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Pigment structure in the violaxanthin–chlorophyll-a-binding protein VCP

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Abstract

Resonance Raman spectroscopy was used to evaluate pigment-binding site properties in the violaxanthin–chlorophyll-a-binding protein (VCP) from Nannochloropsis oceanica. The pigments bound to this antenna protein are chlorophyll-a, violaxanthin, and vaucheriaxanthin. The molecular structures of bound Chl-a molecules are discussed with respect to those of the plant antenna proteins LHCII and CP29, the crystal structures of which are known. We show that three populations of carotenoid molecules are bound by VCP, each of which is in an all-trans configuration. We assign the lower-energy absorption transition of each of these as follows. One violaxanthin population absorbs at 485 nm, while the second population is red-shifted and absorbs at 503 nm. The vaucheriaxanthin population absorbs at 525 nm, a position red-shifted by 2138 cm−1 as compared to isolated vaucheriaxanthin in n-hexane. The red-shifted violaxanthin is slightly less planar than the blue-absorbing one, as observed for the two central luteins in LHCII, and we suggest that these violaxanthins occupy the two equivalent binding sites in VCP at the centre of the cross-brace. The presence of a highly red-shifted vaucheriaxanthin in VCP is reminiscent of the situation of FCP, in which (even more) highly red-shifted populations of fucoxanthin are present. Tuning carotenoids to absorb in the green-yellow region of the visible spectrum appears to be a common evolutionary response to competition with other photosynthetic species in the aquatic environment.

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References

  • Andreeva A, Apostolova I, Velitchkova M (2011) Temperature dependence of resonance Raman spectra of carotenoids. Spectrochim Acta Part A 78(4):1261–1265

    Article  CAS  Google Scholar 

  • Apt KE, Clendennen SK, Powers DA, Grossman AR (1995) The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera. Mol Gen Genet 246(4):455–464

    Article  CAS  PubMed  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 1837(2):306–314

    Article  CAS  PubMed  Google Scholar 

  • Britton G, Liaaen-Jensen S, Pfander H (2008) Carotenoids, vol 4. Verlag, Basel

    Book  Google Scholar 

  • Busch A, Hippler M (2011) The structure and function of eukaryotic photosystem I. Biochim Biophys Acta 1807(8):864–877

    Article  CAS  PubMed  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 1837(8):1235–1246

    Article  CAS  PubMed  Google Scholar 

  • Dokter AM, van Hemert MC, In ‘t Velt CM, van der Hoef K, Lugtenburg J, Frank HA, Groenen EJJ (2002) Resonance Raman spectrum of all-trans-spheroidene. DFT analysis and isotope labeling. J Phys Chem A 106(41):9463–9469

    Article  CAS  Google Scholar 

  • Dolganov NA, Bhaya D, Grossman AR (1995) Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc Natl Acad Sci USA 92(2):636–640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelken J, Brinkmann H, Adamska I (2010) Taxonomic distribution and origins of the extended lhc (light-harvesting complex) antenna protein superfamily. BMC Evol Biol 10(1):1–15

    Article  Google Scholar 

  • Feiler U, Mattioli TA, Katheder I, Scheer H, Lutz M, Robert B (1994) Effects of vinyl substitutions on resonance Raman spectra of (bacterio)chlorophylls. J Raman Spectrosc 25(5):365–370

    Article  CAS  Google Scholar 

  • Fujiwara M, Tasumi M (1986) Metal-sensitive bands in the Raman and infrared spectra of intact and metal-substituted chlorophyll a. J Phys Chem 90(22):5646–5650

    Article  CAS  Google Scholar 

  • Gall A, Pascal AA, Robert B (2015) Vibrational techniques applied to photosynthesis: resonance Raman and fluorescence line-narrowing. Biochim Biophys Acta 1847(1):12–18

    Article  CAS  PubMed  Google Scholar 

  • Hofmann E, Wrench PM, Sharples FP, Hiller RG, Welte W, Diederichs K (1996) Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science 272(5269):1788–1791

    Article  CAS  PubMed  Google Scholar 

  • Keşan G, Litvín R, Bína D, Durchan M, Šlouf V, Polívka T (2016) Efficient light-harvesting using non-carbonyl carotenoids: energy transfer dynamics in the vcp complex from Nannochloropsis oceanica. Biochim Biophys Acta 1857(4):370–379

    Article  PubMed  Google Scholar 

  • Kish E, Wang K, Llansola-Portoles MJ, Ilioaia C, Pascal AA, Robert B, Yang C (2016) Probing the pigment binding sites in LHCII with resonance Raman spectroscopy: the effect of mutations at S123. Biochim Biophys Acta 1857(9):1490–1496

    Article  CAS  PubMed  Google Scholar 

  • Koyama Y, Kito M, Takii T, Saiki K, Tsukida K, Yamashita J (1982) Configuration of the carotenoid in the reaction centers of photosynthetic bacteria. Comparison of the resonance Raman spectrum of the reaction center of Rhodopseudomonas sphaeroides G1C with those of cis–trans isomers of β-carotene. Biochim Biophys Acta 680(2):109–118

    Article  CAS  Google Scholar 

  • Koyama Y, Takii T, Saiki K, Tsukida K (1983) Configuration of the carotenoid in the reaction centers of photosynthetic bacteria. 2. Comparison of the resonance Raman lines of the reaction centers with those of the 14 different cis–trans isomers of β-carotene. Photobiochem Photobiophys 5:139–150

    CAS  Google Scholar 

  • Koyama Y, Takatsuka I, Nakata M, Tasumi M (1988) Raman and infrared spectra of the all-trans, 7-cis, 9-cis, 13-cis and 15-cis isomers of β-carotene: key bands distinguishing stretched or terminal-bent configurations form central-bent configurations. J Raman Spectrosc 19(1):37–49

    Article  CAS  Google Scholar 

  • Koziol AG, Borza T, Ishida K-I, Keeling P, Lee RW, Durnford DG (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143(4):1802–1816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lapouge K, Näveke A, Sturgis JN, Hartwich G, Renaud D, Simonin I, Lutz M, Scheer H, Robert B (1998) Non-bonding molecular factors influencing the stretching wavenumbers of the conjugated carbonyl groups of bacteriochlorophyll a. J Raman Spectrosc 29(10–11):977–981

    Article  CAS  Google Scholar 

  • Litvín R, Bína D, Herbstová M, Gardian Z (2016) Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica. Photosynth Res 130(1):137–150

    Article  PubMed  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 a resolution. Nature 428(6980):287–292

    Article  CAS  PubMed  Google Scholar 

  • Llansola-Portoles MJ, Uragami C, Pascal AA, Bina D, Litvin R, Robert B (2016) Pigment structure in the FCP-like light-harvesting complex from Chromera velia. Biochim Biophys Acta 1857(11):1759–1765

    Article  CAS  PubMed  Google Scholar 

  • Llansola-Portoles MJ, Sobotka R, Kish E, Shukla MK, Pascal AA, Polívka T, Robert B (2017) Twisting a β-carotene, an adaptive trick from nature for dissipating energy during photoprotection. J Biol Chem 292(4):1396–1403

    Article  CAS  PubMed  Google Scholar 

  • Lutz M (1977) Antenna chlorophyll in photosynthetic membranes. A study by resonance Raman spectroscopy. Biochim Biophys Acta 460(3):408–430

    Article  CAS  PubMed  Google Scholar 

  • Lutz M, Mäntele W (1991). In: Scheer H (ed) The chlorophylls. CRC Press Inc., Boca Raton, pp 855–902

    Google Scholar 

  • Lutz M, Szponarski W, Berger G, Robert B, Neumann J-M (1987) The stereoisomerization of bacterial, reaction-center-bound carotenoids revisited: an electronic absorption, resonance Raman and 1H-NMR study. Biochem Biophys Acta 894:423–433

    CAS  Google Scholar 

  • Macernis M, Sulskus J, Malickaja S, Robert B, Valkunas L (2014) Resonance Raman spectra and electronic transitions in carotenoids: a density functional theory study. J Phys Chem A 118(10):1817–1825

    Article  CAS  PubMed  Google Scholar 

  • Macernis M, Galzerano D, Sulskus J, Kish E, Kim Y-H, Koo S, Valkunas L, Robert B (2015) Resonance Raman spectra of carotenoid molecules: influence of methyl substitutions. J Phys Chem A 119(1):56–66

    Article  CAS  PubMed  Google Scholar 

  • Mendes-Pinto MM, Galzerano D, Telfer A, Pascal AA, Robert B, Ilioaia C (2013a) Mechanisms underlying carotenoid absorption in oxygenic photosynthetic proteins. J Biol Chem 288(26):18758–18765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendes-Pinto MM, Sansiaume E, Hashimoto H, Pascal AA, Gall A, Robert B (2013b) Electronic absorption and ground state structure of carotenoid molecules. J Phys Chem B 117(38):11015–11021

    Article  CAS  PubMed  Google Scholar 

  • Näveke A, Lapouge K, Sturgis JN, Hartwich G, Simonin I, Scheer H, Robert B (1997) Resonance Raman spectroscopy of metal-substituted bacteriochlorophylls: characterization of Raman bands sensitive to bacteriochlorin conformation. J Raman Spectrosc 28(8):599–604

    Article  Google Scholar 

  • Neilson JD, Durnford D (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106(1–2):57–71

    Article  CAS  PubMed  Google Scholar 

  • Pan X, Li M, Wan T, Wang L, Jia C, Hou Z, Zhao X, Zhang J, Chang W (2011) Structural insights into energy regulation of light-harvesting complex cp29 from spinach. Nat Struct Mol Biol 18(3):309–315

    Article  CAS  PubMed  Google Scholar 

  • Pascal AA, Caron L, Rousseau B, Lapouge K, Duval JC, Robert B (1998) Resonance Raman spectroscopy of a light-harvesting protein from the brown alga Laminaria saccharina. Biochemistry 37(8):2450–2457

    Article  CAS  PubMed  Google Scholar 

  • Pascal AA, Wacker U, Irrgang K-D, Horton P, Renger G, Robert B (2000) Pigment binding site properties of two photosystem II antenna proteins: a resonance Raman investigation. J Biol Chem 275(29):22031–22036

    Article  CAS  PubMed  Google Scholar 

  • Paulsen H, Rümler U, Rüdiger W (1990) Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed in Escherichia coli. Planta 181(2):204–211

    Article  CAS  PubMed  Google Scholar 

  • Pendon ZD, Sullivan JO, van der Hoef I, Lugtenburg J, Cua A, Bocian DF, Birge RR, Frank HA (2005) Stereoisomers of carotenoids: spectroscopic properties of locked and unlocked cis-isomers of spheroidene. Photosynth Res 86(1):5–24

    Article  CAS  PubMed  Google Scholar 

  • Premvardhan L, Bordes L, Beer A, Büchel C, Robert B (2009) Carotenoid structures and environments in trimeric and oligomeric fucoxanthin chlorophyll a/c2 proteins from resonance Raman spectroscopy. J Phys Chem B 113(37):12565–12574

    Article  CAS  PubMed  Google Scholar 

  • Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropsis gaditana. Nat Commun 3:686

    Article  PubMed  PubMed Central  Google Scholar 

  • Reimers JR, Cai Z-L, Kobayashi R, Rätsep M, Freiberg A, Krausz E (2013) Assignment of the Q-bands of the chlorophylls: coherence loss via Qx–Qy mixing. Sci Rep 3:2761

    Article  PubMed  PubMed Central  Google Scholar 

  • Rimai L, Heyde ME, Gill D (1973) Vibrational spectra of some carotenoids and related linear polyenes. Raman spectroscopic study. J Am Chem Soc 95(14):4493–4501

    Article  CAS  PubMed  Google Scholar 

  • Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102(1):100–112

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Horton P, Robert B (1995) Resonance Raman spectroscopy of the photosystem II light-harvesting complex of green plants: a comparison of trimeric and aggregated states. Biochemistry 34(7):2333–2337

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Pascal AA, Robert B (2000) Xanthophylls of the major photosynthetic light-harvesting complex of plants: identification, conformation and dynamics. FEBS Lett 477(3):181–185

    Article  CAS  PubMed  Google Scholar 

  • Saito S, Tasumi M (1983) Normal-coordinate analysis of β-carotene isomers and assignments of the Raman and infrared bands. J Raman Spectrosc 14(5):310–321

    Article  CAS  Google Scholar 

  • Sforza E, Simionato D, Giacometti GM, Bertucco A, Morosinotto T (2012) Adjusted light and dark cycles can optimize photosynthetic efficiency in algae growing in photobioreactors. PLoS ONE 7(6):e38975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simionato D, Sforza E, Carpinelli EC, Bertucco A, Giacometti GM, Morosinotto T (2011) Acclimation of Nannochloropsis gaditana to different illumination regimes: effects on lipids accumulation. Bioresour Technol 102(10):6026–6032

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the ERC funding agency (PHOTPROT project) and The French Infrastructure for Integrated Structural Biology (FRISBI). The research in the Czech Republic was supported by the Czech Science Foundation Grant 14-01377P and by institutional funding RVO:60077344.

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Authors and Affiliations

  1. Institute for Integrative Biology of the Cell (I2BC), IBITECS, CEA, CNRS, Université Paris-Saclay, 91198, Gif-sur-Yvette Cedex, France

    Manuel J. Llansola-Portoles, Cristian Ilioaia, Andrew A. Pascal & Bruno Robert

  2. Institute of Plant Molecular Biology, Biology Centre CAS, Branisovska 31, 370 05, Ceske Budejovice, Czech Republic

    Radek Litvin & David Bina

  3. Faculty of Science, University of South Bohemia, Branisovska 1760, 370 05, Ceske Budejovice, Czech Republic

    Radek Litvin & David Bina

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  1. Manuel J. Llansola-Portoles
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  2. Radek Litvin
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  3. Cristian Ilioaia
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Correspondence to Manuel J. Llansola-Portoles.

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Llansola-Portoles, M.J., Litvin, R., Ilioaia, C. et al. Pigment structure in the violaxanthin–chlorophyll-a-binding protein VCP. Photosynth Res 134, 51–58 (2017). https://doi.org/10.1007/s11120-017-0407-6

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  • DOI: https://doi.org/10.1007/s11120-017-0407-6

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