SpringerLink
Log in

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

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

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)

References

  • 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 32:131–138

    Article  CAS  PubMed  Google Scholar 

  • 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 390:45–49

    Article  CAS  Google Scholar 

  • 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 111:9179–9181

    Article  CAS  PubMed  Google Scholar 

  • 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 1817:1483–1489

    Article  CAS  Google Scholar 

  • 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 117:235–243

    Article  CAS  PubMed  Google Scholar 

  • 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 113:14864–14869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 84:173–180

    Article  CAS  PubMed  Google Scholar 

  • 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–E2438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blankenship RE (2014) Molecular mechanisms of photosynthesis, 2nd edn. Wiley-Blackwell, Hoboken

    Google Scholar 

  • Caffarri S, Broess K, Croce R, van Amerongen H (2011) Excitation energy transfer and trap** in higher plant Photosystem II complexes with different antenna sizes. Biophys J 100:2094–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:52–56

    Article  CAS  Google Scholar 

  • Chow WS, Melis A, Anderson JM (1990) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc Natl Acad Sci USA 87:7502–7506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 93:888–895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 113:7673–7678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32:327–347

    Article  CAS  Google Scholar 

  • 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 851:395–406

    Article  CAS  Google Scholar 

  • Ghosh AK, Govindjee (1966) Transfer of the excitation energy in Anacystis nidulans grown to obtain different pigment ratios. Biophys J 6:611–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:281–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 121:9081–9090

    Article  CAS  PubMed  Google Scholar 

  • 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 173:205–212

    Article  CAS  PubMed  Google Scholar 

  • 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 208–214

  • Ihalainen JA, van Stokkum IHM, Gibasiewicz K, Germano M, van Grondelle R, Dekker JP (2005) Kinetics of excitation trap** in intact photosystem I of Chlamydomonas reinhardtii and Arabidopsis thaliana. Biochim Biophys Acta Bioenerg 1706:267–275

    Article  CAS  Google Scholar 

  • 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 292:18951–18960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 352–358

    Chapter  Google Scholar 

  • 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 57:1231–1243

    Article  CAS  PubMed  Google Scholar 

  • Ley AC, Butler WL (1980) Effects of chromatic adaptation on the photochemical apparatus of photosynthesis in Porphyridium cruentum. Plant Physiol 65:714–722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 428:287–292

    Article  CAS  PubMed  Google Scholar 

  • Manodori A, Melis A (1986) Cyanobacterial acclimation to PSI or PSII light. Plant Physiol 82:185–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 172:2758–2768

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Harvey GW (1981) Regulation of photosystem stoichiometry, chlorophyll a and chlorophyll b content and relation to chloroplast ultrastructure. Biochim Biophys Acta Bioenerg 637:138–145

    Article  CAS  Google Scholar 

  • 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 47:253–265

    Article  CAS  PubMed  Google Scholar 

  • 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 1767:327–334

    Article  CAS  Google Scholar 

  • 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 117:249–293

    Article  CAS  PubMed  Google Scholar 

  • 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 120:365–376

    Article  CAS  PubMed  Google Scholar 

  • 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 53:141–148

    Article  CAS  Google Scholar 

  • Myers J, Graham JR, Wang RT (1980) Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol 66:1144–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 462:518–521

    Article  CAS  PubMed  Google Scholar 

  • 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 537:563–566

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta Bioenerg 1817:167–181

    Article  CAS  Google Scholar 

  • 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 1807:1423–1431

    Article  CAS  Google Scholar 

  • 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 135:6903–6914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sueoka N (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 46:83–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110:10016–10021

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 125:211–218

    Article  CAS  PubMed  Google Scholar 

  • 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 9:1028–1033

    Article  CAS  PubMed  Google Scholar 

  • 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 108:261–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1857:625–633

    Article  CAS  Google Scholar 

  • Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015a) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675

    Article  CAS  PubMed  Google Scholar 

  • 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 1847:1274–1282

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Graduate School of Science, Kobe University, Kobe, 657-8501, Japan

    Yoshifumi Ueno & Seiji Akimoto

  2. Japan International Research Center for Agricultural Sciences, Tsukuba, 305-8686, Japan

    Shimpei Aikawa

  3. Graduate School of Science, Technology and Innovation, Kobe University, Kobe, 657-8501, Japan

    Akihiko Kondo

Authors
  1. Yoshifumi Ueno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shimpei Aikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akihiko Kondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seiji Akimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seiji Akimoto.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ueno, Y., Aikawa, S., Kondo, A. et al. Adaptation of light-harvesting functions of unicellular green algae to different light qualities. Photosynth Res 139, 145–154 (2019). https://doi.org/10.1007/s11120-018-0523-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-018-0523-y

Keywords

Search

Navigation