Skip to main content
Log in

Influence of Fermentation Reactions on Continuous Hydrogen Photoproduction by Microalga Chlamydomonas reinhardtii under Sulfur Deficiency

  • RESEARCH ARTICLE
  • Published:
Moscow University Biological Sciences Bulletin Aims and scope Submit manuscript

Abstract

The study investigated the effect of the major fermentation enzyme, pyruvate formate lyase, on hydrogen photoproduction by green microalga Chlamydomonas reinhardtii under mineral deprivation. Cultures of the wild type (CC-125) and mutant pfl1 without pyruvate formate lyase activity were incubated on a medium without sulfur in the sealed photoreactors under constant illumination for 96 h. During the experiment, accumulation of hydrogen in a gas phase of photoreactors and factors affecting hydrogen production, such as photosynthetic activity, respiration, and starch content, in cells were assessed. Both strains showed similar photosynthetic activity and starch content when cultivated in the complete medium. Under sulfur depletion, the cultures of the pfl1 mutant began to evolve hydrogen later than the wild type; however, this process lasted much longer in the mutant. The pfl1 cultures showed higher rates of starch accumulation and breakdown during the initial and late stages of sulfur deprivation, respectively. Moreover, the mutant was characterized by higher photosynthetic activity at the later stage of deprivation. The obtained results indicate close relationships between photosynthetic electron transport, hydrogenase reaction, carbohydrate metabolism and fermentation process, pointing to the prospect of using genetic engineering to modify fermentation reactions in order to improve photosynthetic hydrogen production in biotechnology.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Antal, T.K., The metabolic acclimation of Chlamydomonas reinhardtii to depletion of essential nutrients: application for hydrogen production, in Microalgal Hydrogen Production: Achievements and Perspectives, Seibert, M. and Torzillo, G., Eds., RSC Publishing, 2018, pp. 235–264.

    Google Scholar 

  2. Kosourov, S., Böhm, M., Senger, M., Berggren, G., Stensjö, K., Mamedov, F., Lindblad, P., and Allahverdiyeva, Y., Photosynthetic hydrogen production: Novel protocols, promising engineering approaches and application of semi-synthetic hydrogenases, Physiol. Plant., 2021, vol. 173, no. 2, pp. 555–567.

    Article  CAS  Google Scholar 

  3. Antal, T., Petrova, E., Slepnyova, V., Kukarskikh, G., Volgusheva, A., Dubini, A., Baizhumanov, A., Tyystjärvi, T., Gorelova, O., Baulina, O., Chivkunova, O., Solovchenko, A., and Rubin, A., Photosynthetic hydrogen production as acclimation mechanism in nutrient-deprived Chlamydomonas, Algal Res., 2020, vol. 49, art. ID 101951.

    Article  Google Scholar 

  4. Antal, T.K., Krendeleva, T.E., Laurinavichene, T.V., Makarova, V.V., Ghirardi, M.L., Rubin, A.B., Tsygankov, A.A., and Seibert, M., The dependence of algal H2 production on Photosystem II and O2 consumption activities in sulfur-deprived Chlamydomonas reinhardtii cells, Biochim. Biophys. Acta, 2003, vol. 1607, nos. 2–3, pp. 153–160.

    Article  CAS  Google Scholar 

  5. Kosourov, S., Seibert, M., and Ghirardi, M.L., Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H2-producing Chlamydomonas reinhardtii cultures, Plant Cell Physiol., 2003, vol. 44, no. 2, pp. 146–155.

    Article  CAS  Google Scholar 

  6. Gfeller, R.P. and Gibbs, M., Fermentative metabolism of Chlamydomonas reinhardtii 1: I. analysis of fermentative products from starch in dark and light, Plant Physiol., 1984, vol. 75, no. 1, pp. 212–218.

    Article  CAS  Google Scholar 

  7. Atteia, A., van Lis, R., Gelius-Dietrich, G., Adrait, A., Garin, J., Joyard, J., Rolland, N., and Martin, W., Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria, J. Biol. Chem., 2006, vol. 281, no. 15, pp. 9909–9918.

    Article  CAS  Google Scholar 

  8. Terashima, M., Specht, M., Naumann, B., and Hippler, M., Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics, Mol. Cell Proteomics., 2010, vol. 9, no. 7, pp. 1514–1532.

    Article  CAS  Google Scholar 

  9. Philipps, G., Krawietz, D., Hemschemeier, A., and Happe, T., A pyruvate formate lyase-deficient Chla-mydomonas reinhardtii strain provides evidence for a link between fermentation and hydrogen evolution in green algae, Plant J., 2011, vol. 66, no. 2, pp. 330–340.

    Article  CAS  Google Scholar 

  10. Catalanotti, C., Dubini, A., Subramanian, V., Yang, W., Magneschi, L., Mus, F., Seibert, M., Posewitz, M.C., and Grossman, A.R., Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase, Plant Cell., 2012, vol. 24, no. 2, pp. 692–707.

    Article  CAS  Google Scholar 

  11. Burgess, S.J., Tredwell, G., Molnàr, A., Bundy, J.G., and Nixon, P.J., Artificial microRNA-mediated knockdown of pyruvate formate lyase (PFL1) provides evidence for an active 3-hydroxybutyrate production pathway in the green alga Chlamydomonas reinhardtii, J. Biotechnol., 2012, vol. 162, no. 1, pp. 57–66.

    Article  CAS  Google Scholar 

  12. Laurinavichene, T., Tolstygina, I., and Tsygankov, A., The effect of light intensity on hydrogen production by sulfur-deprived Chlamydomonas reinhardtii, J. Biotechnol., 2004, vol. 114, nos. 1–2, pp. 143−151.

    Article  CAS  Google Scholar 

  13. Lichtenthaler, H.K., Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes, in Methods in Enzymology, Douce R., and Packer. L., Eds., New York: Press Inc., 1987, vol. 148, pp. 350–382.

  14. Shreiber, U., Hormann, H., Neubauer, C., and Klughammer, C., Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis, Plant Physiol., 1995, vol. 22, no. 2, pp. 209−220.

    Google Scholar 

  15. Hemschemeier, A., Fouchard, S., Cournac, L., Peltier, G., and Happe, T., Hydrogen production by Chla-mydomonas reinhardtii: an elaborate interplay of electron sources and sinks, Planta, 2008, vol. 227, no. 2, pp. 397−407.

    Article  CAS  Google Scholar 

  16. Volgusheva, A., Styring, S., and Mamedov, F., Increased photosystem II stability promotes H2 production in sulfur-deprived Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 18, pp. 7223–7228.

    Article  CAS  Google Scholar 

Download references

Funding

The research was funded by the Russian Science Foundation, project number 20-64-46018. The results obtained by using fluorescence methods were carried out with support of the Scientific Project of Moscow State University, no. 121032500058-7.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. A. Volgusheva.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any studies involving animals or human participants performed by any of the authors.

CONFLICT OF INTEREST

The authors declare that they have no conflicts of interest.

Additional information

Translated by V. Mittova

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Volgusheva, A.A., Petrova, E.V., Kukarskikh, G.P. et al. Influence of Fermentation Reactions on Continuous Hydrogen Photoproduction by Microalga Chlamydomonas reinhardtii under Sulfur Deficiency. Moscow Univ. Biol.Sci. Bull. 77, 25–31 (2022). https://doi.org/10.3103/S0096392522010060

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0096392522010060

Keywords:

Navigation