Spectral heterogeneity and carotenoid-to-bacteriochlorophyll energy transfer in LH2 light-harvesting complexes from Allochromatium vinosum
详细信息    查看全文
  • 作者:Nikki M. Magdaong ; Amy M. LaFountain ; Kirsty Hacking…
  • 关键词:Carotenoids ; Energy transfer ; Light ; harvesting ; Photosynthesis ; Pigment ; protein complex ; Ultrafast transient absorption spectroscopy
  • 刊名:Photosynthesis Research
  • 出版年:2016
  • 出版时间:February 2016
  • 年:2016
  • 卷:127
  • 期:2
  • 页码:171-187
  • 全文大小:2,304 KB
  • 参考文献:Akahane J, Rondonuwu FS, Fiedor L, Watanabe Y, Koyama Y (2004) Dependence of singlet-energy transfer on the conjugation length of carotenoids reconstituted into the LH1 complex from Rhodospirillum rubrum G9. Chem Phys Lett 393:184–191CrossRef
    Angerhofer A, Bornhäuser F, Gall A, Cogdell RJ (1995) Optical and optically detected magnetic resonance investigation on purple photosynthetic bacterial antenna complexes. Chem Phys 194:259–274CrossRef
    Britton G (1995) UV/Visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1B., Spectroscopy. Birkhäuser Verlag, Basel, pp 13–62
    Carey A-M, Hacking K, Picken N, Honkanen S, Kelly S, Niedzwiedzki DM, Blankenship RE, Shimizu Y, Wang-Otomo Z-Y, Cogdell RJ (2014) Characterization of the LH2 spectral variants produced by the photosynthetic purple sulphur bacterium Allochromatium vinosum. BBA Bioenerg 1837:1849–1860CrossRef
    Cerullo G, Polli D, Lanzani G, De Silvestri S, Hashimoto H, Cogdell RJ (2002) Photosynthetic light harvesting by carotenoids: detection of an intermediate excited state. Science 298:2395–2398PubMed CrossRef
    Cleary L, Chen H, Chuang C, Silbey RJ, Cao J (2013) Optimal fold symmetry of LH2 rings on a photosynthetic membrane. Proc Natl Acad Sci USA 110:8537–8542PubMed PubMedCentral CrossRef
    Cogdell RJ, Scheer H (1985) Circular dichroism of light-harvesting complexes from purple photosynthetic bacteria. Photochem Photobiol 42:669–678CrossRef
    Cogdell RJ, Thornber JP (1980) Light-harvesting pigment-protein complexes of purple photosynthetic bacteria. FEBS Lett 122:1–8CrossRef
    Cogdell RJ, Zuber H, Thornber JP, Drews G, Gingras G, Niederman RA, Parson WW, Feher G (1985) Recommendations for the naming of photochemical reaction centers and light-harvesting pigment-protein complexes from purple photosynthetic bacteria. Biochim Biophys Acta 806:185–186CrossRef
    Cogdell RJ, Isaacs NW, Howard TD, McLuskey K, Fraser NJ, Prince SM (1999) How photosynthetic bacteria harvest solar energy. J Bacteriol 181:3869–3879PubMed PubMedCentral
    Cogdell RJ, Howard TD, Isaacs NW, McLuskey K, Gardiner AT (2002) Structural factors which control the position of the Qy absorption band of bacteriochlorophyll a in purple bacterial antenna complexes. Photosynth Res 74:135–141PubMed CrossRef
    Cogdell RJ, Gall A, Köhler J (2006) The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q Rev Biophys 39:227–324PubMed CrossRef
    Cong H, Niedzwiedzki D, Gibson GN, LaFountain AM, Kelsh RM, Gardiner AT, Cogdell RJ, Frank HA (2008) Ultrafast time-resolved carotenoid-to-bacteriochlorophyll energy transfer in LH2 complexes from photosynthetic bacteria. J Phys Chem B 112:10689–10703PubMed PubMedCentral CrossRef
    Farhoosh R, Chynwat V, Gebhard R, Lugtenburg J, Frank HA (1994) Triplet energy transfer between bacteriochlorophyll and carotenoids in B850 light-harvesting complexes of Rhodobacter sphaeroides R-26.1. Photosynth Res 42:157–166PubMed CrossRef
    Feng J, Wang Q, Wu Y-S, Ai X-C, Zhang X-J, Huang Y-G, Zhang X-K, Zhang J-P (2004) Triplet excitation transfer between carotenoids in the LH2 complex from photosynthetic bacterium Rhodopseudomonas palustris. Photosynth Res 82:83–94PubMed CrossRef
    Frank HA, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63:257–264PubMed CrossRef
    Fuciman M, Enriquez MM, Polivka 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 116:3834–3849PubMed CrossRef
    Gall A, Gardiner AT, Cogdell RJ, Robert B (2006) Carotenoid stoichiometry in the LH2 crystal: no spectral evidence for the presence of the second molecule in the alpha/beta-apoprotein dimer. FEBS Lett 580:3841–3844PubMed CrossRef
    Garcia A, Vernon LP, Mollenhauer H (1966) Properties of Chromatium subchromatophore particles obtained by treatment with Triton X-100. Biochemistry 5:2399–2407PubMed CrossRef
    Gardiner AT, Takaichi S, Cogdell RJ (1992) The effect of changes in light intensity and temperature on the peripheral antenna of Rhodopseudomonas acidophila. Biochem Soc Trans 21:6SCrossRef
    Gardiner AT, Cogdell RJ, Takaichi S (1993) The effect of growth conditions on the light-harvesting apparatus in Rhodopseudomonas acidophila. Photosynth Res 38:159–167PubMed CrossRef
    Gradinaru CC, Kennis JTM, Papagiannakis E, van Stokkum IHM, Cogdell RJ, Fleming GR, Niederman RA, van Grondelle R (2001) An unusual pathway of excitation energy deactivation in carotenoids: singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna. Proc Natl Acad Sci USA 98:2364–2369PubMed PubMedCentral CrossRef
    Hawthornthwaite AM, Cogdell RJ (1991) Bacteriochlorophyll-binding proteins. In: Scheer H (ed) Chlorophylls. CRC Press, Boca Raton, pp 493–528
    Hayashi H, Morita S (1980) Near-infrared absorption spectra of light harvesting bateriochlorophyll protein complexes from Chromatium vinosum. J Biochem 88:1251–1258PubMed
    Hayashi H, Nozawa T, Hatano M, Morita S (1981) Circular dichroism of Bacteriochlorophyll a in light harvesting bacteriochlorophyll protein complexes from Chromatium vinosum. J Biochem 89:1853–1861PubMed
    Heinemeyer E-A, Schmidt K (1983) Changes in carotenoid biosynthesis caused by variations of growth conditions in cultures of Rhodopseudomonas acidophila strain 7050. Arch Microbiol 134:217–221CrossRef
    Holzwarth AR (1996) Data analysis of time-resolved measurements. In: Amesz J, Hoff AJ (eds) Biophysical techniques in photosynthesis, vol 3. Kluwer Academiv Publishers, Dordrecht, pp 75–91CrossRef
    Ilagan RP, Christensen RL, Chapp TW, Gibson GN, Pascher T, Polivka T, Frank HA (2005) Femtosecond time-resolved absorption spectroscopy of astaxanthin in solution and in α-crustacyanin. J Phys Chem A 109:3120–3127PubMed CrossRef
    Kakitani Y, Akahane J, Ishii H, Sogabe H, Nagae H, Koyama Y (2007) Conjugation-length dependence of the T1 lifetimes of carotenoids free in solution and incorporated into the LH2, LH1, RC and RC-LH1 complexes: possible mechanisms of triplet-energy dissipation. Biochemistry 46:2181–2197PubMed CrossRef
    Kennis JTM, Streltsov AM, Vulto SIE, Aartsma TJ, Nozawa T, Amesz J (1997) Femtosecond dynamics in isolated LH2 complexes of various species of purple bacteria. J Phys Chem B 101:7827–7834CrossRef
    Kereïche S, Bourinet L, Keegstra W, Arteni AA, Verbavatz J-M, Boekema EJ, Robert B, Gall A (2008) The peripheral light-harvesting complexes from purple sulfur bacteria have different ‘ring’ sizes. FEBS Lett 582:3650–3656PubMed CrossRef
    Koepke J, Hu X, Schulten K, Michel H (1996) The crystal structure of the light harvesting complex II (B800-850) from Rhodospirillum molischianum. Structure 4:581–597PubMed CrossRef
    Kosumi D, Fujiwara M, Fujii R, Cogdell RJ, Hashimoto H, Yoshizawa M (2009) The dependence of the ultrafast relaxation kinetics of the S2 and S1 states in β-carotene homologs and lycopene on conjugation length studied by femtosecond time-resolved absorption and Kerr-gate fluorescence spectroscopies. J Chem Phys 130:214506–214513PubMed CrossRef
    Koyama Y, Rondonuwu FS, Fujii R, Watanabe Y (2004) Light-harvesting function of carotenoids in photo-synthesis: the roles of the newly found 11B u – state. Biopolymers 74:2–18PubMed CrossRef
    Kramer H, Amesz J (1996) Antenna organization in the purple sulfur bacteria Chromatium tepidum and Chromatium vinosum. Photosynth Res 49:237–244PubMed CrossRef
    Krueger BP, Scholes GD, Fleming GR (1998) Calculation of couplings and energy-transfer pathways between the pigments of LH2 by the ab initio transition density cube method. J Phys Chem B 102:5378–5386CrossRef
    Law CJ, Roszak AW, Southall J, Gardiner AT, Isaacs NW, Cogdell RJ (2004) The structure and function of bacterial light-harvesting complexes (Review). Mol Membr Biol 21:183–191PubMed CrossRef
    Löhner A, Carey A-M, Hacking K, Picken N, Kelly S, Cogdell RJ, Köhler J (2015) The origin of the split B800 absorption peak in the LH2 complexes from Allochromatium vinosum. Photosynth Res 123:23–31PubMed CrossRef
    Macpherson AN, Arellano JB, Fraser NJ, Cogdell RJ, Gillbro T (2001) Efficient energy transfer from the carotenoid S2 state in a photosynthetic light-harvesting complex. Biophys J 80:923–930PubMed PubMedCentral CrossRef
    Magdaong NM, Lafountain AM, Greco JA, Gardiner AT, Carey A-M, Cogdell RJ, Gibson GN, Birge RR, Frank HA (2014) High efficiency light harvesting by carotenoids in the LH2 complex from photosynthetic bacteria: unique adaptation to growth under low-light conditions. J Phys Chem B 118:11172–11189PubMed PubMedCentral CrossRef
    Maiuri M, Polli D, Brida D, Lüer L, LaFountain AM, Fuciman M, Cogdell RJ, Frank HA, Cerullo G (2012) Solvent-dependent activation of intermediate excited states in the energy relaxation pathways of spheroidene. Phys Chem Chem Phys 14:6312–6319PubMed CrossRef
    McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ, Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–521CrossRef
    McLuskey K, Prince SM, Cogdell RJ, Isaacs NW (2001) The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. Biochemistry 40:8783–8789PubMed CrossRef
    Monger TG, Cogdell RJ, Parson WW (1976) Triplet states of bacteriochlorophyll and carotenoids in chromatophores of photosynthetic bacteria. Biochim Biophys Acta 449:136–153PubMed CrossRef
    Niedzwiedzki D, Koscielecki JF, Cong H, Sullivan JO, Gibson GN, Birge RR, Frank HA (2007) Ultrafast dynamics and excited state spectra of open-chain carotenoids at room and low temperatures. J Phys Chem B 111:5984–5998PubMed CrossRef
    Niedzwiedzki DM, Fuciman M, Kobayashi M, Frank HA, Blankenship RE (2011a) Ultrafast time-resolved spectroscopy of the light-harvesting complex 2 (LH2) from the photosynthetic bacterium Thermochromatium tepidum. Photosynth Res 110:49–60PubMed CrossRef
    Niedzwiedzki DM, Kobayashi M, Blankenship RE (2011b) Triplet excited state spectra and dynamics of carotenoids from the thermophilic purple photosynthetic bacterium Thermochromatium tepidum. Photosynth Res 107:177–186PubMed CrossRef
    Niedzwiedzki DM, Bina D, Picken N, Honkanen S, Blankenship RE, Holten D, Cogdell RJ (2012) Spectroscopic studies of two spectral variants of light-harvesting complex 2 (LH2) from the photosynthetic purple sulfur bacterium Allochromatium vinosum. BBA Bioenerg 1817:1576–1587CrossRef
    Noguchi T, Hayashi H, Tasumi T (1990) Factors controlling the efficiency of energy transfer from carotenoids to bacteriochlorophyll in purple photosynthetic bacteria. Biochim Biophys Acta 1017:280–290CrossRef
    Okamoto H, Ogura M, Nakabayashi T, Tasumi M (1998) Sub-picosecond excited-state dynamics of carotenoid (spirilloxanthin) in the light-harvesting systems of Chromatium vinosum. Relaxation procces from the optically allowed S2 state. Chem Phys 236:309–318CrossRef
    Ostroumov EE, Mulvaney RM, Cogdell RJ, Scholes GD (2013) Broadband 2D electronic spectroscopy reveals a carotenoid dark state in purple bacteria. Science 340:52–56PubMed CrossRef
    Papiz MZ, Prince SM, Howard T, Cogdell RJ, Isaacs NW (2003) The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 100 K: new structural features and functionally relevant motions. J Mol Biol 326:1523–1538PubMed CrossRef
    Prince SM, Papiz MZ, Freer AA, McDermott G, Hawthornthwaite-Lawless AM, Cogdell RJ, Isaacs NW (1997) Apoprotein structure in the LH2 complex from Rhodopseudomonas acidophila strain 10050: modular assembly and protein pigment interactions. J Mol Biol 268:412–423PubMed CrossRef
    Rondonuwu FS, Taguchi T, Fujii R, Yokoyama K, Koyama Y, Watanabe Y (2004a) The energies and kinetics of triplet carotenoids in the LH2 antenna complexes as determined by phosphorescence spectroscopy. Chem Phys Lett 384:364–371CrossRef
    Rondonuwu FS, Yokoyama K, Fujii R, Koyama Y, Cogdell RJ, Watanabe Y (2004b) The role of the 11B u − state in carotenoid-to-bacteriochlorophyll singlet-energy transfer in the LH2 antenna complexes from Rhodobacter sphaeroides G1C, Rhodobacter sphaeroides 2.4.1, Rhodospirillum molischianum and Rhodopseudomonas acidophila. Chem Phys Lett 390:314–322CrossRef
    Schiedt K, Liaaen-Jensen S (1995) Isolation and analysis. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1A. Birkhäuser Verlag, Basel
    Schubert A, Stenstam A, Beenken WJD, Herek JL, Cogdell R, Pullerits T, Sundström V (2004) In vitro self-assembly of the light harvesting pigment-protein LH2 revealed by ultrafast spectroscopy and electron microscopy. Biophys J 86:2363–2373PubMed PubMedCentral CrossRef
    Shreve AP, Trautman JK, Frank HA, Owens TG, Van Beek JB, Albrecht AC (1992) On subpicosecond excitation energy transfer in light harvesting complexes (LHC): the B800-850 LHC of Rhodobacter sphaeroides 2.4.1. J Lumin 53:179–186CrossRef
    Takaichi S, Gardiner AT, Cogdell RJ (1992) Pigment composition of light-harvesting pigment-protein complexes from Rhodopseudomonas acidophila: Effect of light intensity. Res photosynth, In: 9th proceedings of international congress photosynthesis, vol 1. pp 149–152
    Thornber JR, Trosper TL, Strouse CE (1978) Bacteriochlorophyll in vivo: relationships of spectral forms to specific membrane components. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, London, pp 133–160
    Trautman JK, Shreve AP, Violette CA, Frank HA, Owens TG, Albrecht AC (1990) Femtosecond dynamics of energy transfer in B800-850 light-harvesting complexes of Rhodobacter sphaeroides. Proc Natl Acad Sci USA 87:215–219PubMed PubMedCentral CrossRef
    van Stokkum IHM, Larsen DS, van Grondelle R (2004) Global and target analysis of time-resolved spectra. Biochim Biophys Acta 1657:82–104PubMed CrossRef
    Wassink EC, Katz E, Dorrestein R (1939) Infrared absorption spectra of various strains of purple bacteria. Enzymologia 7:113–129
    Weissgerber T, Zigann R, Bruce D, Y-j Chang, Detter JC, Han C, Hauser L, Jeffries CD, Land M, Munk C, Tapia R, Dahl C (2011) Complete genome sequence of Allochromatium vinosum DSM 180. Stand Genomic Sci 5:311–330PubMed PubMedCentral CrossRef
    Zuber H, Brunisholz RA (1993) In: Scheer H (ed) The Chlorophylls. CRC, Boca Raton, p 627
    Zuber H, Cogdell RJ (1995) Structure and organization of purple bacterial antenna complexes. In: Blankenship RE, Madigan MT, Bauer CE (eds) Advances in photosynthesis, vol 2., Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 315–348
  • 作者单位:Nikki M. Magdaong (1)
    Amy M. LaFountain (1)
    Kirsty Hacking (2)
    Dariusz M. Niedzwiedzki (3)
    George N. Gibson (4)
    Richard J. Cogdell (2)
    Harry A. Frank (1)

    1. Department of Chemistry, University of Connecticut, 55 North Eagleville Road, Storrs, CT, 06269-3060, USA
    2. Institute of Molecular Cell and Systems Biology, University of Glasgow, Glasgow, Scotland, UK
    3. Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO, USA
    4. Department of Physics, University of Connecticut, 2152 Hillside Road, Storrs, CT, 06269-3046, USA
  • 刊物类别:Biomedical and Life Sciences
  • 刊物主题:Life Sciences
    Plant Physiology
  • 出版者:Springer Netherlands
  • ISSN:1573-5079
文摘
Photosynthetic organisms produce a vast array of spectral forms of antenna pigment-protein complexes to harvest solar energy and also to adapt to growth under the variable environmental conditions of light intensity, temperature, and nutrient availability. This behavior is exemplified by Allochromatium (Alc.) vinosum, a photosynthetic purple sulfur bacterium that produces different types of LH2 light-harvesting complexes in response to variations in growth conditions. In the present work, three different spectral forms of LH2 from Alc. vinosum, B800-820, B800-840, and B800-850, were isolated, purified, and examined using steady-state absorption and fluorescence spectroscopy, and ultrafast time-resolved absorption spectroscopy. The pigment composition of the LH2 complexes was analyzed by high-performance liquid chromatography, and all were found to contain five carotenoids: lycopene, anhydrorhodovibrin, spirilloxanthin, rhodopin, and rhodovibrin. Spectral reconstructions of the absorption and fluorescence excitation spectra based on the pigment composition revealed significantly more spectral heterogeneity in these systems compared to LH2 complexes isolated from other species of purple bacteria. The data also revealed the individual carotenoid-to-bacteriochlorophyll energy transfer efficiencies which were correlated with the kinetic data from the ultrafast transient absorption spectroscopic experiments. This series of LH2 complexes allows a systematic exploration of the factors that determine the spectral properties of the bound pigments and control the rate and efficiency of carotenoid-to-bacteriochlorophyll energy transfer. Keywords Carotenoids Energy transfer Light-harvesting Photosynthesis Pigment-protein complex Ultrafast transient absorption spectroscopy

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700