Advertisement

Photosynthesis Research

, Volume 139, Issue 1–3, pp 145–154 | Cite as

Adaptation of light-harvesting functions of unicellular green algae to different light qualities

  • Yoshifumi Ueno
  • Shimpei Aikawa
  • Akihiko Kondo
  • Seiji AkimotoEmail author
Original Article

Abstract

Oxygenic photosynthetic organisms perform photosynthesis efficiently by distributing captured light energy to photosystems (PSs) at an appropriate balance. Maintaining photosynthetic efficiency under changing light conditions requires modification of light-harvesting and energy-transfer processes. In the current study, we examined how green algae regulate their light-harvesting functions in response to different light qualities. We measured low-temperature time-resolved fluorescence spectra of unicellular green algae Chlamydomonas reinhardtii and Chlorella variabilis cells grown under different light qualities. By observing the delayed fluorescence spectra, we demonstrated that both types of green algae primarily modified the associations between light-harvesting chlorophyll protein complexes (LHCs) and PSs (PSII and PSI). Under blue light, Chlamydomonas transferred more energy from LHC to chlorophyll (Chl) located far from the PSII reaction center, while energy was transferred from LHC to PSI via different energy-transfer pathways in Chlorella. Under green light, both green algae exhibited enhanced energy transfer from LHCs to both PSs. Red light induced fluorescence quenching within PSs in Chlamydomonas and LHCs in Chlorella. In Chlorella, energy transfer from PSII to PSI appears to play an important role in balancing excitation between PSII and PSI.

Keywords

Light harvesting Energy transfer Light adaptation Green algae Photosystem 

Abbreviations

Car

Carotenoid

Chl

Chlorophyll

DF

Delayed fluorescence

FDAS

Fluorescence decay-associated spectrum (spectra)

LED

Light-emitting diodes

LHC

Light-harvesting chlorophyll protein complex

LHCSR

Light-harvesting complex stress-related

PBS

Phycobilisome

PC

Phycocyanin

PE

Phycoerythrin

PS

Photosystem

RC

Reaction center

TRFS

Time-resolved fluorescence spectrum (spectra)

Notes

Acknowledgements

This work was supported in part by Special Coordination Funds for promoting Science and Technology, Creation of Innovation Centers for Advanced Interdisciplinary Research Areas (Innovative Bioproduction, Kobe), Japan, and by JSPS KAKENHI (Grant No. 16H06553 to S.A.). We thank Benjamin Knight, MSc., from Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

References

  1. Aizawa K, Shimizu T, Hiyama T, Satoh K, Nakamura Y, Fujita Y (1992) Changes in composition of membrane proteins accompanying the regulation of PSI/PSII stoichiometry observed with Synechocystis PCC 6803. Photosynth Res 32:131–138CrossRefGoogle Scholar
  2. Akimoto S, Yamazaki I, Murakami A, Takaichi S, Mimuro M (2004) Ultrafast excitation relaxation dynamics and energy transfer in the siphonaxanthin-containing green alga Codium fragile. Chem Phys Lett 390:45–49CrossRefGoogle Scholar
  3. Akimoto S, Tomo T, Naitoh Y, Otomo A, Murakami A, Mimuro M (2007) Identification of a new excited state responsible for the in vivo unique absorption band of siphonaxanthin in the green alga Codium fragile. J Phys Chem B 111:9179–9181CrossRefGoogle Scholar
  4. Akimoto S, Yokono M, Hamada F, Teshigahara A, Aikawa S, Kondo A (2012) Adaptation of light-harvesting systems of Arthrospira platensis to light conditions, probed by time-resolved fluorescence spectroscopy. Biochim Biophys Acta Bioenerg 1817:1483–1489CrossRefGoogle Scholar
  5. Akimoto S, Yokono M, Aikawa S, Kondo A (2013) Modification of energy-transfer processes in the cyanobacterium, Arthrospira platensis, to adapt to light conditions, probed by time-resolved fluorescence spectroscopy. Photosynth Res 117:235–243CrossRefGoogle Scholar
  6. Allorent G, Lefebvre-Legendre L, Chappuis R, Kuntz M, Truong TB, Niyogi KK, Ulm R, Goldschmidt-Clermont M (2016) UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 113:14864–14869CrossRefGoogle Scholar
  7. Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180CrossRefGoogle Scholar
  8. Ballottari M, Alcocer MJP, D’Andrea C, Viola D, Ahn TK, Petrozza A, Polli D, Fleming GR, Cerullo G, Bassi R (2014) Regulation of photosystem I light harvesting by zeaxanthin. Proc Natl Acad Sci USA 111:E2431–E2438CrossRefGoogle Scholar
  9. Blankenship RE (2014) Molecular mechanisms of photosynthesis, 2nd edn. Wiley-Blackwell, HobokenGoogle Scholar
  10. Caffarri S, Broess K, Croce R, van Amerongen H (2011) Excitation energy transfer and trapping in higher plant Photosystem II complexes with different antenna sizes. Biophys J 100:2094–2103CrossRefGoogle Scholar
  11. Chen HB, Wu JY, Wang CF, Fu CC, Shieh CJ, Chen CI, Wang CY, Liu YC (2010) Modeling on chlorophyll a and phycocyanin production by Spirulina platensis under various light-emitting diodes. Biochem Eng J 53:52–56CrossRefGoogle Scholar
  12. Chow WS, Melis A, Anderson JM (1990) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc Natl Acad Sci USA 87:7502–7506CrossRefGoogle Scholar
  13. Cunningham FX Jr, Dennenberg RJ, Jursinic PA, Gantt E (1990) Growth under red light enhances photosystem II relative to photosystem I and phycobilisomes in the red alga Porphyridium cruentum. Plant Physiol 93:888–895CrossRefGoogle Scholar
  14. Dinc E, Tian L, Roy LM, Roth R, Goodenough U, Croce R (2016) LHCSR1 induces a fast and reversible pH-dependent fluorescence quenching in LHCII in Chlamydomonas reinhardtii cells. Proc Natl Acad Sci USA 113:7673–7678CrossRefGoogle Scholar
  15. Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32:327–347CrossRefGoogle Scholar
  16. Garnier J, Maroc J, Guyon D (1986) 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. Biochim Biophys Acta Bioenerg 851:395–406CrossRefGoogle Scholar
  17. Ghosh AK, Govindjee (1966) Transfer of the excitation energy in Anacystis nidulans grown to obtain different pigment ratios. Biophys J 6:611–619CrossRefGoogle Scholar
  18. Groot ML, Peterman EJG, van Stokkum IHM, Dekker JP, van Grondelle R (1995) Triplet and fluorescing states of the CP47 antenna complex of photosystem II studied as a function of temperature. Biophys J 68:281–290CrossRefGoogle Scholar
  19. Hamada F, Murakami A, Akimoto S (2017) Adaptation of divinyl chlorophyll a/b-containing cyanobacterium to different light conditions: Three strains of Prochlorococcus marinus. J Phys Chem B 121:9081–9090CrossRefGoogle Scholar
  20. Humbeck K, Hoffmann B, Senger H (1988) Influence of energy flux and quality of light on the molecular organization of the photosynthetic apparatus in Scenedesmus. Planta 173:205–212CrossRefGoogle Scholar
  21. Ichimura T (1971) Sexual cell division and conjugation-papilla formation in sexual reproduction of Closterium strigosum. In: Nishizawa K (ed) Proceedings of the 7th international seaweed symposium, University of Tokyo Press, Tokyo, pp 208–214Google Scholar
  22. Ihalainen JA, van Stokkum IHM, Gibasiewicz K, Germano M, van Grondelle R, Dekker JP (2005) Kinetics of excitation trapping in intact photosystem I of Chlamydomonas reinhardtii and Arabidopsis thaliana. Biochim Biophys Acta Bioenerg 1706:267–275CrossRefGoogle Scholar
  23. Kim E, Akimoto S, Tokutsu R, Yokono M, Minagawa J (2017) Fluorescence lifetime analyses reveal how the high light-responsive protein LHCSR3 transforms PSII light-harvesting complexes into an energy-dissipative state. J Biol Chem 292:18951–18960CrossRefGoogle Scholar
  24. Kowallik W, Schürmann R (1984) Chlorophyll a/Chlorophyll b ratios of Chlorella vulgaris in blue or red light. In: Senger H (ed) Blue light effects in biological systems. Springer, Berlin/Heidelberg, pp 352–358CrossRefGoogle Scholar
  25. Kunugi M, Satoh S, Ihara K, Shibata K, Yamagishi Y, Kogame K, Obokata J, Takabayashi A, Tanaka A (2016) Evolution of green plants accompanied changes in light-harvesting systems. Plant Cell Physiol 57:1231–1243CrossRefGoogle Scholar
  26. Ley AC, Butler WL (1980) Effects of chromatic adaptation on the photochemical apparatus of photosynthesis in Porphyridium cruentum. Plant Physiol 65:714–722CrossRefGoogle Scholar
  27. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292CrossRefGoogle Scholar
  28. Manodori A, Melis A (1986) Cyanobacterial acclimation to PSI or PSII light. Plant Physiol 82:185–189CrossRefGoogle Scholar
  29. Markou G (2014) Effect of various colors of light-emitting diode (LEDs) on the biomass composition of Arthrospira platensis cultivated in semi-continuous mode. Appl Biochem Biotechnol 172:2758–2768CrossRefGoogle Scholar
  30. Melis A, Harvey GW (1981) Regulation of photosystem stoichiometry, chlorophyll a and chlorophyll b content and relation to chloroplast ultrastructure. Biochim Biophys Acta Bioenerg 637:138–145CrossRefGoogle Scholar
  31. Melis A, Murakami A, Nemson JA, Aizawa K, Ohki K, Fujita Y (1996) Chromatic regulation in Chlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosynth Res 47:253–265CrossRefGoogle Scholar
  32. Mimuro M, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T (2007) Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta Bioenerg 1767:327–334CrossRefGoogle Scholar
  33. Mirkovic T, Ostroumov EE, Anna JM, van Grondelle R, Govindjee, Scholes GD (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117:249–293CrossRefGoogle Scholar
  34. Mohamed A, Nagao R, Noguchi T, Fukumura H, Shibata Y (2016) Structure-based modeling of fluorescence kinetics of photosystem II: relation between its dimeric form and photoregulation. J Phys Chem B 120:365–376CrossRefGoogle Scholar
  35. Murakami A (1997) Quantitative analysis of 77K fluorescence emission spectra in Synechocystis sp. PCC 6714 and Chlamydomonas reinhardtii with variable PSI/PSII stoichiometries. Photosynth Res 53:141–148CrossRefGoogle Scholar
  36. Myers J, Graham JR, Wang RT (1980) Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol 66:1144–1149CrossRefGoogle Scholar
  37. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521CrossRefGoogle Scholar
  38. Petroutsos D, Tokutsu R, Maruyama S, Flori S, Greiner A, Magneschi L, Cusant L, Kottke T, Mittag M, Hegemann P, Finazzi G, Minagawa J (2016) A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537:563–566CrossRefGoogle Scholar
  39. Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta Bioenerg 1817:167–181CrossRefGoogle Scholar
  40. Schlodder E, Hussels M, Cetin M, Karapetyan NV, Brecht M (2011) Fluorescence of the various red antenna states in photosystem I complexes from cyanobacteria is affected differently by the redox state of P700. Biochim Biophys Acta Bioenerg 1807:1423–1431CrossRefGoogle Scholar
  41. Shibata Y, Nishi S, Kawakami K, Shen JR, Renger T (2013) Photosystem II does not possess a simple excitation energy funnel: time-resolved fluorescence spectroscopy meets theory. J Am Chem Soc 135:6903–6914CrossRefGoogle Scholar
  42. Sueoka N (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 46:83–91CrossRefGoogle Scholar
  43. Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110:10016–10021CrossRefGoogle Scholar
  44. Ueno Y, Aikawa S, Kondo A, Akimoto S (2015) Light adaptation of the unicellular red alga Cyanidioschyzon merolae, probed by time-resolved fluorescence spectroscopy. Photosynth Res 125:211–218CrossRefGoogle Scholar
  45. Ueno Y, Shimakawa G, Miyake C, Akimoto S (2018) Light-harvesting strategy during CO2-dependent photosynthesis in the green alga Chlamydomonas reinhardtii. J Phys Chem Lett 9:1028–1033CrossRefGoogle Scholar
  46. Wlodarczyk LM, Snellenburg JJ, Ihalainen JA, van Grondelle R, van Stokkum IHM, Dekker JP (2015) Functional rearrangement of the light-harvesting antenna upon state transitions in a green alga. Biophys J 108:261–271CrossRefGoogle Scholar
  47. Wlodarczyk LM, Dinc E, Croce R, Dekker JP (2016) Excitation energy transfer in Chlamydomonas reinhardtii deficient in the PSI core or the PSII core under conditions mimicking state transitions. Biochim Biophys Acta Bioenerg 1857:625–633CrossRefGoogle Scholar
  48. Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015a) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675CrossRefGoogle Scholar
  49. Yokono M, Nagao R, Tomo T, Akimoto S (2015b) Regulation of excitation energy transfer in diatom PSII dimer: how does it change the destination of excitation energy? Biochim Biophys Acta Bioenerg 1847:1274–1282CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Yoshifumi Ueno
    • 1
  • Shimpei Aikawa
    • 2
  • Akihiko Kondo
    • 3
  • Seiji Akimoto
    • 1
    Email author
  1. 1.Graduate School of ScienceKobe UniversityKobeJapan
  2. 2.Japan International Research Center for Agricultural SciencesTsukubaJapan
  3. 3.Graduate School of Science, Technology and InnovationKobe UniversityKobeJapan

Personalised recommendations