Skip to main content
SpringerLink
Log in

Excitation energy transfer in the far-red absorbing violaxanthin/vaucheriaxanthin chlorophyll a complex from the eustigmatophyte alga FP5

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

Abstract

This work highlights spectroscopic investigations on a new representative of photosynthetic antenna complexes in the LHC family, a putative violaxanthin/vaucheriaxanthin chlorophyll a (VCP) antenna complex from a freshwater Eustigmatophyte alga FP5. A representative VCP-like complex, named as VCP-B3 was studied with both static and time-resolved spectroscopies with the aim of obtaining a deeper understanding of excitation energy migration within the pigment array of the complex. Compared to other VCP representatives, the absorption spectrum of the VCP-B3 is strongly altered in the range of the chlorophyll a Qy band, and is substantially red-shifted with the longest wavelength absorption band at 707 nm at 77 K. VCP-B3 shows a moderate xanthophyll-to-chlorophyll a efficiency of excitation energy transfer in the 50–60% range, 20–30% lower from comparable VCP complexes from other organisms. Transient absorption studies accompanied by detailed data fitting and simulations support the idea that the xanthophylls that occupy the central part of the complex, complementary to luteins in the LHCII, are violaxanthins. Target analysis suggests that the primary route of xanthophyll-to-chlorophyll a energy transfer occurs via the xanthophyll S1 state.

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

Access this article

Log in via an institution

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

2-MTHF:

2-Methyl-tetrahydrofuran

ACN:

Acetonitrile

Chl:

Chlorophyll

DADS:

Decay-associated difference spectra

EADS:

Evolution-associated difference spectra

EET:

Efficiency of excitation energy transfer

ESA:

Excited state absorption

ET:

Energy transfer

Exc:

Excitation

FWHM:

Full width at half maximum

HPLC:

High-performance liquid chromatography

ISC:

Inter-system crossing

LED:

Light-emitting diode

MeOH:

Methanol

NIR:

Near infrared

PMMA:

Poly(methyl methacrylate)

PS:

Photosystem

RC:

Reaction center

RT:

Room temperature

SADS:

Species-associated difference spectra

TA:

Transient absorption

THF:

Tetrahydrofuran

T-S:

Triplet-minus-singlet

UV–Vis:

Ultraviolet–visible

Vauch:

Vaucheriaxanthin

VCP-(B3):

Violaxanthin/vaucheriaxanthin chlorophyll a-(band 3)

Viol:

Violaxanthin

Xanth:

Xanthophyll

References

  • Angerhofer A, Bornhauser F, Gall A, Cogdell RJ (1995) Optical and optically detected magnetic-resonance investigation on purple photosynthetic bacterial antenna complexes. Chem Phys 194:259–274

    Article  CAS  Google Scholar 

  • Ballottari M, Girardon J, Dall’Osto L, Bassi R (2012) Evolution and functional properties of Photosystem II light harvesting complexes in eukaryotes. Biochim Biophys Acta Bioenerg 1817:143–157

    Article  CAS  Google Scholar 

  • Basso S, Simionato D, Gerotto C, Segalla A, Giacometti GM, Morosinotto T (2014) Characterization of the photosynthetic apparatus of the Eustigmatophycean Nannochloropsis gaditana: evidence of convergent evolution in the supramolecular organization of photosystem I. Biochim Biophys Acta Bioenerg 1837:306–314

    Article  CAS  Google Scholar 

  • Bina D, Gardian Z, Herbstova M, Kotabova E, Konik P, Litvin R, Prasil O, Tichy J, Vacha F (2014) Novel type of red-shifted chlorophyll a antenna complex from Chromera velia: II. Biochemistry and spectroscopy. Biochim Biophys Acta Bioenerg 1837:802–810

    Article  CAS  Google Scholar 

  • Bina D, Durchan M, Kuznetsova V, Vacha F, Litvin R, Polivka T (2019) Energy transfer dynamics in a red-shifted violaxanthin-chlorophyll a light-harvesting complex. Biochim Biophys Acta Bioenerg 1860:111–120

    Article  CAS  PubMed  Google Scholar 

  • Blankenship RE (2014) Molecular mechanisms of photosynthesis. Wiley, Oxford

    Google Scholar 

  • Bowers PG, Porter G (1967) Quantum yields of triplet formation in solutions of chlorophyll. Proc R Soc A 296:435–441

    Article  Google Scholar 

  • Brown JS (1987) Functional organization of chlorophyll-a and carotenoids in the alga, Nannochloropsis salina. Plant Physiol 83:434–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carbonera D, Agostini A, Di Valentin M, Gerotto C, Basso S, Giacometti GM, Morosinotto T (2014) Photoprotective sites in the violaxanthin-chlorophyll a binding protein (VCP) from Nannochloropsis gaditana. Biochim Biophys Acta Bioenerg 1837:1235–1246

    Article  CAS  Google Scholar 

  • Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Li YQ, Birch D, Willows RD (2012) A cyanobacterium that contains chlorophyll f—a red-absorbing photopigment. Febs Lett 586:3249–3254

    Article  CAS  PubMed  Google Scholar 

  • Cong H, Niedzwiedzki DM, Gibson GN, Frank HA (2008) Ultrafast time-resolved spectroscopy of xanthophylls at low temperature. J Phys Chem B 112:3558–3567

    Article  CAS  PubMed  Google Scholar 

  • Dall’Ostro L, Bassi R, Ruban AV (2014) Photoprotective mechanisms: carotenoids. In: Theg SM, Wollman FA (eds) Plastid biology, advances in plant biology, vol 5. Springer, New York, pp 393–435

    Chapter  Google Scholar 

  • Eliáš M, Amaral R, Fawley KP, Fawley MW, Němcová Y, Neustupa J, Přibyl P, Santos LMA, Ševčíková T (2007) Eustigmatophyceae. In: Archibald JM, Simpson AGB, Slamovits CH (ed) Handbook of the protists. Springer, Berlin, pp. 367–406

    Google Scholar 

  • Emerson R, Lewis CM (1943) The dependence of the quantum yield of chlorella photosynthesis on wave length of light. Am J Bot 30:165–178

    Article  CAS  Google Scholar 

  • Fork DC, Larkum AWD (1989) Light harvesting in the green alga Ostreobium sp., a coral symbiont adapted to extreme shade. Mar Biol 103:381–385

    Article  Google Scholar 

  • Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR (1994) Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth Res 41:389–395

    Article  CAS  PubMed  Google Scholar 

  • Fuciman M, Enriquez MM, Polívka T, Dall’Osto L, Bassi R, Frank HA (2012) Role of xanthophylls in light harvesting in green plants: a spectroscopic investigation of mutant LHCII and Lhcb pigment-protein complexes. J Phys Chem B 116:3834–3849

    Article  CAS  PubMed  Google Scholar 

  • Guglielmi G, Lavaud J, Rousseau B, Etienne AL, Houmard J, Ruban AV (2005) The light-harvesting antenna of the diatom Phaeodactylum tricornutum—evidence for a diadinoxanthin-binding subcomplex. Febs J 272:4339–4348

    Article  CAS  PubMed  Google Scholar 

  • Gundermann K, Buchel C (2014) Structure and functional heterogeneity of fucoxanthin-chlorophyll proteins in diatoms. In: Hohmann-Marriott MF (ed) The structural basis of biological energy generation, vol. advances in photosynthesis and respiration, Dordrecht: Springer, pp. 21–37

    Chapter  Google Scholar 

  • Herek JL, Polivka T, Pullerits T, Fowler GJS, Hunter CN, Sundstrom V (1998) Ultrafast carotenoid band shifts probe structure and dynamics in photosynthetic antenna complexes. Biochemistry 37:7057–7061

    Article  CAS  PubMed  Google Scholar 

  • Herek JL, Wendling M, He Z, Polivka T, Garcia-Asua G, Cogdell RJ, Hunter CN, van Grondelle R, Sundstrom V, Pullerits T (2004) Ultrafast carotenoid band shifts: experiment and theory. J Phys Chem B 108:10398–10403

    Article  CAS  Google Scholar 

  • Kesan G, Litvin R, Bina D, Durchan M, Slouf V, Polivka T (2016) Efficient light-harvesting using non-carbonyl carotenoids: energy transfer dynamics in the VCP complex from Nannochloropsis oceanica. Biochim Biophys Acta Bioenerg 1857:370–379

    Article  CAS  Google Scholar 

  • Kotabova E, Jaresova J, Kana R, Sobotka R, Bina D, Prasil O (2014) Novel type of red-shifted chlorophyll alpha antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochim Biophys Acta Bioenerg 1837:734–743

    Article  CAS  Google Scholar 

  • Krasnovsky AA, Cheng P, Blankenship RE, Moore TA, Gust D (1993) The photophysics of monomeric bacteriochlorophylls c and bacteriochlorophylls d and their derivatives—properties of the triplet ttate and singlet oxygen photogeneration and quenching. Photochem Photobiol 57:324–330

    Article  CAS  PubMed  Google Scholar 

  • Litvin R, Bina D, Herbstova M, Gardian Z (2016) Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica. Photosynth Res 130:137–150

    Article  CAS  PubMed  Google Scholar 

  • Liu ZF, Yan HC, Wang KB, Kuang TY, Zhang JP, Gui LL, An XM, Chang WR (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292

    Article  CAS  PubMed  Google Scholar 

  • Majumder ELW, Wolf BM, Liu HJ, Berg RH, Timlin JA, Chen M, Blankenship RE (2017) Subcellular pigment distribution is altered under far-red light acclimation in cyanobacteria that contain chlorophyll f. Photosynth Res 134:183–192

    Article  CAS  PubMed  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402–402

    Article  CAS  Google Scholar 

  • Morosinotto T, Breton J, Bassi R, Croce R (2003) The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J Biol Chem 278:49223–49229

    Article  CAS  PubMed  Google Scholar 

  • Morosinotto T, Mozzo M, Bassi R, Croce R (2005) Pigment-pigment interactions in Lhca4 antenna complex of higher plants photosystem I. J Biol Chem 280:20612–20619

    Article  CAS  PubMed  Google Scholar 

  • Niedzwiedzki DM, Blankenship RE (2010) Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls. Photosynth Res 106:227–238

    Article  CAS  PubMed  Google Scholar 

  • Niedzwiedzki DM, Sullivan JO, Polivka T, Birge RR, Frank HA (2006) Femtosecond time-resolved transient absorption spectroscopy of xanthophylls. J Phys Chem B 110:22872–22885

    Article  CAS  PubMed  Google Scholar 

  • Niedzwiedzki DM, Enriquez MM, LaFountain AM, Frank HA (2010) Ultrafast time-resolved absorption spectroscopy of geometric isomers of xanthophylls. Chem Phys 373:80–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niedzwiedzki DM, Jiang J, Lo CS, Blankenship RE (2013) Low-temperature spectroscopic properties of the peridinin—chlorophyll a—protein (PCP) complex from the coral symbiotic dinoflagellate Symbiodinium. J Phys Chem B 117:11091–11099

    Article  CAS  PubMed  Google Scholar 

  • Niedzwiedzki DM, Tronina T, Liu H, Staleva H, Komenda J, Sobotka R, Blankenship RE, Polivka T (2016) Carotenoid-induced non-photochemical quenching in the cyanobacterial chlorophyll synthase-HliC/D complex. BBA Bioeneg 1857:1430–1439

    Article  CAS  Google Scholar 

  • Peterman EJG, Gradinaru CC, Calkoen F, Borst JC, vanGrondelle R, vanAmerongen H (1997) Xanthophylls in light-harvesting complex II of higher plants: Light harvesting and triplet quenching. Biochemistry 36:12208–12215

    Article  CAS  PubMed  Google Scholar 

  • Pettai H, Oja V, Freiberg A, Laisk A (2005a) The long-wavelength limit of plant photosynthesis. Febs Lett 579:4017–4019

    Article  CAS  PubMed  Google Scholar 

  • Pettai H, Oja V, Freiberg A, Laisk A (2005b) Photosynthetic activity of far-red light in green plants. Biochim Biophys Acta Bioenerg 1708:311–321

    Article  CAS  Google Scholar 

  • Pignon CP, Jaiswal D, McGrath JM, Long SP (2017) Loss of photosynthetic efficiency in the shade. An Achilles heel for the dense modern stands of our most productive C-4 crops? J Exp Bot 68:335–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polivka T, Sundstrom V (2004) Ultrafast dynamics of carotenoid excited states-from solution to natural and artificial systems. Chem Rev 104:2021–2071

    Article  CAS  PubMed  Google Scholar 

  • Polivka T, Herek JL, Zigmantas D, Akerlund HE, Sundstrom V (1999) Direct observation of the (forbidden) S1 state in carotenoids. Proc Natl Acad Sci USA 96:4914–4917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polivka T, Zigmantas D, Sundstrom V, Formaggio E, Cinque G, Bassi R (2002) Carotenoid S1 state in a recombinant light-harvesting complex of photosystem II. Biochemistry 41:439–450

    Article  CAS  PubMed  Google Scholar 

  • Polívka T, Frank HA (2010) Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc Chem Res 43:1125–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polívka T, Sundström V (2009) Dark excited states of carotenoids: consensus and controversy. Chem Phys Lett 477:1–11

    Article  CAS  Google Scholar 

  • Rivadossi A, Zucchelli G, Garlaschi FM, Jennings RC (1999) The importance of PSI chlorophyll red forms in light-harvesting by leaves. Photosynth Res 60:209–215

    Article  CAS  Google Scholar 

  • Rochaix JD (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65 65:287–309

    Article  CAS  PubMed  Google Scholar 

  • Schulte T, Niedzwiedzki DM, Birge RR, Hiller RG, Polivka T, Hofmann E, Frank HA (2009) Identification of a single peridinin sensing Chl-a excitation in reconstituted PCP by crystallography and spectroscopy. Proc Natl Acad Sci USA 106:20764–20769

    Article  PubMed  PubMed Central  Google Scholar 

  • Standfuss R, van Scheltinga ACT, Lamborghini M, Kuhlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. Embo J 24:919–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukenik A, Livne A, Apt KE, Grossman AR (2000) Characterization of a gene encoding the light-harvesting violaxanthin-chlorophyll protein of Nannochloropsis sp (Eustigmatophyceae). J Phycol 36:563–570

    Article  CAS  PubMed  Google Scholar 

  • van Stokkum IHM, Larsen DS, van Grondelle R (2004) Global and target analysis of time-resolved spectra. Biochim Biophys Acta Bioenerg 1657:82–104

    Article  CAS  Google Scholar 

  • van der Vos R, Carbonera D, Hoff AJ (1991) Microwave and optical spectroscopy of carotenoid triplets in light-harvesting complex LHCII of spinach by absorbance-detected magnetic resonance. Appl Magn Reson 2:179–202

    Article  Google Scholar 

  • Wientjes E, Croce R (2011) The light-harvesting complexes of higher-plant Photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem J 433:477–485

    Article  CAS  PubMed  Google Scholar 

  • Wientjes E, Roest G, Croce R (2012) From red to blue to far-red in Lhca4: how does the protein modulate the spectral properties of the pigments? Biochim Biophys Acta Bioenerg 1817:711–717

    Article  CAS  Google Scholar 

  • Wolf BM, Niedzwiedzki DM, Magdaong NCM, Roth R, Goodenough U, Blankenship RE (2018) Characterization of a newly isolated freshwater Eustigmatophyte alga capable of utilizing far-red light as its sole light source. Photosynth Res 135:177–189

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Steady-state and time-resolved spectroscopic studies were performed in the Ultrafast Laser Facility of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center (EFRC) funded by Grant #DE-SC 0001035. Benjamin M. Wolf was supported by the William H. Danforth Plant Science Fellowship.

Author information

Authors and Affiliations

  1. Department of Energy, Environmental & Chemical Engineering and Center for Solar Energy and Energy Storage, Washington University in St Louis, St. Louis, MO, 63130, USA

    Dariusz M. Niedzwiedzki

  2. Photosynthetic Antenna Research Center, Washington University in St Louis, St. Louis, MO, 63130, USA

    Dariusz M. Niedzwiedzki

  3. Department of Biology, Washington University in St Louis, St. Louis, MO, 63130, USA

    Benjamin M. Wolf & Robert E. Blankenship

  4. Department of Chemistry, Washington University in St Louis, St. Louis, MO, 63130, USA

    Robert E. Blankenship

Authors
  1. Dariusz M. Niedzwiedzki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benjamin M. Wolf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert E. Blankenship
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dariusz M. Niedzwiedzki.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 856 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Niedzwiedzki, D.M., Wolf, B.M. & Blankenship, R.E. Excitation energy transfer in the far-red absorbing violaxanthin/vaucheriaxanthin chlorophyll a complex from the eustigmatophyte alga FP5. Photosynth Res 140, 337–354 (2019). https://doi.org/10.1007/s11120-019-00615-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-019-00615-y

Keywords

Search

Navigation