Protein shape and crowding drive domain formation and curvature in biological membranes

R.N. Frese, Josep C. Pamies, John D. Olsen, S. Bahatyrova, Chantal D. van der Weij-de Wit, Thijs J. Aartsma, Cornelis Otto, C. Neil Hunter, Daan Frenkel, Rienk van Grondelle

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Abstract

Folding, curvature, and domain formation are characteristics of many biological membranes. Yet the mechanisms that drive both curvature and the formation of specialized domains enriched in particular protein complexes are unknown. For this reason, studies in membranes whose shape and organization are known under physiological conditions are of great value. We therefore conducted atomic force microscopy and polarized spectroscopy experiments on membranes of the photosynthetic bacterium Rhodobacter sphaeroides. These membranes are densely populated with peripheral light harvesting (LH2) complexes, physically and functionally connected to dimeric reaction center-light harvesting (RC-LH1-PufX) complexes. Here, we show that even when converting the dimeric RC-LH1-PufX complex into RC-LH1 monomers by deleting the gene encoding PufX, both the appearance of protein domains and the associated membrane curvature are retained. This suggests that a general mechanism may govern membrane organization and shape. Monte Carlo simulations of a membrane model accounting for crowding and protein geometry alone confirm that these features are sufficient to induce domain formation and membrane curvature. Our results suggest that coexisting ordered and fluid domains of like proteins can arise solely from asymmetries in protein size and shape, without the need to invoke specific interactions. Functionally, coexisting domains of different fluidity are of enormous importance to allow for diffusive processes to occur in crowded conditions.
Original languageEnglish
Pages (from-to)-
JournalBiophysical journal
Volume94
Issue number2
DOIs
Publication statusPublished - 2007

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Membranes
Proteins
Rhodobacter sphaeroides
Light
Atomic Force Microscopy
Spectrum Analysis
Bacteria
Genes
Protein Domains

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Frese, R. N., Pamies, J. C., Olsen, J. D., Bahatyrova, S., van der Weij-de Wit, C. D., Aartsma, T. J., ... van Grondelle, R. (2007). Protein shape and crowding drive domain formation and curvature in biological membranes. Biophysical journal, 94(2), -. https://doi.org/10.1529/biophysj.107.116913
Frese, R.N. ; Pamies, Josep C. ; Olsen, John D. ; Bahatyrova, S. ; van der Weij-de Wit, Chantal D. ; Aartsma, Thijs J. ; Otto, Cornelis ; Hunter, C. Neil ; Frenkel, Daan ; van Grondelle, Rienk. / Protein shape and crowding drive domain formation and curvature in biological membranes. In: Biophysical journal. 2007 ; Vol. 94, No. 2. pp. -.
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Frese, RN, Pamies, JC, Olsen, JD, Bahatyrova, S, van der Weij-de Wit, CD, Aartsma, TJ, Otto, C, Hunter, CN, Frenkel, D & van Grondelle, R 2007, 'Protein shape and crowding drive domain formation and curvature in biological membranes' Biophysical journal, vol. 94, no. 2, pp. -. https://doi.org/10.1529/biophysj.107.116913

Protein shape and crowding drive domain formation and curvature in biological membranes. / Frese, R.N.; Pamies, Josep C.; Olsen, John D.; Bahatyrova, S.; van der Weij-de Wit, Chantal D.; Aartsma, Thijs J.; Otto, Cornelis; Hunter, C. Neil; Frenkel, Daan; van Grondelle, Rienk.

In: Biophysical journal, Vol. 94, No. 2, 2007, p. -.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Protein shape and crowding drive domain formation and curvature in biological membranes

AU - Frese, R.N.

AU - Pamies, Josep C.

AU - Olsen, John D.

AU - Bahatyrova, S.

AU - van der Weij-de Wit, Chantal D.

AU - Aartsma, Thijs J.

AU - Otto, Cornelis

AU - Hunter, C. Neil

AU - Frenkel, Daan

AU - van Grondelle, Rienk

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N2 - Folding, curvature, and domain formation are characteristics of many biological membranes. Yet the mechanisms that drive both curvature and the formation of specialized domains enriched in particular protein complexes are unknown. For this reason, studies in membranes whose shape and organization are known under physiological conditions are of great value. We therefore conducted atomic force microscopy and polarized spectroscopy experiments on membranes of the photosynthetic bacterium Rhodobacter sphaeroides. These membranes are densely populated with peripheral light harvesting (LH2) complexes, physically and functionally connected to dimeric reaction center-light harvesting (RC-LH1-PufX) complexes. Here, we show that even when converting the dimeric RC-LH1-PufX complex into RC-LH1 monomers by deleting the gene encoding PufX, both the appearance of protein domains and the associated membrane curvature are retained. This suggests that a general mechanism may govern membrane organization and shape. Monte Carlo simulations of a membrane model accounting for crowding and protein geometry alone confirm that these features are sufficient to induce domain formation and membrane curvature. Our results suggest that coexisting ordered and fluid domains of like proteins can arise solely from asymmetries in protein size and shape, without the need to invoke specific interactions. Functionally, coexisting domains of different fluidity are of enormous importance to allow for diffusive processes to occur in crowded conditions.

AB - Folding, curvature, and domain formation are characteristics of many biological membranes. Yet the mechanisms that drive both curvature and the formation of specialized domains enriched in particular protein complexes are unknown. For this reason, studies in membranes whose shape and organization are known under physiological conditions are of great value. We therefore conducted atomic force microscopy and polarized spectroscopy experiments on membranes of the photosynthetic bacterium Rhodobacter sphaeroides. These membranes are densely populated with peripheral light harvesting (LH2) complexes, physically and functionally connected to dimeric reaction center-light harvesting (RC-LH1-PufX) complexes. Here, we show that even when converting the dimeric RC-LH1-PufX complex into RC-LH1 monomers by deleting the gene encoding PufX, both the appearance of protein domains and the associated membrane curvature are retained. This suggests that a general mechanism may govern membrane organization and shape. Monte Carlo simulations of a membrane model accounting for crowding and protein geometry alone confirm that these features are sufficient to induce domain formation and membrane curvature. Our results suggest that coexisting ordered and fluid domains of like proteins can arise solely from asymmetries in protein size and shape, without the need to invoke specific interactions. Functionally, coexisting domains of different fluidity are of enormous importance to allow for diffusive processes to occur in crowded conditions.

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M3 - Article

VL - 94

SP - -

JO - Biophysical journal

JF - Biophysical journal

SN - 0006-3495

IS - 2

ER -

Frese RN, Pamies JC, Olsen JD, Bahatyrova S, van der Weij-de Wit CD, Aartsma TJ et al. Protein shape and crowding drive domain formation and curvature in biological membranes. Biophysical journal. 2007;94(2):-. https://doi.org/10.1529/biophysj.107.116913