Skip to main content
SpringerLink
Log in

Singlet oxygen formation and chlorophyll a triplet excited state deactivation in the cytochrome b 6 f complex from Bryopsis corticulans

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

We have attempted to investigate the correlation between the detergent-perturbed structural integrity of the Cyt b 6 f complex from the marine green alga Bryopsis corticulans and its photo-protective properties, for which the nonionic detergents n-octyl-β-d-glucopyranoside (β-OG) and n-dodecyl-β-d-maltoside (β-DM), respectively, were used for the preparation of Cyt b 6 f, and the singlet oxygen (1O2*) production as well as the triplet excited-state chlorophyll a (3Chl a*) formation and deactivation were examined by spectroscopic means. Near-infrared luminescence of 1O2 * (~1,270 nm) on photo-irradiation was detected for the β-OG preparation where the complex is mainly in oligomeric state, but not for the β-DM one in which the complex exists in dimeric form. Under anaerobic condition, photo-excitation of Chl a in the β-DM preparation generated 3Chl a* with a lower quantum yield of ΦT ~ 0.02 and a longer lifetime of ~600 μs with respect to those as in the case of β-OG preparation, ΦT ~ 0.12 and 200–300 μs. These results prove that the enzymatically active and intact Cyt b 6 f complex on photo-excitation tends to produce little 3Chl a* or 1O2 *, which implies that the pigment–protein assembly of Cyt b 6 f complex per se is crucial for photo-protection.

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

Similar content being viewed by others

Abbreviations

Car:

Carotenoid

3Chl a*:

Triplet excited state chlorophyll a

Cyt b 6 f :

Cytochrome b 6 f complex

β-DM:

n-Dodecyl-β-d-maltoside

EET:

Excitation energy transfer

1O2 * :

Singlet oxygen

β-OG:

n-Octyl-β-d-glucopyranoside

SDS:

Sodium dodecyl sulfate

ΦT :

Quantum yield of triplet excited state chlorophyll a

References

  • Anderson JM (1992) Cytochrome b 6 f complex: dynamic molecular organization, function and acclimation. Photosynth Res 34:341–357. doi:10.1007/BF00029810

    Article  CAS  Google Scholar 

  • Boronowsky U, Wenk SO, Schneider D, Jäger C, Rögner M (2001) Isolation of membrane protein subunits in their native states: evidence for selective binding of chlorophyll and carotenoid to the b 6 subunit of the cytochrome b 6 f complex. Biochim Biophys Acta 1506:55–66. doi:10.1016/S0005-2728(01)00184-0

    Article  PubMed  CAS  Google Scholar 

  • Bowers PG, Porter G (1967) Quantum yields of triplet formation in solutions of chlorophyll. Proc R Soc A 296:435–441. doi:10.1098/rspa.1967.0036

    Article  Google Scholar 

  • Breyton C, Tribet C, Olive J, Dubacq JP, Popot JL (1997) Dimer to monomer conversion of the cytochrome b 6 f complex. J Biol Chem 272:21892–21900. doi:10.1074/jbc.272.35.21892

    Article  PubMed  CAS  Google Scholar 

  • Chen XB, Zhao XH, Zhu Y, Gong YD, Li LB, Zhang JP, Kuang TY (2006) Hydrogen peroxide-induced chlorophyll a bleaching in the cytochrome b 6 f complex: a simple and effective assay for stability of the complex in detergent solutions. Photosynth Res 90:205–214. doi:10.1007/s11120-006-9118-0

    Article  PubMed  CAS  Google Scholar 

  • Cogdell RJ, Hipkins MF, MacDonald W, Truscott TG (1981) Energy transfer between the carotenoid and the bacteriochlorophyll within the B800–850 light-harvesting pigment–protein complex of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 634:191–202. doi:10.1016/0005-2728(81)90138-9

    Article  PubMed  CAS  Google Scholar 

  • Cramer WA, Soriano GM, Ponomarev M, Huang D, Zhang H, Martinez SE, Smith JL (1996) Some new structural aspects and old controversies concerning the cytochrome b 6 f complex of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47:477–508. doi:10.1146/annurev.arplant.47.1.477

    Article  PubMed  CAS  Google Scholar 

  • Cramer WA, Zhang HM, Yan JS, Kurisu G, Smith JL (2004) Evolution of photosynthesis: time-independent structure of the cytochrome b 6 f complex. Biochemistry 43:5921–5929. doi:10.1021/bi049444o

    Article  PubMed  CAS  Google Scholar 

  • Cramer WA, Yan JS, Zhang HM, Kurisu G, Smith JL (2005) Structure of the cytochrome b 6 f complex: new prosthetic groups, Q-space, and the ‘hors d’oeuvres hypothesis’ for assembly of the complex. Photosynth Res 85:133–144. doi:10.1007/s11120-004-2149-5

    Article  PubMed  CAS  Google Scholar 

  • Crystall B, Booth PJ, Klug DR, Barber J, Porter G (1989) Resolution of a long lived fluorescence component from D1/D2/cytochrome b-559 reaction centers. FEBS Lett 249:75–78. doi:10.1016/0014-5793(89)80019-5

    Article  CAS  Google Scholar 

  • Dashdorj N, Zhang HM, Kim H, Yan JS, Cramer WA, Savikhin (2005) The single chlorophyll a molecule in the cytochrome b 6 f complex: unusual optical properties protect the complex against singlet oxygen. Biophys J 88:4178–4187. doi:10.1529/biophysj.104.058693

    Article  PubMed  CAS  Google Scholar 

  • Dědic R, Svoboda A, Pšeněík J, Lupínková L, Komenda J, Hála J (2003) Time and spectral resolved phosphorescence of singlet oxygen and pigments in photosystem II particles. J Lumin 102:313–317. doi:10.1016/S0022-2313(02)00524-0

    Article  Google Scholar 

  • Frank HA, Cogdell RJ (1993) Photochemistry and functions of carotenoids in photosynthesis. In: Young A, Britton G (eds) Carotenoids in photosynthesis. Chapman and Hall, London, pp 252–326

  • Hope AB (1993) The chloroplast cytochrome bf complex: a critical focus on function. Biochim Biophys Acta 1143:1–22. doi:10.1016/0005-2728(93)90210-7

    Article  PubMed  CAS  Google Scholar 

  • Horigome D, Satoh H, Itoh N, Mitsunaga K, Oonishi I, Nakagawa A, Uchida A (2007) Structural mechanism and photoprotective function of water-soluble chlorophyll-binding protein. J Biol Chem 282:6525–6531. doi:10.1074/jbc.M609458200

    Article  PubMed  CAS  Google Scholar 

  • Kim H, Dashdorj N, Zhang HM, Yan JS, Cramer WA, Savikhin S (2005) An anomalous distance dependence of intra-protein chlorophyll-carotenoid triplet energy transfer. Biophys J 89:L28–L30. doi:10.1529/biophysj.105.069609

    Article  PubMed  CAS  Google Scholar 

  • Kingma H, van Grondelle R, Duysens LNM (1985) Magnetic-field effects in photosynthetic bacteria. II. Formation of triplet states in the reaction center and the antenna of Rhodospirillum rubrum and Rhodopseudomonas sphaeroides. Biochim Biophys Acta 808:383–399. doi:10.1016/0005-2728(85)90147-1

    Article  CAS  Google Scholar 

  • Krinsky NI (1979) Carotenoid protection against oxidation. Pure Appl Chem 51:649–660. doi:10.1351/pac197951030649

    Article  CAS  Google Scholar 

  • Kurisu G, Zhang HM, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014. doi:10.1126/science.1090165

    Article  PubMed  CAS  Google Scholar 

  • Lavalette AL, Finazzi G, Zito F (2008) b 6 f-Associated chlorophyll: structural and dynamic contribution to the different cytochrome functions. Biochemistry 47:5259–5265. doi:10.1021/bi800179b

    Article  Google Scholar 

  • Li YF, Zhou W, Blankenship RE, Allen JP (1997) Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. J Mol Biol 271:456–471. doi:10.1006/jmbi.1997.1189

    Article  PubMed  CAS  Google Scholar 

  • Li BX, Zuo P, Chen XB, Li LB, Zhang JP, Kuang TY (2006) Study on energy transfer between carotenoid and chlorophyll a in cytochrome b 6 f complex from Bryopsis corticulans. Photosynth Res 88:43–50. doi:10.1007/s11120-005-9020-1

    Article  PubMed  CAS  Google Scholar 

  • Peterman EJG, Wenk SO, Pullerits T, Pålsson LO, van Grondelle R, Dekker JP, Rögner M, van Amerongen H (1998) Fluorescence and absorption spectroscopy of the weakly fluorescent chlorophyll a in cytochrome b 6 f of Synechocystis PCC6803. Biophys J 75:389–398. doi:10.1016/S0006-3495(98)77523-X

    Article  PubMed  CAS  Google Scholar 

  • Pierre Y, Breyton C, Lemoine Y, Robert B, Vernotte C, Popot JL (1997) On the presence and role of a molecule of chlorophyll a in the cytochrome b 6 f complex. J Biol Chem 272:21901–21908. doi:10.1074/jbc.272.35.21901

    Article  PubMed  CAS  Google Scholar 

  • Schödel R, Irrgang KD, Voigt J, Renger G (1998) Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys J 75:3143–3153. doi:10.1016/S0006-3495(98)77756-2

    Article  PubMed  Google Scholar 

  • Seely GR, Connolly JS (1986) Fluorescence of photosynthetic pigments in vitro. In: Govindjee JA, Fork DC (eds) Light emission by plants and bacteria. Academic Press, New York, pp 99–133

  • Siefermann-Harms D (1987) The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Physiol Plant 69:561–568. doi:10.1111/j.1399-3054.1987.tb09240.x

    Article  CAS  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426:413–418. doi:10.1038/nature02155

    Article  PubMed  CAS  Google Scholar 

  • Truong T, Bersohn R, Brumer P, Luk CK, Tao T (1967) Effect of pH on the phosphorescence of tryptophan, tyrosine and proteins. J Biol Chem 242:2979–2985

    PubMed  CAS  Google Scholar 

  • van Stokkum IM, Larsen DS, van Grondelle R (2004) Global and target analysis of time-resolved spectra. Biochim Biophys Acta 1657:82–104. doi:10.1016/j.bbabio.2004.04.011

    Article  PubMed  Google Scholar 

  • Yan JS, Liu YL, Mao DZ, Li LB, Kuang TY (2001) The presence of 9-cis-β-carotene in cytochrome b 6 f complex from spinach. Biochim Biophys Acta 1506:182–188. doi:10.1016/S0005-2728(01)00212-2

    Article  PubMed  CAS  Google Scholar 

  • Yan JS, Dashdorj N, Baniulis D, Yamashita E, Savikhin S, Cramer WA (2008) On the structural role of the aromatic residue environment of the chlorophyll a in the cytochrome b 6 f complex. Biochemistry 47:3654–3661. doi:10.1021/bi702299b

    Article  PubMed  CAS  Google Scholar 

  • Zhang HM, Huang DR, Cramer WA (1999) Stoichiometrically bound β-carotene in the cytochrome b 6 f complex of oxygenic photosynthesis protects against oxygen damage. J Biol Chem 274:1581–1587. doi:10.1074/jbc.274.3.1581

    Article  PubMed  CAS  Google Scholar 

  • Zuo P, Li BX, Zhao XH, Wu YS, Ai XC, Zhang JP, Li LB, Kuang TY (2006) Ultrafast carotenoid-to-chlorophyll singlet energy transfer in the cytochrome b 6 f complex from Bryopsis corticulans. Biophys J 90:4145–4154. doi:10.1529/biophysj.105.076612

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful for the assistance in DLS experiments by Dr. Yi-Wei Liu at the Department of Biological Science and Biotechnology, Tsinghua University. This work has been jointly supported by the National Basic Research Program of China (2009CB220008), the Natural Science Foundation of China (20673144 and 20703067) and the Natural Science Foundation of Hebei Province (C2008000684).

Author information

Authors and Affiliations

  1. Beijing National Laboratory for Molecular Science (BNLMS), State Key Laboratory for Structural Chemistry of Unstable and Stable Species, Institute of Chemistry, Chinese Academy of Sciences, Beijing, 100080, China

    Fei Ma

  2. Department of Chemistry, Renmin University of China, 59 Zhongguancun Street, Beijing, 100872, China

    Fei Ma, Peng Wang & Jian-Ping Zhang

  3. Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing, 100093, China

    Xiao-Bo Chen, Min Sang, Liang-Bi Li & Ting-Yun Kuang

Authors
  1. Fei Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-Bo Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Sang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian-Ping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Liang-Bi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ting-Yun Kuang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jian-Ping Zhang or Liang-Bi Li.

Additional information

F. Ma and X.-B. Chen contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ma, F., Chen, XB., Sang, M. et al. Singlet oxygen formation and chlorophyll a triplet excited state deactivation in the cytochrome b 6 f complex from Bryopsis corticulans . Photosynth Res 100, 19–28 (2009). https://doi.org/10.1007/s11120-009-9418-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-009-9418-2

Keywords

Search

Navigation