Skip to main content
SpringerLink
Log in

Exchange and Complementation of Genes Coding for Photosynthetic Reaction Center Core Subunits among Purple Bacteria

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

A mutant of the phototrophic species belonging to the β-proteobacteria, Rubrivivax gelatinosus, lacking the photosynthetic growth ability was constructed by the removal of genes coding for the L, M, and cytochrome subunits of the photosynthetic reaction center complex. The L, M, and cytochrome genes derived from five other species of proteobacteria, Acidiphilium rubrum, Allochromatium vinosum, Blastochloris viridis, Pheospirillum molischianum, and Roseateles depolymerans, and the L and M subunits from two other species, Rhodobacter sphaeroides and Rhodopseudomonas palustris, respectively, have been introduced into this mutant. Introduction of the genes from three of these seven species, Rte. depolymerans, Ach. vinosum, and Psp. molischianum, restored the photosynthetic growth ability of the mutant of Rvi. gelatinosus, although the growth rates were 1.5, 9.4, and 10.7 times slower, respectively, than that of the parent strain. Flash-induced kinetic measurements for the intact cells of these three mutants showed that the photo-oxidized cytochrome c bound to the introduced reaction center complex could be rereduced by electron donor proteins of Rvi. gelatinosus with a t1/2 of less than 10 ms. The reaction center core subunits of photosynthetic proteobacteria appear to be exchangeable if the sequence identities of the LM core subunits between donor and acceptor species are high enough, i.e., 70 % or more.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aklujkar M, Prince RC, Beatty JT (2005) The PuhB protein of Rhodobacter capsulatus functions in photosynthetic reaction center assembly with a secondary effect on light-harvesting complex 1. J Bacteriol 187:1334–1343. doi:10.1128/JB.187.4.1334-1343.2005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aklujkar M, Prince RC, Beatty JT (2006) The photosynthetic deficiency due to puhC gene deletion in Rhodobacter capsulatus suggests a PuhC protein-dependent process of RC/LH1/PufX complex reorganization. Arch Biochem Biophys 454:59–71. doi:10.1016/j.abb.2006.07.009

    Article  CAS  PubMed  Google Scholar 

  • Bauer CE, Buggy JJ, Yang ZM, Marrs BL (1991) The superoperonal organization of genes for pigment biosynthesis and reaction center proteins is a conserved feature in Rhodobacter capsulatus: analysis of overlapping bchB and puhA transcripts. Mol Gen Genet 228:433–444

    Article  CAS  PubMed  Google Scholar 

  • Bose SK (1963) Media for anaerobic growth of photosynthetic bacteria. In: Gest H (ed) Bacterial photosynthesis. The Antioch Press, Yellow Springs, pp 501–510

    Google Scholar 

  • Bullough PA, Qian P, Hunter CN (2009) Reaction center-light harvesting core complexes of purple bacteria In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The Purple Phototrophic Bacteria. Advances in Photosynthesis and Respiration, vol 28. Springer, Netherlands, pp 155–179

  • Coomber SA, Chaudhri M, Connor A, Britton G, Hunter CN (1990) Localized transposon Tn5 mutagenesis of the photosynthetic gene cluster of Rhodobacter sphaeroides. Mol Microbiol 4:977–989

    Article  CAS  PubMed  Google Scholar 

  • Gabrielsen M, Gardiner AT, Cogdell RJ (2009) Peripheral complexes of purple bacteria. In: Hunter C, Daldal F, Thurnauer M, Beatty J (eds) The purple phototrophic bacteria. Advances in Photosynthesis and Respiration, vol 28. Springer, Netherlands, pp 135–153

  • Igarashi N, Harada J, Nagashima S, Matsuura K, Shimada K, Nagashima KVP (2001) Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria. J Mol Evol 52:333–341. doi:10.1007/s002390010163

    CAS  PubMed  Google Scholar 

  • Jones MR (2009) Structural plasticity of reaction centers from purple bacteria. In: Hunter CN, Daldal F, Thurnauer M, Beatty JT (eds) The purple phototrophic bacteria, vol 28., Advances in Photosynthesis and Respiration, Springer, Netherlands, pp 295–321

    Chapter  Google Scholar 

  • Kortlüke C, Breese K, Gad’on N, Labahn A, Drews G (1997) Structure of the puf operon of the obligately aerobic, bacteriochlorophyll α-containing bacterium Roseobacter denitrificans OCh114 and its expression in a Rhodobacter capsulatus puf puc deletion mutant. J Bacteriol 179:5247–5258

    PubMed Central  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Lavergne J, Verméglio A, Joliot P (2009) Functional coupling between reaction centers and cytochrome bc 1 complexes. In: Hunter CN, Daldal F, Thurnauer M, Beatty JT (eds) The purple phototrophic bacteria, vol 28., Advances in Photosynthesis and Respiration, Springer, Netherlands, pp 509–536

    Chapter  Google Scholar 

  • Lupo D, Ghosh R (2004) The reaction center H subunit is not required for high levels of light-harvesting complex 1 in Rhodospirillum rubrum mutants. J Bacteriol 186:5585–5595. doi:10.1128/JB.186.17.5585-5595.2004

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maki H, Matsuura K, Shimada K, Nagashima KVP (2003) Chimeric photosynthetic reaction center complex of purple bacteria composed of the core subunits of Rubrivivax gelatinosus and the cytochrome subunit of Blastochloris viridis. J Biol Chem 278:3921–3928. doi:10.1074/jbc.M209069200

    Article  CAS  PubMed  Google Scholar 

  • Marrs B (1981) Mobilization of the genes for photosynthesis from Rhodopseudomonas capsulata by a promiscuous plasmid. J Bacteriol 146:1003–1012

    PubMed Central  CAS  PubMed  Google Scholar 

  • Menin L, Yoshida M, Jaquinod M, Nagashima KVP, Matsuura K, Parot P, Verméglio A (1999) Dark aerobic growth conditions induce the synthesis of a high midpoint potential cytochrome c 8 in the photosynthetic bacterium Rubrivivax gelatinosus. Biochemistry 38:15238–15244

    Article  CAS  PubMed  Google Scholar 

  • Michel H, Weyer KA, Gruenberg H, Dunger I, Oesterhelt D, Lottspeich F (1986) The ‘light’ and ‘medium’ subunits of the photosynthetic reaction centre from Rhodopseudomonas viridis: isolation of the genes, nucleotide and amino acid sequence. EMBO J 5:1149–1158

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nagashima S, Nagashima KVP (2013) Comparison of photosynthesis gene clusters retrieved from total genome sequences of purple bacteria. In: Beatty TJ (ed) Genome Evolution of Photosynthetic Bacteria, vol 66. Academic Press, Elsevier Inc., pp 151–178

  • Nagashima KVP, Itoh S, Shimada K, Matsuura K (1993) Photo-oxidation of reaction center-bound cytochrome c and generation of membrane potential determined by carotenoid band shift in the purple photosynthetic bacterium, Rhodospirillum molischianum. Biochim Biophys Acta 1140:297–303

    Article  CAS  Google Scholar 

  • Nagashima KVP, Shimada K, Matsuura K (1996) Shortcut of the photosynthetic electron transfer in a mutant lacking the reaction center-bound cytochrome subunit by gene disruption in a purple bacterium, Rubrivivax gelatinosus. FEBS Lett 385:209–213

    Article  CAS  PubMed  Google Scholar 

  • Nagashima KVP, Hiraishi A, Shimada K, Matsuura K (1997a) Horizontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J Mol Evol 45:131–136

    Article  CAS  PubMed  Google Scholar 

  • Nagashima KVP, Matsuura K, Wakao N, Hiraishi A, Shimada K (1997b) Nucleotide sequences of genes coding for photosynthetic reaction centers and light-harvesting proteins of Acidiphilium rubrum and related aerobic acidophilic bacteria. Plant Cell Physiol 38:1249–1258

    Article  CAS  PubMed  Google Scholar 

  • Nagashima KVP, Sakuragi Y, Shimada K, Matsuura K (1998) Comparative analysis of the primary structure of the reaction center-bound cytochrome subunit in purple bacteria. Photosynth Res 55:349–355. doi:10.1023/a:1005912810674

    Article  CAS  Google Scholar 

  • Nagashima KVP, Matsuura K, Shimada K, Verméglio A (2002) High-potential iron-sulfur protein (HiPIP) is the major electron donor to the reaction center complex in photosynthetically growing cells of the purple bacterium Rubrivivax gelatinosus. Biochemistry 41:14028–14032

    Article  CAS  PubMed  Google Scholar 

  • Ohmine M, Matsuura K, Shimada K, Alric J, Verméglio A, Nagashima KVP (2009) Cytochrome c 4 can be involved in the photosynthetic electron transfer system in the purple bacterium Rubrivivax gelatinosus. Biochemistry 48:9132–9139. doi:10.1021/bi901202m

    Article  CAS  PubMed  Google Scholar 

  • Okamura K, Takamiya K, Nishimura M (1985) Photosynthetic electron transfer system is inoperative in anaerobic cells of Erythrobacter species strain OCh 114. Arch Microbiol 142:12–17. doi:10.1007/bf00409229

    Article  CAS  Google Scholar 

  • Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochimica et Biophysica Acta 1458:148–163. doi:10.1016/S0005-2728(00)00065-7

    Article  CAS  PubMed  Google Scholar 

  • Penfold RJ, Pemberton JM (1992) An improved suicide vector for construction of chromosomal insertion mutations in bacteria. Gene 118:145–146

    Article  CAS  PubMed  Google Scholar 

  • Schoepp B, Parot P, Menin L, Gaillard J, Richaud P, Verméglio A (1995) In vivo participation of a high potential iron-sulfur protein as electron donor to the photochemical reaction center of Rubrivivax gelatinosus. Biochemistry 34:11736–11742

    Article  CAS  PubMed  Google Scholar 

  • Shimada K (1995) Aerobic anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, vol 2., Advances in Photosynthesis and Respiration, Springer, Netherlands, pp 105–122

    Chapter  Google Scholar 

  • Suyama T, Shigematsu T, Takaichi S, Nodasaka Y, Fujikawa S, Hosoya H, Tokiwa Y, Kanagawa T, Hanada S (1999) Roseateles depolymerans gen. nov., sp. nov., a new bacteriochlorophyll a-containing obligate aerobe belonging to the beta-subclass of the Proteobacteria. Int J Syst Bacteriol 49:449–457

    Article  PubMed  Google Scholar 

  • Suyama T, Shigematsu T, Suzuki T, Tokiwa Y, Kanagawa T, Nagashima KVP, Hanada S (2002) Photosynthetic apparatus in Roseateles depolymerans 61A is transcriptionally induced by carbon limitation. Appl Environ Microbiol 68:1665–1673

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Verméglio A, Joliot P (2014) Modulation of the redox state of quinones by light in Rhodobacter sphaeroides under anaerobic conditions. Photosynth Res 120:237–246. doi:10.1007/s11120-013-9961-8

    Article  PubMed  Google Scholar 

  • Verméglio A, Nagashima S, Alric J, Arnoux P, Nagashima KVP (2012) Photo-induced electron transfer in intact cells of Rubrivivax gelatinosus mutants deleted in the RC-bound tetraheme cytochrome: insight into evolution of photosynthetic electron transport. Biochim Biophys Acta 1817:689–696. doi:10.1016/j.bbabio.2012.01.011

    Article  PubMed  Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wong DK-H, Collins WJ, Harmer A, Lilburn TG, Beatty JT (1996) Directed mutagenesis of the Rhodobacter capsulatus puhA gene and orf 214: pleiotropic effects on photosynthetic reaction center and light-harvesting 1 complexes. J Bacteriol 178:2334–2342

    PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong J, Inoue K, Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95:14851–14856

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730

    Article  CAS  PubMed  Google Scholar 

  • Yurkov V, Csotonyi JT (2009) New light on aerobic anoxygenic phototrophs. In: Hunter CN, Daldal F, Thurnauer M, Beatty JT (eds) The purple phototrophic bacteria, vol 28., Advances in Photosynthesis and Respiration, Springer, Netherlands, pp 31–55

    Chapter  Google Scholar 

  • Zilsel J, Lilburn TG, Beatty JT (1989) Formation of functional inter-species hybrid photosynthetic complexes in Rhodobacter capsulatus. FEBS Lett 253:247–252

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by PRESTO of the Japan Science and Technology Agency (to K.V.P.N.) and grant-in aid for Scientific Research on Innovative Areas (No.24107004) and Strategic Research Base Development Program for Private Universities from MEXT, Japan (to K. I.).

Author information

Authors and Affiliations

  1. Research Institute for Photobiological Hydrogen Production, Kanagawa University, 2946 Tsuchiya, Hiratsuka, 259-1293, Kanagawa, Japan

    Kenji V. P. Nagashima, Naoki Fusada & Kazuhito Inoue

  2. PRESTO/JST, 4-1-8 Honcho, Kawaguchi, 332-0012, Saitama, Japan

    Kenji V. P. Nagashima

  3. CEA-Cadarache DSV-SBVME Laboratoire de Bioénergétique Cellulaire UMR 7265 CNRS-CEA-Aix-Marseille II, 13108, Saint Paul lez Durance Cedex, France

    André Verméglio

  4. Department of Biological Sciences, Kanagawa University, 2946 Tsuchiya, Hiratsuka, 259-1293, Kanagawa, Japan

    Sakiko Nagashima & Kazuhito Inoue

  5. Department of Biology, Tokyo Metropolitan University, Hachioji, 192-0397, Tokyo, Japan

    Sakiko Nagashima & Keizo Shimada

Authors
  1. Kenji V. P. Nagashima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. André Verméglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naoki Fusada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sakiko Nagashima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Keizo Shimada
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kazuhito Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenji V. P. Nagashima.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nagashima, K.V.P., Verméglio, A., Fusada, N. et al. Exchange and Complementation of Genes Coding for Photosynthetic Reaction Center Core Subunits among Purple Bacteria. J Mol Evol 79, 52–62 (2014). https://doi.org/10.1007/s00239-014-9634-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-014-9634-z

Keywords

Search

Navigation