Skip to main content
SpringerLink
Log in

Molecular Crowding: A Way to Deal with Crowding in Photosynthetic Membranes

  • Chapter
Book cover Bioengineering in Cell and Tissue Research

Abstract

In the last decades our view of biological systems has changed dramatically. One reason is an increasing awareness of molecular crowding in virtually all living cells. An example for a crowded system is photosynthesis. At the first glance, for many years the riddle of photosynthesis and the involved flow of electrons seemed to be solved since long ago. Nearly all involved proteins were known as well as most mechanisms of electron transfer within them. Between the photosynthetic proteins electrons were assumed to be transported via free diffusion of electron carriers. However, the diffusion of these carriers within the photosynthetic membrane may be strongly influenced by molecular crowding, which might nearly completely restrict it. Nevertheless, effects of molecular crowding are only sparsely investigated in the available literature although they show again that “the whole is more than the sum of its parts” (Aristotle). Even if all single components of a process are known, this does not mean that their interplay is really understood. Apart from diffusion many other important parameters determining the metabolism in a cell or within a membrane, like e. g. reaction equilibria, aggregation, self organisation or reaction rates, are also influenced by molecular crowding. Hence, molecular crowding is an important but underestimated phenomenon that is worth to be investigated in more detail already because of its omnipresence.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albertsson P-Å (1995) The structure and function of the chloroplast photosynthetic membrane – a model for the domain organization. Photosynth Res 46:141–149

    Article  Google Scholar 

  2. Albertsson P-Å (2000) The domain structure and function of the thylakoid membrane. Recent Res Devel Bioener 1:143–171

    Google Scholar 

  3. Albertsson P-Å (2001) A quantitative model of the domain structure of the photosynthetitc membrane. Trends in Plant Science 6:349–354

    Article  Google Scholar 

  4. Almeida PFF, Vaz WLC (1995) Handbook of Biological Physics, chapter 6. Lateral Diffusion in Membranes, Elsevier Science BV, Amsterdam, pp 305–357

    Google Scholar 

  5. Anderson JM (1982) The significance of grana stacking in chlorophyll b containing chloroplasts. Photobiochem Photophys 3:225–241

    Google Scholar 

  6. Anderson JM, Melis A (1983) Localization of different photosystems in seperate regions of chloroplast membranes. Proc Natl Acad Sci USA 80:745–749

    Article  Google Scholar 

  7. P-Arvidson O, Sundby C (1999) A model for the topology of the chloroplast thylakoid membrane. Aust J Plant Physiol 26:687–694

    Article  Google Scholar 

  8. Berry H (2002) Monte Carlo simulations of enzyme reactions in two dimensions: fractal kinetics and spatial segregation. Biophys J 83(4):1891–901

    Google Scholar 

  9. Berry S, Rumberg B (2000) Kinetic modeling of the photosynthetic electron transport chain. Biochemistry 53:35–53

    Google Scholar 

  10. Blackwell MF, Gibas C, Gygax S, Roman D, Wagner B (1994) The plastoquinone diffusion coefficient in chloroplasts and its mechanistic implications. Biochem Biophys Acta 1183:533–543

    Article  Google Scholar 

  11. Blackwell MF, Whitmarsh J (1989) Examination of plastoquinone diffusion in lipid vesicles. Biophys J 58:1259–1271

    Google Scholar 

  12. Boekema EJ, van Breemen JFL, van Roon H, Dekker JP (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301:1123–1133

    Article  Google Scholar 

  13. Bray D (1998) Signalling complexes: biophysical constraints on intercellular communication. Annu Rev Biophys Biomol Struct 27:59–75

    Article  Google Scholar 

  14. Breyton C (2000) Conformational changes in the cytochrome b6f complex induced by inhibitor binding. J Biol Chem 275:13195–13201

    Article  Google Scholar 

  15. Broadbent SR, Hammersley J-M (1957) Percolation processes I. Crystals and mazes. Proc Cambr Phil Soc 53:629–641

    MATH  MathSciNet  Google Scholar 

  16. Burg MB (2002) Macromolecular crowding as a cell volume sensor. Cell Physiol Biochem 10:251–256

    Article  Google Scholar 

  17. Chapman DJ, Barber J (1990) Analysis of plastoquinone-9 levels in appressed and non-appressed thylakoid membrane regions. Biochim Biophys Acta 850:170–172

    Google Scholar 

  18. Chebotareva NA, Kurganov BI, Livanova NB (2004) Biochemical effects of molecular crowding. Biochemistry (Mosc) 69(11):1239–51

    Article  Google Scholar 

  19. 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 b6f complex of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47:477–508

    Article  Google Scholar 

  20. Diner AB, Babcock GT (1996) Oxygenic photosynthesis: The light reactions, chapter 12. Structure, dynamics, and energy conversion efficiency in photosystem II. Kluwer Academic Publishers, pp 213–247

    Google Scholar 

  21. Eggers DK, Valentine JS (2001) Molecular confinement influences protein structure and enhances thermal protein stability. Prot Sci 10:250–261

    Article  Google Scholar 

  22. Eisinger J, Flores J, Petersen WP (1986) A milling crowd model for local and long–range obstructed lateral diffusion. Biophys J 49:987–1001

    Google Scholar 

  23. Ellis RJ (2001a) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 11:114–119

    Article  Google Scholar 

  24. Ellis RJ (2001b) Macromolecular crowding: obvious but underappreciated. TiBS 26(10):597–604

    Google Scholar 

  25. Ellis RJ, Minton AP (2003) Join the crowd. Nature 425:27–28

    Article  Google Scholar 

  26. Elowitz MB, Surette MG, Wolf P-E, Stock JB, Leibler S (2003) Protein mobility in the cytoplasm of Escherichia coli. J Bacteriol 181:197–302

    Google Scholar 

  27. Flory PJ (1941) Molecular size distribution in three dimensional polymers. I, II, III. J Am Chem Soc 63:3083–3100

    Article  Google Scholar 

  28. Fulton AB (1982) How crowded is the cytoplasm? Cell 30:345–347

    Article  Google Scholar 

  29. Grima R, Schnell S (2006) A systematic investigation of the rate laws valid in intracellular environments. Biophys Chem 124:1–10

    Article  Google Scholar 

  30. Guttman HJ, Anderson CF Jr, Record TM (1995) Analyses of thermodynamic data for concentrated hemoglobin solutions using scaled particle theory: implications for a simple two-state model of water in thermodynamic analyses of crowding in vitro and in vivo. Biophys J 68:835–846

    Google Scholar 

  31. Haehnel W (1976) The reduction kinetics of chlorophyll a I as an indicator for proton uptake between the light reactions in chloroplasts. Biochim Biophys Acta 440:506–521

    Article  Google Scholar 

  32. Haehnel W (1984) Photosynthetic electron transport in higher plants. Ann Rev Plant Physiol 35:659–693

    Google Scholar 

  33. Hall D, Minton AP (2003) Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochim Biophys Acta 1649(2):127–39

    Google Scholar 

  34. Hankamer B, Barber J, Boekema EJ (1997) Structure and membrane organization of photosystem II in green plants. Annu Rev Plant Physiol Plant Mol Biol 48:641–671

    Article  Google Scholar 

  35. Hauska G, Schütz M, Büttner M (1996) Oxygenic Photosynthesis: The Light Reactions, chapter 19. The Cytochrome b6f Complex–Composition, Structure and Function. Kluwer Academic Publishers, pp 377–398

    Google Scholar 

  36. Herzfeld J (1996) Entropically-driven order in crowded solutions: from liquid crystals to cell biology. Acc Chem Res 29:31–37

    Article  Google Scholar 

  37. Hope AB, Huligol RR, Panizza M, Thompson M, Matthews DB (1992) The flash induced turnover of cytochrome b-563, cytochrome f and plastocyanin in chloroplasts. Models and estimation of kinetic parameters. Biochim Biophys Acta 1100:15–26

    Article  Google Scholar 

  38. Hsu B-D (1992) A theoretical study on the fluorescence induction curve of spinach in the absence of DCMU. Biochim Biophys Acta, 1140:30–36

    Article  Google Scholar 

  39. Ignatova Z, Gierasch LM (2004) Quantitative protein stability and aggregation in vivo by real time fluorescent labeling. Proc Natl Acad Sci USA 101:523–528

    Article  Google Scholar 

  40. Joliot P, Joliot A (1992) Electron transfer between photosystem II and the cytochrome bf complex: mechanistic and structural implications. Biochim Biophys Acta 1102:53–61

    Article  Google Scholar 

  41. Joliot P, Lavergne J, Béal D (1992) Plastoquinone compartmentation in chloroplasts. I. evidence for domains with different rates of photo-reduction. Biochim Biophys Acta 1101:1–12

    Google Scholar 

  42. Kirchhoff H, Horstmann S, Weis E (2000) Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. Biochim Biophys Acta, Bioenergetics 1459(1):148–168

    Article  Google Scholar 

  43. Kirchhoff H, Mukherjee U, Galla H-J (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41:4872–4882

    Article  Google Scholar 

  44. Kirchhoff H, Tremmel I, Haase W, Kubitscheck U (2004) Supramolecular photosystem II organization in grana thylakoid membranes: evidence for a structured arrangement. Biochemistry 43:9204–13

    Article  Google Scholar 

  45. Kopelman R (1986) Rate-processes on fractals: theory, simulations, and experiments. J Stat Phys 42:185–200

    Article  Google Scholar 

  46. Kopelman R (1988) Fractal reaction kinetics. Science 241:1620–1626

    Article  Google Scholar 

  47. Kühlbrandt W, Wang DN (1991) Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature 350:130–134

    Article  Google Scholar 

  48. Lang F, Busch GL, Ritter M, Völkl H, Waldegger S, Gulbins E, Häussinger D (1998) Functional significance of cell volume regulatory mechanisms. Physiol Rev 78:247–306

    Google Scholar 

  49. Lavergne J, Bouchaud J-P, Joliot P (1992) Plastoquinone compartmentation in chloroplasts. II. theoretical aspects. Biochim Biophys Acta 1101:13–22

    Google Scholar 

  50. Lavergne J, Briantais J-M (1996) Oxygenic Photosynthesis: The Light Reactions, chapter 14. Photosystem II Heterogeneity. Kluwer Academic Publishers, pp 265–287

    Google Scholar 

  51. Lavergne J, Joliot P (1991) Restricted diffusion in photosynthetic membranes. TiBS 16:129–134

    Google Scholar 

  52. Lebowitz JL, Helfand E, Praestgaard E (1965) Scaled particle theory of fluid mixtures. J Chem Phys 43:774–779

    Article  Google Scholar 

  53. Luby-Phelps K (2000) Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int Rev Cytol 192:189–221

    Article  Google Scholar 

  54. Marcelja S (1999) Towards a realistic theory of the interaction of membrane inclusions. Biophys J 76:593–594

    Google Scholar 

  55. Mc Nulty BC, Young GB, Pielak GJ (2006) Macromolecular crowding in the Escherichia coli periplasm maintains alpha-synuclein disorder. J Mol Biol 355:893–897

    Article  Google Scholar 

  56. Michaelis L, Menten M (1913) Die Kinetik der Invertinwirkung. Biochem Z 49:333–369

    Google Scholar 

  57. Minton AP (1981) Excluded volume as a determinant of macromolecular structure and reactivity. Biopolymers 20:(2093)–2120

    Article  Google Scholar 

  58. Minton AP (1983) The effect of volume occupancy upon the thermodynamic activity of proteins: some biochemical consequences. Mol Cell Biochem 55:119–140

    Article  Google Scholar 

  59. Minton AP (1997) Influence of excluded volume upon macromolecular structure and associations in ‘crowded’ media. Curr Opin Biotechnol 8:65–69

    Article  Google Scholar 

  60. Minton AP (2000) Implications of macromolecular crowding for protein assembly. Curr Opin Struct Biol 10:34–39

    Article  Google Scholar 

  61. Minton AP (2001) The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276(14):10577–10580

    Article  Google Scholar 

  62. Minton AP (2006a) How can biochemical reactions within cells differ from those in test tubes. J Cell Sci 119(14):2863–2869

    Article  Google Scholar 

  63. Minton AP (2006b) Macromolecular crowding. Curr Biol 16(8):269–271

    Article  Google Scholar 

  64. Minton AP, Colclasure GC, Parker JC (1992) Model for the role of macromolecular crowding in regulation of cellular volume. Proc Natl Acad Sci USA 89(21):10504–10506

    Article  Google Scholar 

  65. Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol 62:327–367

    Article  Google Scholar 

  66. Mitchell R, Spillmann A, Haehnel W (1990) Plastoquinol diffusion in linear photosynthetic electron transport. Biophys J 58:1011–1024

    Google Scholar 

  67. Ovchinnikov AA, Zeldovich YB (1978) Role of density fluctuations in bimolecular reaction kinetics. Chem Phys 28:215–218

    Article  Google Scholar 

  68. Pierre Y, Breyton C, Tribet C, Kramer D, Olive J, Popot JL (1995) Purification and characterization of the cytochrome b6f complex from Chlamydomonas reinhardtii. J Biol Chem 270:29342–29349

    Article  Google Scholar 

  69. Pink DA (1985) Protein lateral movement in lipid bilayers. simulation studies of its dependence upon protein concentration. Biochim Biophys Acta 818:200–204

    Article  Google Scholar 

  70. Ralston GB (1990) The effect of crowding in protein solutions. J Chem Educ 67:857–860

    Article  Google Scholar 

  71. Rivas G, Fernandez JA, Minton AP (1999) Direct observation of the self-association of dilute proteins in the presence of inert macromolecules at high concentration via tracer sedimentation equilibrium: Theory, experiment, and biological significance. Biochemistry, 38(29):9379–9388

    Article  Google Scholar 

  72. Rivas G, Fernandez JA, Minton AP (2001) Direct observation of the enhancement of non-cooperative protein assembly by macromolecular crowding: indefinite self-association of the bacterial cell division protein. Proc Natl Acad Sci USA 98:3150–3155

    Article  Google Scholar 

  73. Rivas G, Ferrone F, Herzfeld J (2004) Life in a crowded world. EMBO Reports 5(1):23–27

    Article  Google Scholar 

  74. Rohwer JM, Postma PW, Kholodenko BN, Westerhoff HV (1998) Implications of macromolecular crowding for signal transduction and metabolite channeling. Biochemistry 95(18):10547–10552

    Google Scholar 

  75. Ross PD, Minton AP (1977) Analysis of non-ideal behavior in concentrated hemoglobin solutions. J Mol Biol 112(3):437–452

    Article  Google Scholar 

  76. Saxton MJ (1987) Lateral diffusion in an archipelago. The effect of mobile obstacles. Biophys J 52:989–997

    Article  Google Scholar 

  77. Saxton MJ (1989) Lateral diffusion in an archipelago. Distance dependence of the diffusion coefficient. Biophys J 56:615–622

    Google Scholar 

  78. Saxton MJ (2002) Chemically limited reactions on a percolation cluster. J Chem Phys 116(1):203–208

    Article  MathSciNet  Google Scholar 

  79. Saxton MJ, Owicki JC (1989) Concentration effects on reactions in membranes: rhodopsin and transducin. Biochim Biophys Acta 979:27–34

    Article  Google Scholar 

  80. Segal HL (1959) The Enzymes, 2nd ed., chapter: The development of enzyme kinetics. Academic Press, New York, pp 1–48

    Google Scholar 

  81. Somalinga B, Roy R (2002) Volume exclusion effect as a driving force for reverse proteolysis. J Biol Chem 277:43253–43261

    Article  Google Scholar 

  82. Staehelin LA, van der Staay GWM (1996) Oxygenic Photosynthesis: The Light Reactions, chapter 2. Structure, composition, functional organization and dynamic properties of thylakoid membranes. Kluwer Academic Publishers, pp 11–30

    Google Scholar 

  83. Stiehl HH, Witt HT (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Z Naturforsch 24:1588–1598

    Google Scholar 

  84. Stockmayer WH (1943) Theory of molecular size distribution and gel formation in branched chain polymers. J Chem Phys 11:45

    Article  Google Scholar 

  85. Torquato S, Truskett P, Debendetti P (2000) Is random close packing of spheres well defined? Phys Rev Lett 84:2064–2067

    Article  Google Scholar 

  86. Toussaint D, Wilczek F (1983) Particle-antiparticle annihilation in diffusive motion. J Chem Phys 78:2642–2647

    Article  Google Scholar 

  87. Tremmel IG, Kirchhoff H, Weis E, Farquhar GD (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral proteins. Biochim Biophys Acta 1607:97–109

    Article  Google Scholar 

  88. Tremmel IG, Weis E, Farquhar GD (2005) The influence of protein-protein interactions on the organisation of proteins within thylakoid membranes. Biophys J 88:2650–2660

    Article  Google Scholar 

  89. Tremmel IG, Weis E, Farquhar GD (2007) Macromolecular crowding and its influence on possible reaction mechanisms in photosynthetic electron flow. Biochim Biophys Acta 1767:353–361

    Article  Google Scholar 

  90. Uversky VN, Cooper EM, Bower KS, Li J, Fink AL (2001) Accelerated α-synuclein fibrillation in crowded milieu. FEBS Letters 515:99–103

    Article  Google Scholar 

  91. Vaz WLC, Almeida PFF (1993) Phase tolopogy and percolation in multi–phase lipid bilayers: is the biological membrane a domain mosaic? Curr Opinion Struct Biol 3:482–488

    Article  Google Scholar 

  92. Verkman AS (2002) Solute and macromolecular diffusion in cellular aqueous compartments. TiBS 27:27–32

    Google Scholar 

  93. Williams WP (1998) Lipids in Photosynthesis: Structure, Function and Genetics, chapter: The physical properties of thylakoid membrane lipids and their relation to photosynthesis. Kluwer Academic Publishers, pp 103–118

    Google Scholar 

  94. Wollenberger L, Stefansson H, Yu S-G, Albertsson P-Å (1994) Isolation and characterization of vesicles originating from the grana margins. Biochim Biophys Acta 1184:93–102

    Article  Google Scholar 

  95. Yakushevska AE, Jensen PE, Keegstra W, van Roon H, Scheller HV, Boekema EJ, Dekker JP (2001) Supermolecular organization of photosystem II and its associated light-harvesting antenna in arabidopsis thaliana. Eur J Biochem 268:6020–6028

    Article  Google Scholar 

  96. Zimmerman SB, Minton AP (1991) Estimation of macromolecule concentration and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222:599–620

    Article  Google Scholar 

  97. Zimmermann SB, Minton AP (1993) Macromolecular crowding: biophysical, biochemical, and physiological consequences. Annu Rev Biophys Biomol Struct 22:27–65

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Computational Biomolecular Dynamics Group, Max-Planck-Institut für biophysikalische Chemie, Am Fassberg 11, 37077, Göttingen, Germany

    Ira G. Tremmel

Authors
  1. Ira G. Tremmel
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Cellular Engineering, Aachen University of Sciences, Ginsterweg 1, 52428, Jülich, Germany

    Gerhard M. Artmann

  2. Department of Bioengineering and Whitaker Institute of Biomedical Engineering San Diego, University of California, 92093-0412, La Jolla, CA, USA

    Shu Chien

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Tremmel, I. (2008). Molecular Crowding: A Way to Deal with Crowding in Photosynthetic Membranes. In: Artmann, G., Chien, S. (eds) Bioengineering in Cell and Tissue Research. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-75409-1_23

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-75409-1_23

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-75408-4

  • Online ISBN: 978-3-540-75409-1

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics

Search

Navigation