Photosynthetica, 2019 (vol. 57), issue 2

Photosynthetica 2019, 57(2):617-626 | DOI: 10.32615/ps.2019.056

Photoinhibition and continuous growth of the wild-type and a high-light tolerant strain of Chlamydomonas reinhardtii

O. VIRTANEN1, D. VALEV1, O. KRUSE2, L. WOBBE2, E. TYYSTJÄRVI1
1 University of Turku, Department of Biochemistry/Molecular Plant Biology, 20014 Turku, Finland
2 Bielefeld University, Algae Biotechnology and Bioenergy, Faculty of Biology, Center for Biotechnology (CeBiTec), Universitätsstrasse 27, 33615 Bielefeld, Germany

The volumetric productivity of the high-light tolerant strain hit2 of Chlamydomonas reinhardtii was found to be higher than that of the parental strain CC124 during continuous growth at PPFD from 200 to 1,500 µmol m-2 s-1. At PPFD of 1,250 µmol m-2 s-1, hit2 produced 2.53 ± 0.18 and CC124 produced 2.05 ± 0.12 g(biomass) dm-3 d-1. The rate constant of photoinhibition of hit2 was less than half of that of CC124, suggesting that hit2 produces more biomass than CC124 because hit2 does not need to allocate as much resources for PSII repair as CC124. Growth in high light triggered similar loss of chlorophyll, increase in the carotenoid-to-chlorophyll ratio, and decrease in PSI fluorescence in both strains. Thermoluminescence B band was shifted toward the Q band in hit2, suggesting that low redox potential of the QB/QB- pair contributes to the photoinhibition tolerance of hit2.

Additional key words: algae; biomass production; carotenoid; growth rate; nonphotochemical quenching; turbidostat.

Received: September 22, 2018; Accepted: March 15, 2019; Prepublished online: April 29, 2019; Published: May 16, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
VIRTANEN, O., VALEV, D., KRUSE, O., WOBBE, L., & TYYSTJÄRVI, E. (2019). Photoinhibition and continuous growth of the wild-type and a high-light tolerant strain of Chlamydomonas reinhardtii. Photosynthetica57(2), 617-626. doi: 10.32615/ps.2019.056.
Download citation

References

  1. Ananyev G., Gates C., Kaplan A., Dismukes G.C.: Photosystem II-cyclic electron flow powers exceptional photoprotection and record growth in the microalga Chlorella ohadii. - BBA-Bioenergetics 1858: 873-883, 2017.
  2. Andrade L.A., Batista F.R.X., Lira T.S. et al.: Characterization and product formation during the catalytic and non-catalytic pyrolysis of the green microalgae Chlamydomonas rein-hardtii. - Renew. Energ. 119: 731-740, 2018. Go to original source...
  3. Aro E.M., Virgin I., Andersson B.: Photoinhibition of Photo-system II. Inactivation, protein damage and turnover. - BBA-Bioenergetics 1143: 113-134, 1993. Go to original source...
  4. Bonente G., Pippa S., Castellano S. et al.: Acclimation of Chlamydomonas reinhardtii to different growth irradiances. -J. Biol. Chem. 287: 5833-5847, 2012. Go to original source...
  5. Brinkert K., De Causmaecker S., Krieger-Liszkay A. et al.: Bicarbonate-induced redox tuning in Photosystem II for regulation and protection. - P. Natl. Acad. Sci. USA 113: 12144-12149, 2016. Go to original source...
  6. Campbell D.A., Tyystjärvi E.: Parameterization of photosystem II photoinactivation and repair. - BBA-Bioenergetics 1817: 258-265, 2012.
  7. Förster B., Osmond C.B., Pogson B.J.: Improved survival of very high light and oxidative stress is conferred by spontaneous gain-of-function mutations in Chlamydomonas. - BBA-Bioenergetics 1709: 45-57, 2005. Go to original source...
  8. Garnier J., Maroc J., Guyon D.: Low-temperature fluorescence emission spectra and chlorophyll-protein complexes in mutants of Chlamydomonas reinhardtii: evidence for a new chlorophyll-a-protein complex related to Photosystem I. - BBA-Bioenergetics 851: 395-406, 1986. Go to original source...
  9. Gilmore A.M., Yamamoto H.Y.: Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching me-diated by ATP. - P. Natl. Acad. Sci. USA 89: 1899-1903, 1992.
  10. Gorman D.S., Levine R.P.: Cytochrome f and plastocyanin: Their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. - P. Natl. Acad. Sci. USA 54: 1665-1669, 1965. Go to original source...
  11. Goss R., Oroszi S., Wilhelm C.: The importance of grana stacking for xanthophyll cycle-dependent NPQ in the thylakoid mem-branes of higher plants. - Physiol. Plantarum 131: 496-507, 2007. Go to original source...
  12. Hakala M., Tuominen I., Keränen M. et al.: Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. - BBA-Bioenergetics 1706: 68-80, 2005. Go to original source...
  13. Hakala-Yatkin M., Sarvikas P., Paturi P. et al.: Magnetic field protects plants against high light by slowing down production of singlet oxygen. - Physiol. Plantarum 142: 26-34, 2011. Go to original source...
  14. Havurinne V., Tyystjärvi E.: Action spectrum of photoinhibition in the diatom Phaeodactylum tricornutum. - Plant Cell Physiol. 58: 2217-2225, 2017. Go to original source...
  15. Hoops S., Sahle S., Gauges R. et al.: COPASI: a COmplex PAthway SImulator. - Bioinformatics 22: 3067-3074, 2006. Go to original source...
  16. Keränen M., Mulo P., Aro E. et al: Thermoluminescence B and Q bands are at the same temperature in an autotrophic and a heterotrophic D1 protein mutant of Synechocystis sp. PCC6803. - In: Garab G. (ed.): Photosynthesis: Mechanisms and Effects. Pp. 1145-1148. Vol II. Kluwer Academic Publishers, Dordrecht 1996.
  17. Kong Q., Li L., Martinez B. et al.: Culture of microalgae Chlamydomonas reinhardtii in wastewater for biomass feed-stock production. - Appl. Biochem. Biotech. 160: 9-18, 2010. Go to original source...
  18. Krieger A., Moya I., Weis E.: Energy-dependent quenching of chlorophyll a fluorescence: effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid membranes and Photosystem II preparations. - BBA-Bioenergetics 1102: 167-176, 1992. Go to original source...
  19. Krieger A., Rutherford A.W., Johnson G.N.: On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in Photosystem II. - BBA-Bioenergetics 1229: 193-201, 1995. Go to original source...
  20. Krieger-Liszkay A., Fufezan C., Trebst A.: Singlet oxygen pro-duction in photosystem II and related protection mechanism. -Photosynth. Res. 98: 551-564, 2008. Go to original source...
  21. Kropat J., Hong-Hermesdorf A., Casero D. et al.: A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. - Plant J. 66: 770-780, 2011. Go to original source...
  22. Lin T.H., Rao M.Y., Lu H.W. et al.: A role for glutathione reductase and glutathione in the tolerance of Chlamydomonas reinhardtii to photo-oxidative stress. - Physiol. Plantarum 162: 35-48, 2018. Go to original source...
  23. Mulders K.J.M., Lamers P.P., Martens D.E., Wijffels R.H.: Phototrophic pigment production with microalgae: biological constraints and opportunities. - J. Phycol. 50: 229-242, 2014. Go to original source...
  24. Mulo P., Laakso S., Mäenpää P., Aro E.-M.: Stepwise photo-inhibition of Photosystem II. - Plant Physiol. 117: 483-490, 1998. Go to original source...
  25. Muramatsu M., Hihara Y.: Acclimation to high-light conditions in cyanobacteria: from gene expression to physiological responses. - J. Plant Res. 125: 11-39, 2012. Go to original source...
  26. Murata N., Nishiyama Y.: ATP is a driving force in the repair of photosystem II during photoinhibition. - Plant Cell Environ. 41: 285-299, 2018. Go to original source...
  27. Nishiyama Y., Yamamoto H., Allakhverdiev S.I. et al.: Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. - EMBO J. 20: 5587-5594, 2001. Go to original source...
  28. Ramel F., Birtic S., Cuiné S. et al.: Chemical quenching of singlet oxygen by carotenoids in plants. - Plant Physiol. 158: 1267-1278, 2012. Go to original source...
  29. Roach T., Baur T., Stöggl W., Krieger-Liszkay A.: Chlamydomonas reinhardtii responding to high light: a role for 2-propenal (acrolein). - Physiol. Plantarum 161: 75-87, 2017. Go to original source...
  30. Roach T., Na C.S.: LHCSR3 affects de-coupling and re-coupling of LHCII to PSII during state transitions in Chlamydomonas reinhardtii. - Sci. Rep. 7: 431-454, 2017. Go to original source...
  31. Sarvikas P., Hakala M., Pätsikkä E. et al.: Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. - Plant Cell Physiol. 47: 391-400, 2006. Go to original source...
  32. Schierenbeck L., Ries D., Rogge K. et al.: Fast forward genetics to identify mutations causing a high light tolerant phenotype in Chlamydomonas reinhardtii by whole-genome-sequencing. -BMC Genomics 16: 57, 2015. Go to original source...
  33. Schumann T., Paul S., Melzer M. et al.: Plant growth under natural light conditions provides highly flexible short-term acclimation properties toward high light stress. - Front. Plant Sci. 8: 681, 2017. Go to original source...
  34. Sforza E., Simionato D., Giacometti G.M. et al.: Adjusted light and dark cycles can optimize photosynthetic efficiency in algae growing in photobioreactors. - PLoS ONE 7: e38975, 2012. Go to original source...
  35. Singh S.P., Singh P.: Effect of temperature and light on the growth of algae species: A review. - Renew. Sust. Energ. Rev. 50: 431-444, 2015. Go to original source...
  36. Solovchenko A., Neverov K.: Carotenogenic response in photo-synthetic organisms: a colorful story. - Photosynth. Res. 133: 31-47, 2017. Go to original source...
  37. Takahashi S., Murata N.: Interruption of the Calvin cycle inhibits the repair of Photosystem II from photodamage. - BBA-Bioenergetics 1708: 352-361, 2005. Go to original source...
  38. Tilbrook K., Dubois M., Crocco C.D. et al.: UV-B perception and acclimation in Chlamydomonas reinhardtii. - Plant Cell 28: 966-983, 2016. Go to original source...
  39. Treves H., Raanan H., Kedem I. et al.: The mechanisms whereby the green alga Chlorella ohadii, isolated from desert soil crust, exhibits unparalleled photodamage resistance. - New Phytol. 210: 1229-1243, 2016. Go to original source...
  40. Tyystjärvi E., Aro E.M.: The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. - P. Natl. Acad. Sci. USA 93: 2213-2218, 1996. Go to original source...
  41. Tyystjärvi E., Tyystjärvi J., Rantamäki S.: Connectivity of photo-system II is the physical basis of retrapping in photosynthetic thermoluminescence. - Biophys. J. 96: 3735-3743, 2009. Go to original source...
  42. Tyystjärvi E.: Photoinhibition of Photosystem II. - Int. Rev. Cel. Mol. Bio. 300: 243-303, 2013. Go to original source...
  43. Ünlü C., Drop B., Croce R., van Amerongen H.: State transitions in Chlamydomonas reinhardtii strongly modulate the fun-ctional size of photosystem II but not photosystem I. - P. Natl. Acad. Sci. USA 111: 3460-3465, 2014.
  44. Wellburn A.R.: The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. - J. Plant Physiol. 144: 307-313, 1994. Go to original source...
  45. Wobbe L., Bassi R., Kruse O.: Multi-level light capture control in plants and green algae. - Trends Plant Sci. 21: 55-68, 2016. Go to original source...
  46. Xing J., Liu P., Zhao L., Huang F.: Deletion of CGLD1 impairs PSII and increases singlet oxygen tolerance of green alga Chlamydomonas reinhardtii. - Front. Plant Sci. 8: 2154, 2017. Go to original source...
  47. Xu Y., Guerra L.T., Li Z. et al.: Altered carbohydrate metabolism in glycogen synthase mutants of Synechococcus sp. strain PCC 7002: Cell factories for soluble sugars. - Metab. Eng. 16: 56-67, 2013. Go to original source...
  48. Yang L., Chen J., Qin S. et al.: Growth and lipid accumulation by different nutrients in the microalga Chlamydomonas reinhardtii. - Biotechnol. Biofuels 11: 40, 2018. Go to original source...
  49. Yang Y., Gao K.: Effects of CO2 concentrations on the freshwater microalgae, Chlamydomonas reinhardtii, Chlorella pyre-noidosa and Scenedesmus obliquus (Chlorophyta). - J. Appl. Phycol. 15: 378-389, 2003. Go to original source...
  50. Yin Z., Johnson G.N.: Photosynthetic acclimation of higher plants to growth in fluctuating light environments. - Photosynth. Res. 63: 97-107, 2000. Go to original source...