The effects of protein crowding in bacterial photosynthetic membranes on the flow of quinone redox species between the photochemical reaction center and the ubiquinol-cytochrome c2 oxidoreductase

Abstract

Atomic force microscopy (AFM) of the native architecture of the intracytoplasmic membrane (ICM) of a variety of species of purple photosynthetic bacteria, obtained at submolecular resolution, shows a tightly packed arrangement of light harvesting (LH) and reaction center (RC) complexes. Since there are no unattributed structures or gaps with space sufficient for the cytochrome bc(1) or ATPase complexes, they are localized in membrane domains distinct from the flat regions imaged by AFM. This has generated a renewed interest in possible long-range pathways for lateral diffusion of UQ redox species that functionally link the RC and the bc(1) complexes. Recent proposals to account for UQ flow in the membrane bilayer are reviewed, along with new experimental evidence provided from an analysis of intrinsic near-IR fluorescence emission that has served to test these hypotheses. The results suggest that different mechanism of UQ flow exist between species such as Rhodobacter sphaeroides, with a highly organized arrangement of LH and RC complexes and fast RC electron transfer turnover, and Phaeospirillum molischianum with a more random organization and slower RC turnover. It is concluded that packing density of the peripheral LH2 antenna in the Rba. sphaeroides ICM imposes constraints that significantly slow the diffusion of UQ redox species between the RC and cytochrome bc(1) complex, while in Phs. molischianum, the crowding of the ICM with LH3 has little effect upon UQ diffusion. This supports the proposal that in this type of ICM, a network of RC-LH1 core complexes observed in AFM provides a pathway for long-range quinone diffusion that is unaffected by differences in LH complex composition or organization.

Overall energy conversion efficiency of a photosynthetic vesicle

“…The redox state is affected by not only RC and cytbc 1 reactions, but also by transmembrane enzymes succinate dehydrogenase and NADH dehydrogenase ( Figure 5). The low-light and high-light limits for the cycling time, t RC , employed below are based on experimental observation (Woronowicz et al, 2011b(Woronowicz et al, , 2011aCrofts, 2004) instead of direct computation; the reported values of t RC implicitly combine the redox reactions of all enzymes interacting with the quinone/quinol pool, including NADH dehydrogenase. In a stationary state, the rate k ATP ðIÞ of ATP synthesis is equal to the rate k Q!QH 2 ðIÞ as stated in Equation (1), which according to Equations (11) and (13) can be expressed through the cycling time, t RC ðIÞ.…”

“…The low-light limit, t L , of the cycling time, t RC ðIÞ, is observed to range from 0.7 ms for the membrane of an LH2-minus mutant to about 3 ms for the LH2-rich chromatophores adapted to low-light growth conditions (Woronowicz et al, 2011b(Woronowicz et al, , 2011a. In the following, we assume t L ¼ 3 ms for the low-light growth vesicle shown in Figure 1.…”

“…At the high-light limit, the immediate vicinity of a RC contains mostly quinols and the replacement of the converted quinones at the RC becomes rate limited by the turnover at cytbc 1 (Woronowicz et al, 2011b(Woronowicz et al, , 2011a). The high-light limit, t H , of the cycling time, t RC ðIÞ, can be estimated by considering the total turn-over rate at all RCs, namely n RC t À1 H .…”

“…The architecture of the chromatophore, reported in (Ş ener et al, 2007, 2010Cartron et al, 2014), has been determined by combining atomic force microscopy (AFM) (Bahatyrova et al, 2004;Olsen et al, 2008), cryo-electron microscopy (cryo-EM) (Qian et al, 2005;Cartron et al, 2014), crystallography (Koepke et al, 1996;McDermott et al, 1995;Papiz et al, 2003;Jamieson et al, 2002), optical spectroscopy Sener et al, 2010), mass spectroscopy (Cartron et al, 2014), and proteomics (Jackson et al, 2012;Woronowicz and Niederman, 2010;Woronowicz et al, 2013) data. The composition of the chromatophore depends on growth conditions such as light intensity (Adams and Hunter, 2012;Woronowicz et al, 2011bWoronowicz et al, , 2011a) and can also be influenced by mutations Hsin et al, 2010b).…”

Subcellular Localization and Logistics of Integral Membrane Protein Biogenesis in Escherichia coli

“…mesosomes [Pilhofer et al, 2010]) as discussed in detail in this written symposium. Even with these ICMs, many basic unanswerable questions regarding their biogenesis, maintenance and turnover remain [Drews and Niederman, 2002;Tucker et al, 2010;Woronowicz et al, 2011]. These may be relevant to ICM and micelle biogenesis in E. coli and higher eukaryotes.…”