photosynthesis.


Photosynthesis Algae Culture system Chlorella Cyanobacteria Biomass 



The authors are indebted to Ms. Sachi Masui, Ms. Makiko Miyaji, and Ms. Marii Takahashi for their technical assistance, and to Mr. N. J. Halewood for correcting the English version of this paper.

Author Contributions

M T, K O, and S F conceived and designed the project; K O, H I, M H, T O, H S, R A, H M, and K H collected the data; M T, K O, H M, and S F analyzed the data; all authors were involved in writing the article and had final approval of the submitted and published versions.

Funding Information

This research was supported by the Ministry of Education, Science and Culture, CREST of Japan Science and Technology, and Kawasaki City.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interest.

Supplementary material

10126_2019_9890_MOESM1_ESM.pptx (61 kb)
ESM 1 (PPTX 61.1 kb)


  1. Abu-Ghosh S, Fixier D, Dubinsky Z, Iluz D (2016) Flashing light in microalgae biotechnology. Bioresour Technol 203:357–363CrossRefGoogle Scholar
  2. Anemaet IG, Bekker M, Hellingwerf KJ (2010) Algal photosynthesis as the primary driver for a sustainable development in energy, feed, and food production. Mar Biotechnol 12:619–629CrossRefGoogle Scholar
  3. Aoki J, Kawamata T, Kodaka A, Minakawa M, Tsuzuki M, Asayama M (2018) Biofuel production utilizing a dual-phase cultivation system with filamentous cyanobacteria. J Biotechnol 280:55–61CrossRefGoogle Scholar
  4. Chiu S-Y, Kao C-Y, Chen T-Y, Chang Y-B, Kuo C-M, Lin C-S (2015) Cultivation of microalgal Chlorella for biomass and lipid production using wastewater as nutrient resource. Bioresour Technol 184:179–189CrossRefGoogle Scholar
  5. Choudhary P, Malik A, Pant KK (2017) Mass-scale algal biomass production using algal biofilm reactor and conversion to energy and chemical precursors by hydropyrolysis. ACS Sustain Chem Eng 5:4234–4242CrossRefGoogle Scholar
  6. de Vree JH, Bosma R, Janssen M, Barbosa MJ, Wijffels RH (2015) Comparison of four outdoor pilot-scale photobioreactors. Biotechnol Biofuels 8:215–226CrossRefGoogle Scholar
  7. Desplats P, Folco E, Saleno GL (2005) Sucrose may play an additional role to that of an osmolyte in Synechocystis sp. PCC 6803 salt-shocked cells. Plant Physiol Biochem 43:133–138CrossRefGoogle Scholar
  8. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158CrossRefGoogle Scholar
  9. Gross M, Mascarenhas V, Wen Z (2015) Evaluating algal growth performance and water use efficiency of pilot-scale revolving algal biofilm (RAB) culture systems. Biotechnol Bioeng 112:2040–2050CrossRefGoogle Scholar
  10. Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequence for ultrastructure, physiological and molecular mechanism. Front Plant Sci 4:327CrossRefGoogle Scholar
  11. Kanesaki Y, Suzuki I, Allakhverdiev SI, Mikami K, Murata N (2002) Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 290:339–348CrossRefGoogle Scholar
  12. Kazamia E, Smith A (2014) Assessing the environmental sustainability of biofuels. Trends Plant Sci 19:615–618CrossRefGoogle Scholar
  13. Liu T, Wang J, Hu Q, Cheng P, Ji B, Liu J, Chen Y, Zhang W, Chen X, Chen L, Gao L, Ji C, Wang H (2013) Attached cultivation technology of microalgae for efficient biomass feedstock production. Bioresour Technol 127:216–222CrossRefGoogle Scholar
  14. Long SP, Zhu X-G, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330CrossRefGoogle Scholar
  15. Lynd LR, Laser MS, Bransby D, Dale BE, Davison B, Hamilton R, Himmel M, Keller M, McMillan JD, Sheehan J, Wyman CE (2008) How biotech can transform biofuels. Nat Biotechnol 26:169–172CrossRefGoogle Scholar
  16. Marin K, Stirnberg M, Eisenhut M, Krämer R, Hagemann M (2006) Osmotic stress in Synechocystis sp. PCC 6803: low tolerance towards nonionic osmotic stress results from lacking activation of glucosylglycerol accumulation. Microbiol 152:2023–2030CrossRefGoogle Scholar
  17. Martin-Girela I, Curt MD, Fernandez J (2017) Flashing light effects on CO2 absorption by microalgae grown on a biofilm photobioreactor. Algal Res 25:421–430CrossRefGoogle Scholar
  18. Mascarelli AL (2009) Gold rush for algae. Nature 461:460–461CrossRefGoogle Scholar
  19. Miyachi S, Tsuzuki M, Avramova ST (1983) Utilization modes of inorganic carbon for photosynthesis in various species of Chlorella. Plant Cell Physiol 24:441–451Google Scholar
  20. Ochsenreither K, Glück C, Stressler T, Fischer L, Syldatk C (2016) Production strategies and applications of microbial single cell oils. Front Microbiol 7:1539CrossRefGoogle Scholar
  21. Ohkubo K, Aburai N, Miyauchi H, Tsuzuki M, Abe K (2017) CO2 fixation and lipid accumulation in biofilms of the aerial microalga Coccomyxa sp. KGU-D001 (Trebouxiophyceae). J Appl Phycol 29:1745–1753CrossRefGoogle Scholar
  22. Okada K, Horii E, Nagashima Y, Mitsui M, Matsuura H, Fujiwara S, Tsuzuki M (2015) Genes for a series of proteins that are involved in glucose catabolism are upregulated by the Hik8-cascade in Synechocystis sp. PCC 6803. Planta 241:1453–1462CrossRefGoogle Scholar
  23. Olivier JGJ, Janssens-Maenhout G, Muntean M, Peters JAHW (2016) Trends in global CO2 emissions: 2016 report. PBL Netherlands Environmental Assessment Agency, The Hague; European Commission, Joint Research Centre, IspraGoogle Scholar
  24. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805Google Scholar
  25. Schultze LKP, Simon M-V, Li T, Langenbach D, Podola B, Melkonian M (2015) High light and carbon dioxide optimize surface productivity in a twin-layer biofilm photobioreactor. Algal Res 8:37–45CrossRefGoogle Scholar
  26. Schuurmans RM, van Alphen P, Schuurmans JM, Matthijs HCP, Hellingwerf KJ (2015) Comparison of the photosynthetic yield of cyanobacteria and green algae: different methods give different answers. PLoS One 10:e0139061CrossRefGoogle Scholar
  27. Seth JR, Wangikar PP (2015) Challenges and opportunities for microalgae-mediated CO2 capture and refinery. Biotechnol Bioeng 112:1281–1296CrossRefGoogle Scholar
  28. Sueoka N, Chiang KS, Kates JR (1967) Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardtii I Isotopic transfer experiments with a strain producing eight zoospores. J Mol Biol 25:44–67CrossRefGoogle Scholar
  29. Suzuki M, Watanabe K, Fujiwara S, Kurasawa T, Wakabayashi T, Tsuzuki M, Iguchi K, Yamori T (2003) Isolation of peridinin-related norcarotenoids with cell growth-inhibitory activity from the cultured dinoflagellate of Symbiodinium sp., a symbiont of the Okinawan soft coral Clavularia viridis, and analysis of fatty acids of the dinoflagellate. Chem Pharm Bull 51:724–727CrossRefGoogle Scholar
  30. Takayanagi T, Hirokawa Y, Yamamoto M, Ohki T, Fujiwara S, Tsuzuki M (2007) Protoplast formation of the coccolithophorid Pleurochrysis haptonemofera in hypoosmotic K+ solution: shedding of the coccosphere and regrowth of the protoplast in normal medium. Mar Biotechnol 9:56–65CrossRefGoogle Scholar
  31. Tsutsumi M, Kawaguchi K, Kaneko M, Tsuzuki M (1995) CO2 fixation system by Chlorella on a filter membrane. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol V. Kluwer, pp881–884Google Scholar
  32. Tsuzuki M, Shiraiwa Y, Miyachi S (1980) Role of carbonic anhydrase in photosynthesis in Chlorella derived from kinetic analysis of 14CO2 fixation. Plant Cell Physiol 21:677–688CrossRefGoogle Scholar
  33. Tsuzuki M, Shiratake T, Suzuki M, Saijo H, Asayama M, Miyasaka Y, Okada K, Imamura N, Konishi J (2012) A new culture system for microalgae under LED illumination. The Bulletin of Tokyo University of Pharmacy and Life Sciences 15:9–16 (Japanese) ISSN 1343-8956Google Scholar
  34. Unkefer CJ, Sayre RT, Magnuson JK, Anderson DB, Baxter I, Blaby IK, Brown JK, Carleton M, Cattolico RA, Dale T, Devarenne TP, Downes CM, Dutcher SK, Fox DT, Goodenough U, Jaworski J, Holladay JE, Kramer DM, Olivares JA (2017) Review of the algal biology program within the National Alliance for Advanced Biofuels and Bioproducts. Algal Res 22:187–215CrossRefGoogle Scholar
  35. Vitova M, Bisova K, Kawano S, Zachleder V (2015) Accumulation of energy reserves in algae: from cell cycles to biotechnological applications. Biotechnol Adv 33:1204–1218CrossRefGoogle Scholar
  36. Walker D (2009) Biofuels, facts, fantasy and feasibility. J Appl Phycol 21:509–517CrossRefGoogle Scholar
  37. Watanabe A (1960) List of algal strains on collection at the Institute of Applied Microbiology, University of Tokyo. J Gen Appl Microbiol 6:283–292CrossRefGoogle Scholar
  38. Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799CrossRefGoogle Scholar
  39. Zhou W, Wang J, Chen P, Ji C, Kang Q, Lu B, Li K, Liu J, Ruan R (2017) Bio-mitigation of carbon dioxide using microalgal systems: advances and perspectives. Renew Sust Energ Rev 76:1163–1175CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Mikio Tsuzuki
    • 1
  • Katsuhiko Okada
    • 1
    Email author
  • Haruna Isoda
    • 1
  • Masayuki Hirano
    • 1
  • Tetsuo Odaka
    • 1
  • Hirotaka Saijo
    • 1
  • Risa Aruga
    • 1
  • Hiroki Miyauchi
    • 1
  • Shoko Fujiwara
    • 1
    Email author
  1. 1.School of Life SciencesTokyo University of Pharmacy and Life SciencesHachiojiJapan

Personalised recommendations