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

  • Dariusz M. NiedzwiedzkiEmail author
  • Benjamin M. Wolf
  • Robert E. Blankenship
Original Article
  • 54 Downloads

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.

Keywords

Transient absorption Vaucheriaxanthin Light-harvesting complex Photosynthesis Chlorophyll a Violaxanthin 

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

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2019_615_MOESM1_ESM.docx (857 kb)
Supplementary material 1 (DOCX 856 KB)

References

  1. Angerhofer A, Bornhauser F, Gall A, Cogdell RJ (1995) Optical and optically detected magnetic-resonance investigation on purple photosynthetic bacterial antenna complexes. Chem Phys 194:259–274CrossRefGoogle Scholar
  2. 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 1817:143–157CrossRefGoogle Scholar
  3. 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 1837:306–314CrossRefGoogle Scholar
  4. 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 1837:802–810CrossRefGoogle Scholar
  5. 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 1860:111–120CrossRefGoogle Scholar
  6. Blankenship RE (2014) Molecular mechanisms of photosynthesis. Wiley, OxfordGoogle Scholar
  7. Bowers PG, Porter G (1967) Quantum yields of triplet formation in solutions of chlorophyll. Proc R Soc A 296:435–441Google Scholar
  8. Brown JS (1987) Functional organization of chlorophyll-a and carotenoids in the alga, Nannochloropsis salina. Plant Physiol 83:434–437CrossRefGoogle Scholar
  9. 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 1837:1235–1246CrossRefGoogle Scholar
  10. Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431CrossRefGoogle Scholar
  11. Chen M, Li YQ, Birch D, Willows RD (2012) A cyanobacterium that contains chlorophyll f—a red-absorbing photopigment. Febs Lett 586:3249–3254CrossRefGoogle Scholar
  12. Cong H, Niedzwiedzki DM, Gibson GN, Frank HA (2008) Ultrafast time-resolved spectroscopy of xanthophylls at low temperature. J Phys Chem B 112:3558–3567CrossRefGoogle Scholar
  13. 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 393–435Google Scholar
  14. 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. 367–406Google Scholar
  15. Emerson R, Lewis CM (1943) The dependence of the quantum yield of chlorella photosynthesis on wave length of light. Am J Bot 30:165–178CrossRefGoogle Scholar
  16. Fork DC, Larkum AWD (1989) Light harvesting in the green alga Ostreobium sp., a coral symbiont adapted to extreme shade. Mar Biol 103:381–385CrossRefGoogle Scholar
  17. 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 41:389–395CrossRefGoogle Scholar
  18. 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 116:3834–3849CrossRefGoogle Scholar
  19. 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 272:4339–4348CrossRefGoogle Scholar
  20. 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. 21–37CrossRefGoogle Scholar
  21. 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 37:7057–7061CrossRefGoogle Scholar
  22. 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 108:10398–10403CrossRefGoogle Scholar
  23. 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 1857:370–379CrossRefGoogle Scholar
  24. 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 1837:734–743CrossRefGoogle Scholar
  25. 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 57:324–330CrossRefGoogle Scholar
  26. Litvin R, Bina D, Herbstova M, Gardian Z (2016) Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica. Photosynth Res 130:137–150CrossRefGoogle Scholar
  27. 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 428:287–292CrossRefGoogle Scholar
  28. 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 134:183–192CrossRefGoogle Scholar
  29. Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402–402CrossRefGoogle Scholar
  30. 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 278:49223–49229CrossRefGoogle Scholar
  31. Morosinotto T, Mozzo M, Bassi R, Croce R (2005) Pigment-pigment interactions in Lhca4 antenna complex of higher plants photosystem I. J Biol Chem 280:20612–20619CrossRefGoogle Scholar
  32. Niedzwiedzki DM, Blankenship RE (2010) Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls. Photosynth Res 106:227–238CrossRefGoogle Scholar
  33. Niedzwiedzki DM, Sullivan JO, Polivka T, Birge RR, Frank HA (2006) Femtosecond time-resolved transient absorption spectroscopy of xanthophylls. J Phys Chem B 110:22872–22885CrossRefGoogle Scholar
  34. Niedzwiedzki DM, Enriquez MM, LaFountain AM, Frank HA (2010) Ultrafast time-resolved absorption spectroscopy of geometric isomers of xanthophylls. Chem Phys 373:80–89CrossRefGoogle Scholar
  35. 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 117:11091–11099CrossRefGoogle Scholar
  36. 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 1857:1430–1439CrossRefGoogle Scholar
  37. 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 36:12208–12215CrossRefGoogle Scholar
  38. Pettai H, Oja V, Freiberg A, Laisk A (2005a) The long-wavelength limit of plant photosynthesis. Febs Lett 579:4017–4019CrossRefGoogle Scholar
  39. Pettai H, Oja V, Freiberg A, Laisk A (2005b) Photosynthetic activity of far-red light in green plants. Biochim Biophys Acta Bioenerg 1708:311–321CrossRefGoogle Scholar
  40. 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 68:335–345CrossRefGoogle Scholar
  41. Polivka T, Sundstrom V (2004) Ultrafast dynamics of carotenoid excited states-from solution to natural and artificial systems. Chem Rev 104:2021–2071CrossRefGoogle Scholar
  42. 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 96:4914–4917CrossRefGoogle Scholar
  43. 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 41:439–450CrossRefGoogle Scholar
  44. Polívka T, Frank HA (2010) Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc Chem Res 43:1125–1134CrossRefGoogle Scholar
  45. Polívka T, Sundström V (2009) Dark excited states of carotenoids: consensus and controversy. Chem Phys Lett 477:1–11CrossRefGoogle Scholar
  46. Rivadossi A, Zucchelli G, Garlaschi FM, Jennings RC (1999) The importance of PSI chlorophyll red forms in light-harvesting by leaves. Photosynth Res 60:209–215CrossRefGoogle Scholar
  47. Rochaix JD (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65 65:287–309CrossRefGoogle Scholar
  48. 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 106:20764–20769CrossRefGoogle Scholar
  49. 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 24:919–928CrossRefGoogle Scholar
  50. 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 36:563–570CrossRefGoogle Scholar
  51. van Stokkum IHM, Larsen DS, van Grondelle R (2004) Global and target analysis of time-resolved spectra. Biochim Biophys Acta Bioenerg 1657:82–104CrossRefGoogle Scholar
  52. 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 2:179–202CrossRefGoogle Scholar
  53. 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 433:477–485CrossRefGoogle Scholar
  54. 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 1817:711–717CrossRefGoogle Scholar
  55. 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 135:177–189CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Energy, Environmental & Chemical Engineering and Center for Solar Energy and Energy StorageWashington University in St LouisSt. LouisUSA
  2. 2.Photosynthetic Antenna Research CenterWashington University in St LouisSt. LouisUSA
  3. 3.Department of BiologyWashington University in St LouisSt. LouisUSA
  4. 4.Department of ChemistryWashington University in St LouisSt. LouisUSA

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