DOI: 10.3724/SP.J.1145.2011.00138

Chinese Journal of Appplied Environmental Biology (应用与环境生物学报) 2011/17:1 PP.138-143

Molecular Mechanism of Solar Energy Harvesting by Purple Photosynthetic Bacteria*

Photosynthesis is arguably the most important biological process, biology harvests solar energy and transfers it into chemical energy for the growth and reproduction of organisms. The photosynthetic bacteria were the earliest microbe with photosynthesis being found on earth. The photosynthetic apparatus of purple bacteria is a nanometric assembly in the intracytoplasmic membranes and consists of pigment-protein complexes, the photosynthetic RC (Reaction center) and LH (Light harvesting). The primary processes of photosynthesis involve absorption of photons by LH complexes, transfer of excitation energy from the LH complexes to the photosynthetic RC, where the primary energy conversion takes place. The researches on molecular structure and mechanism of purple photosynthetic bacteria harvesting solar energy were summarized. Molecular biology techniques and spectroscopic analysis were applied to research the expression and function of puc2BA and pucsBA by the authors, it was concluded that the puc2BA gene was normally expressed and functional in Rhodobacter sphaeroides, the pucsBA gene of Rhodovulum sulfidophilum and the pufBA gene of Rhodobacter sphaeroides were expressed in Rhodobacter sphaeroides, the heterologous LHII and native LHI were produced and assembled in the membrane. Fig 3, Ref 48

Key words:purple photosynthetic bacteria,solar energy,light-harvesting protein,molecular mechanism

ReleaseDate:2014-07-21 15:54:05

Funds:Supported by the “863” Program of the Ministry of Science and Technology of China (No. 2006AA02Z138), the National Natural Science Foundation of China (Nos. 30600044,30771464), and the Natural Science Foundation of Chongqing, China (Nos. 2006BB1193, 2007BB5414)

1 Bahatyrova S, Frese RN, Siebert CA, Olsen JD, Van Der Werf KO, Van Grondelle R, Niederman RA, Bullough PA, Otto C, Hunter CN. The native architecture of a photosynthetic membrane. Nature, 2004, 430: 1058~1062

2 Garcia-Martin A, Kwa L G, Strohmann B . Structural role of (bacterio) chlorophyll ligated in the energetically unfavorable beta-position. J Biol Chem, 2006, 281: 10626~10634

3 Fowler GJS, Sockalingam GD, Robert B, Hunter CN. Blue shifts in bacteriochlorophyll absorbance correlate with changed hydrogen bonding patterns in light-harvesting LH2 mutants of Rhodobacter sphaeroides with alterations at a Tyr44 and a Tyr45. Biochem J, 1994, 299: 695~700

4 Hu XC, Damjanović A, Ritz T, Schulten K. Photosynthetic apparatus of purple bacteria. Q Rev Biophys, 2002, 35: 1~62

5 Gudowska-Nowak E, Newton MD, Fajer J. Conformational and environmental effects on bacteriochlorophyll optical spectra: Correlations of calculated spectra with structural results. J Phys Chem, 1990, 94: 5795~5801

6 Kwa LG, García-Martín A, Végh AP, Strohmann B , Robert B , Braun P. Hydrogen bonding in a model bacteriochlorophyll-binding site drives assembly of light harvesting complex. J Biol Chem, 2004, 279 (15): 15067~15075

7 Barz WP, Francia F, Venturoli G, Melandri BA, Verméglio A, Oesterhelt D. Role of PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 1. PufX is required for efficient light-driven electron transfer and photophosphorylation under anaerobic conditions. Biochemistry, 1995, 34: 15235~15247

8 Koblízek M, Shih JD, Breitbart SI, Ratcliffe EC, Kolber ZS, Hunter CN, Niederman RA. Sequential assembly of photosynthetic units in Rhodobacter sphaeroides as revealed by fast repetition rate analysis of variable bacteriochlorophylla fluorescence. Biochim Biophys Acta, 2005, 1706: 220~231

9 Barz WP, Verméglio A, Francia F, Venturoli G, Melandri BA, Oesterhelt D. Role of PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 2. PufX is required of efficient ubiquinone/ubiquinol exchange between the reaction centre Q(B) site and the cytochrome b/c1complex. Biochemistry, 1995, 34: 15248~15258

10 Palsdottir H, Hunte C. Lipids in membrane protein structures. Biochim Biophys Acta, 2004, 1666: 2~18

11 Hunte C. Specific protein–lipid interactions in membrane proteins. Biochem Soc Trans, 2005, 33: 938~942

12 Francia F, Wang J, Zischka H, Venturoli G, Oesterhelt D. Role of the N-and C-terminal regions of the Pufx protein in the structural organization of the photosynthetic core complex of Rhodobacter sphaeroides. Eur J Biochem, 2002, 269: 1877~1885

13 Cogdell RJ, Isaacs NW, Freer AA, Arrelano J, Howard TD, Papiz MZ, Hawthornthwaite-Lawless AM, Prince S. The structure and function of the LH2 (B800-850) complex from the purple photosynthetic bacterium Rhodopseudomonas acidophila strain 10050. Prog Biophys & Mol Biol, 1997, 68: 1~27

14 Deinum G, Otte SCM, Gardiner AT, Aartsma TJ, Cogdell RJ, Amesz J. Antenna organisation of Rhodopseudomonas acidophila: a study of the excitation migration. Biochim Biophys Acta, 1991, 1060: 125~131

15 Freer A, Prince S, Sauer K, Papiz M, Lawless A H, McDermott G, Cogdell R, Isaacs NW. Pigment protein interactions and energy transfer in the antenna complex of the photosynthetic bacterium Rhodopseudomonas acidophila. Structure, 1996, 4: 449~462

16 Willett J, Smart JL, Bauer CE. RegA control of bacteriochlorophyll and carotenoid synthesis in Rhodobacter capsulatus. J Bacteriol, 2007, 189 (21): 7765~7773

17 Iustman LJ, Pucheu NL, Kerber NL, Vandekerckhove J, Tadros MH, Garcia AF. Phosphorylation of LHI ß during membrane synthesis in the photosynthetic bacterium Rhodovulum sulfidophilum. Current Microbiol, 2001, 42: 323~329

18 Schubert A , Stenstam A, Beenken WJD, Herek JL, Cogdell R, Pullerits T, Sundstrom V. In vitro self-assembly of the light harvesting pigment-protein LH2 revealed by ultrafast spectroscopy and electron microscopy. Biophys J, 2004, 86: 2363~2373

19 Herek J L, Fraser N J, Pullerits T, Martinsson P, Polívka T, Scheer H, Cogdell RJ, Sundström V. B800 -> B850 energy transfer mechanism in bacterial LH2 complexes investigated by B800 pigment exchange. Biophys J, 2000, 78: 2590~2596

20 Fowler GJS, Visschers RW, Grief GG, Van Grondeller R, Hunter CN. Genetically modified photosynthetic antenna complexes with blue-shifted absorbance bands. Nature, 1992, 355: 848~850

21 Jia C (贾诚), Zhu X (朱恂), Tian X (田鑫), Liao Q (廖强), Wang YZ (王永忠), Xie XW (谢学旺). Effect of initial glucose concentration on glucose transmembrane transportation and metabolism of hydrogen-producing photosynthetic bacteria. Chin J Appl Environ Biol (应用与环境生物学报), 2010, 16 (2): 264~268

22 Saga Y, Tamiaki H. Transmission electron microscopic study on supramolecular nanostructures of bacteriochlorophyll self-aggregates in chlorosomes of green photosynthetic bacteria. J Biosci & Bbioeng, 2006, 102: 118~123

23 Masuda S, Tomida Y, Ohta H, Takamiya K. The critical role of a hydrogen bond between Gln63 and Trp104 in the blue-light sensing BLUFdomain that controls AppA activity. J Mol Biol, 2007, 368 (5): 1223~1230

24 Han Y, Braatsch S , Osterloh L, Klug G . A eukaryotic BLUF domain mediates light-dependent gene expression in the purple bacterium Rhodobacter sphaeroides 2.4.1. Proc Nat Acad Sci, 2004, 101: 12306~12311

25 Ma F, Kimura Y, Zhao XH, Wu YS, Wang P, Fu LM, Wang ZY, Zhang JP. Excitation dynamics of two spectral forms of the core complexes from photosynthetic bacterium Thermochromatium tepidum. Biophys J, 2008, 95 (7): 3349~3357

26 Bauer CE, Bird TH. Regulatory circuits controlling photosynthesis gene expression. Cell, 1996, 85: 5~8

27 Kim YJ, Ko IJ, Lee JM, Kang HY, Kim YM, Kaplan S, Oh JI. Dominant role of the cbb3 oxidase inregulation of photosynthesis gene expression through the PrrBA system in Rhodobacter sphaeroides 2.4.1. J Bacteriol, 2007, 189 (15): 5617~5625

28 Kwa LG, Wegmann D, Brügger B, Wieland FT, Wanner G, Braun P. Mutation of a single residue, β-glutamate-20, alters protein-lipid interactions of light harvesting complex II. Mol Microbiol, 2008, 67: 63~77

29 He Z, Sundström V, Pullerits T. Intermolecular hydrogen bonding between carotenoid and bacteriochlorophyll in LH2. FEBS Lett, 2001, 496: 36~39

30 Francke C, Amesz J. The size of the photosynthetic unit in purple bacteria. Photosyn Res, 1995, 46: 347~352

31 Han Y, Meyer MH, Keusgen M, Klug G. A haem cofactor is required for redox and light signaling by the AppA proteinof Rhodobacter sphaeroides. Mol Microbiol, 2007, 64 (4): 1090~1104

32 Hoffman E, Wrench PM, Sharples FP, Hiller RG, Welte W, Diederichs K. Structural basis of light-harvesting by carotenoids: peridinin-chlorophyll-protein from Anphidinium carterae. Science, 1996, 272: 1788~1791

33 Cogdell RJ, Durant I, Valentine J, Lindsay JG, Schmidt K. The isolation and partial characterisation of the light-harvesting pigment protein complexes of Rhodopseudomonas acidophila. Biochim Biophys Acta, 1983, 722: 427~435

34 Happ HN, Braatsch S, Broschek V, Osterloh L, Klug G. Light-dependent regulation of photosynthesis genes in Rhodobacter sphaeroides 2.4.1 is coordinately controlled by photosynthetic electron transport via the PrrBA two-component system and the photoreceptor AppA. Mol Microbiol, 2005, 58 (3): 903~914

35 Jager A, Braatsch S, Haberzettl K, Metz S, Osterloh L, Han Y C, Klug G. The AppA and PpsR proteins from Rhodobacter sphaeroides can establish a redox-dependent signal chain but fail to transmit blue-light signals in other bacteria. J Bacteriol, 2007, 189 (6): 2274~2282

36 Gardiner AT, MacKenzie RC, Barrett SJ, Kaiser K , Cogdell R J. The purple photosynthetic bacterium Rhodopseudomonas acidophila contains multiple puc peripheral antenna complex (LH2) genes: Cloning and initial characterisation of four β/α pairs. Photosyn Res, 1996, 49: 223~235

37 Tadros MH, Waterkamp K. Multiple copies of the coding regions for the light-harvesting B800–850 α and -polypeptides are present in the Rhodopseudomonas palustris genome. EMBO J, 1989, 8: 1303~1308

38 Tadros MH, Katsiou E, Hoon MA, Yurkova N, Ramji DP. Cloning of a new antenna gene cluster and expression and expression analysis of the antenna gene family of Rhodopseudomonas palustris. Eur J Biochem, 1993, 217: 867~875

39 Wang WN, Hu ZL, Li JZ, Chen GP. Expression characterization and actual function of the second pucBA in Rhodobacter sphaeroides. Biosci Rep, 2009, 29: 165~172

40 Wang WN, Hu ZL, Li JZ, Chen GP. Characteristics of light-harvesting II mutant of Rhodobacter sphaeroides with alterations at the transmembrane helices of β-subunit. Biochemistry (Moscow), 2009, 74 (7): 807~812

41 Wang WN, Hu ZL, Chen XQ, Zhao ZP, Li JZ, Chen GP. Heterologous synthesis and assembly of functional LHii antenna complexes from Rhodovulum sulfidophilum in Rhodobacter sphaeroides mutant. Mol Biol Rep, 2009, 36 (7): 1695~1702

42 Deisenhofer J, Epp O, Miki K, Huber R, Michel H. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3Å resolution. Nature, 1985, 318: 618~624

43 Cogdell RJ, Fyfe PK, Barrett SJ, Prince SM, Freer AA, Isaacs NW, McGlynn P, Hunter CN. The purple bacterial photosynthetic unit. Photosynt Res, 1996, 48: 55~63

44 Shimada H, Ishida K, Machiya Y, Takamiya K. Isolation of SIP, a protein that Interacts with SPB, a possible transcriptional regulatory factor in Rhodobacter sphaeroides. Plant & Cell Physiol, 2007, 48 (10): 1504~1508

45 Ouchane S, Picaud M, Therizoles P, Reiss-Husson F, Astier C. Global regulation of photosynthesis and respiration by FnrL: The first two targets in the tetrapyrrole pathway. J Biol Chem, 2007, 282 (10): 7690~7699

46 Geyer T. On the effects of PufX on the absorption properties of the light-harvesting complexes of Rhodobacter sphaeroides. Biophys J, 2007, 93 (12): 4374~4381

47 Oh JI, Ko IJ, Kaplan S. Reconstitution of the Rhodobacter sphaeroides cbb3-PrrBA signal transduction pathway in vitro. Biochem J, 2004, 43 (24): 7915~7923

48 Dong C, Elsen S, Swem LR, Bauer CE. AerR, a second aerobic repressor of photosynthesis gene expression in Rhodobacter capsulatus. J Bacteriol, 2002, 5: 2805~2814