The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes

Abstract

This review describes the structures of the two major integral membrane pigment complexes, the RC-LH1 'core' and LH2 complexes, which together make up the light-harvesting system present in typical purple photosynthetic bacteria. The antenna complexes serve to absorb incident solar radiation and to transfer it to the reaction centres, where it is used to 'power' the photosynthetic redox reaction and ultimately leads to the synthesis of ATP. Our current understanding of the biosynthesis and assembly of the LH and RC complexes is described, with special emphasis on the roles of the newly described bacteriophytochromes. Using both the structural information and that obtained from a wide variety of biophysical techniques, the details of each of the different energy-transfer reactions that occur, between the absorption of a photon and the charge separation in the RC, are described. Special emphasis is given to show how the use of single-molecule spectroscopy has provided a more detailed understanding of the molecular mechanisms involved in the energy-transfer processes. We have tried, with the help of an Appendix, to make the details of the quantum mechanics that are required to appreciate these molecular mechanisms, accessible to mathematically illiterate biologists. The elegance of the purple bacterial light-harvesting system lies in the way in which it has cleverly exploited quantum mechanics.

Nanoantenna enhanced emission of light-harvesting complex 2: the role of resonance, polarization, and radiative and non-radiative rates

“…1,39 Light energy absorbed by the carotenoids and the B800 ring is transferred within one picosecond to the B850 ring, 40 from which emission occurs. The LH2 absorption and emission spectra are presented in Fig.…”

“…1,2 To understand the amazingly high and robust transfer efficiency (490%) several spectroscopic methods have been used to study photosynthetic systems at different levels. Particularly single-molecule fluorescence studies have given valuable information on the electronic properties of individual LH complexes, which are otherwise hidden in the ensemble average.…”

Overall energy conversion efficiency of a photosynthetic vesicle

“…The primary components of chromatophore vesicles in purple bacteria, as depicted in Figure 1, are, in order of energy utililization (Cogdell et al, 2006,Cartron et al, 2014: (i) light harvesting complex 2 (LH2) (Koepke et al, 1996;Papiz et al, 2003); (ii) light harvesting complex 1 (LH1 Sener et al, 2009]); (iii) RC (Jamieson et al, 2002;Strümpfer and Schulten, 2012a); (iv) cytbc 1 (Crofts, 2004;Crofts et al, 2006); and (v) ATP synthase (Feniouk and Junge, 2009;Hakobyan et al, 2012). RC-LH1 complexes typically form dimeric RC-LH1-PufX complexes facilitated by the polypeptide PufX Sener et al, 2009), although monomeric complexes are also found in membranes from photosynthetically grown cells at a ratio of approximately 10% .…”

“…Carotenoids transfer excitation within less than a picosecond to a nearby BChl (Damjanovic´et al, 1999;Berera et al, 2009) and also play a role in quenching triplet states of BChls through reverse excitation transfer (Ritz et al, 2000a). The electronic excitations of BChls embedded in LH1 and LH2 are reviewed in (Hu et al, , 2002Cogdell et al, 2006;van Grondelle and Novoderezhkin, 2006b;Kosztin and Schulten, 2014). These excitations form so-called exciton states, excitations shared among LH1 or LH2 BChls (Ma et al, 1997;Bradforth et al, 1995) coherently (Strümpfer et al, 2012;Ishizaki and Fleming, 2009b;Rebentrost et al, 2009).…”

“…sphaeroides the basic photosynthetic unit is the chromatophore (Cogdell et al, 2006;Strümpfer et al, 2011;Cartron et al, 2014), a 50-70 nm diameter vesicle, as shown in Figure 1, formed through invagination of the intracytoplasmic membrane (Tucker et al, 2010;Gubellini et al, 2007) and comprising over a hundred protein complexes (Jackson et al, 2012;Woronowicz and Niederman, 2010;Woronowicz et al, 2013). The proteins that constitute the chromatophore are primarily the light harvesting (LH) complexes, photosynthetic reaction centers (RCs), cytbc 1 complexes, and ATP synthases, which cooperate to harvest light energy for photophosphorylation.…”