Skip to main content
SpringerLink
Log in

Evolution of heliobacteria: Implications for photosynthetic reaction center complexes

  • Group 6: Genes and Evolution
  • Regular Papers
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The evolutionary position of the heliobacteria, a group of green photosynthetic bacteria with a photosynthetic apparatus functionally resembling Photosystem I of plants and cyanobacteria, has been investigated with respect to the evolutionary relationship to Gram-positive bacteria and cyanobacteria. On the basis of 16S rRNA sequence analysis, the heliobacteria appear to be most closely related to Gram-positive bacteria, but also an evolutionary link to cyanobacteria is evident. Interestingly, a 46-residue domain including the putative sixth membrane-spanning region of the heliobacterial reaction center protein shows rather strong similarity (33% identity and 72% similarity) to a region including the sixth membrane-spanning region of the CP47 protein, a chlorophyll-binding core antenna polypeptide of Photosystem II. The N-terminal half of the heliobacterial reaction center polypeptide shows a moderate sequence similarity (22% identity over 232 residues) with the CP47 protein, which is significantly more than the similarity with the Photosystem I core polypeptides in this region. An evolutionary model for photosynthetic reaction center complexes is discussed, in which an ancestral homodimeric reaction center protein (possibly resembling the heliobacterial reaction center protein) with 11 membrane-spanning regions per polypeptide has diverged to give rise to core of Photosystem I, Photosystem II, and of the photosynthetic apparatus in green, purple, and heliobacteria.

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

Similar content being viewed by others

References

  • Amesz J (1989) Energy transfer and electron transport inHeliobacterium chlorum. Photosynthetica 23: 403–410

    Google Scholar 

  • Beer-Romero P and Gest H (1987)Heliobacillus mobilis, a peritrichously flagellated anoxyphototroph containing bacteriochlorophyllg. FEMS Microbiol Lett 49: 451–454

    Google Scholar 

  • Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33: 91–111

    Google Scholar 

  • Bricker TM (1990) The structure and function of CPa-1 and CPa-2 in Photosystem II. Photosynth Res 24: 1–13

    Google Scholar 

  • Britschgi TB and Giovannoni SJ (1991) Phylogenetic analysis of a natural marine bacterioplankton population by rRNA gene cloning and sequencing. Appl Environm Microbiol 57: 1707–1713

    Google Scholar 

  • Brockmann HJr and Lipinski A (1983) Bacteriochlorophyllg. A new bacteriochlorophyll fromHeliobacterium chlorum. Arch Microbiol 136: 17–19

    Google Scholar 

  • Bryant DA (1992) Molecular biology of Photosystem. I. In: Barber J (ed) Topics in Photosynthesis, Vol 11, pp 501–549. Elsevier, Amsterdam

    Google Scholar 

  • Büttner M, Xie DL, Nelson H, Pinther W, Hauska G and Nelson N (1992) Photosynthetic reaction center genes in green sulfur bacteria and in Photosystem I are related. Proc Natl Acad Sci USA 89: 8135–8139

    Google Scholar 

  • Devereux J, Haeberli P and Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395

    Google Scholar 

  • Erickson JM and Rochaix J-D (1992) The molecular biology of Photosystem II. In: Barber J (ed) Topics in Photosynthesis, Vol 11, pp 101–177. Elsevier, Amsterdam

    Google Scholar 

  • Fish LE, Kück U and Bogorad L (1985) Analysis of the two partially homologous P700 chlorophylla proteins of maize Photosystem I: predictions based on the primary sequences and features shared by other chlorophyll proteins. In: Steinback KE, Bonitz S, Arntzen CJ and Bogorad L (eds) Molecular Biology of the Photosynthetic Apparatus, pp 111–120. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Gest H and Favinger JL (1983)Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a ‘new’ form of bacteriochlorophyll. Arch Microbiol 136: 11–16

    Google Scholar 

  • Giovannoni S, Turner S, Olsen GJ, Barns S, Lane DJ and Pace NR (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170: 3584–3592

    Google Scholar 

  • Golbeck JH (1992) Structure and function of Photosystem I. Ann Rev Plant Physiol Plant Mol Biol 43: 293–324

    Google Scholar 

  • Golbeck JH and Bryant DA (1991) Photosystem I. In: Lee CP (ed) Current Topics in Bioenergetics, Vol 16, pp 83–177. Academic Press, San Diego, CA

    Google Scholar 

  • Hawthornthwaite AM and Cogdell RJ (1991) Bacteriochlorophyll-binding proteins. In: Scheer H (ed) Chlorophylls, pp 493–528. CRC Press, Boca Raton, FL

    Google Scholar 

  • Krauss N, Hinrichs W, Witt I, Fromme P, Pritzkow W, Dauter Z, Betzel C, Wilson KS, Witt HT and Sänger W (1993) Three-dimensional structure of system I of photosynthesis at 6 Å resolution. Nature 361: 326–331

    Google Scholar 

  • Kühlbrandt W, Wang DN and Fujiyoshi (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621

    Google Scholar 

  • Liebl U, Mockensturm-Wilson M, Trost JT, Brune DC, Blankenship RE and Vermaas W (1993) Single core polypeptide in the reaction center of the photosynthetic bacteriumHeliobacillus mobilis: Structural implications and relations to other photosystems. Proc Natl Acad Sci USA 90: 7124–7128

    Google Scholar 

  • Madigan M (1992) The family Heliobacteriaceae. In: Balows A Trüper HG, Dworkin M, Schliefer KH and Harder W (eds) The Prokaryotes, 2nd ed, pp 1981–1992. Springer, Berlin

    Google Scholar 

  • Margulies MM (1991) Sequence similarity between photosystems I and II. Identification of a Photosystem I reaction center transmembrane helix that is similar to transmembrane helix IV of the D2 subunit of Photosystem II and the M subunit of the non-sulfur purple and flexible green bacteria. Photosynth Res 29: 133–147

    Google Scholar 

  • Michel H and Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II. Biochemistry 27: 1–7

    Google Scholar 

  • Neefs J-M, Van dePeer Y, DeRijk P, Chapelle S and DeWachter R (1993) Compilation of small ribosomal subunit RNA structures. Nucl Acids Res 21: 3025–3049

    Google Scholar 

  • Rochaix J-D, Dron M, Rahire M and Malnoë P (1984) Sequence homology between the 32 kDalton and the D2 chloroplast membrane polypeptides ofChlamydomonas reinhardtii, Plant Mol Biol 3: 363–370

    Google Scholar 

  • Shen G and Vermaas WFJ (1994) Mutation of chlorophyll ligands in the chlorophyll-binding CP47 protein as studied in aSynechocystis sp. PCC 6803 Photosystem I-less background. Biochemistry (in press)

  • Shen G, Eaton-Rye JJ and Vermaas WFJ (1993) Mutation of histidine residues in CP47 leads to destabilization of the Photosystem II complex and to impairment of light energy transfer. Biochemistry 32: 5109–5115

    Google Scholar 

  • Thornber JP, Morishige DT, Anandan S and Peter GF (1991) Chlorophyll-carotenoid proteins of higher plant thylakoids. In: Scheer H (ed) Chlorophylls, pp 549–585 CRC Press, Boca Raton, FL

    Google Scholar 

  • Tomioka N and Sugiura M (1983) The complete nucleotide sequence of a 16S ribosomal RNA gene from a blue-green alga,Anacystis nidulans. Mol Gen Genet 191: 46–50

    Google Scholar 

  • Trebst A (1986) The topology of the plastoquinone and herbicide binding peptides of Photosystem II in the thylakoid membrane. Z Naturforsch 41c: 240–245

    Google Scholar 

  • Trost JT and Blankenship RE (1989) Isolation of a photoactive photosynthetic reaction center-core antenna complex fromHeliobacillus mobilis. Biochemistry 28: 9898–9904

    Google Scholar 

  • Trost JT, Brune DC and Blankenship RE (1992) Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to Photosystem I. Photosynth Res 32: 11–22

    Google Scholar 

  • Urbach E, Robertson DL and Chisholm SW (1992) Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355, 267–270

    Google Scholar 

  • Vermaas W (1993) Moelcular-biological approaches to analyze Photosystem II structure and function. Ann Rev Plant Physiol Plant Mol Biol 44: 457–481

    Google Scholar 

  • Vermaas WFJ, Williams JGK and Arntzen CJ (1987) Sequencing and modification ofpsbB, the gene encoding the CP-47 protein of Photosystem II, in the cyanobacteriumSynechocystis 6803. Plant Mol Biol 8: 317–326

    Google Scholar 

  • VonHeijne G and Gavel Y (1988) Topogenic signals in integral membrane proteins. Eur J Biochem 174: 671–678

    Google Scholar 

  • Ward DM, Bateson MM, Weller R and Ruff-Roberts AL (1992) Ribosomal RNA analysis of microorganisms as they occur in nature. Adv Microb Ecol 12: 219–286

    Google Scholar 

  • Weller R, Walsh-Weller J and Ward DM (1991) 16S rRNA sequences of uncultivated hot springs cyanobacterial mat inhabitants retrieved as randomly primed cDNA. Appl Environm Microbiol 57: 1146–1151

    Google Scholar 

  • Wilmotte A (1994) Molecular evolution and taxonomy of the cyanobacteria. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria. Kluwer, Academic Publishers, Dordrecht, The Netherlands (in press)

    Google Scholar 

  • Wilmotte A, Turner S, Van dePeer Y and Pace NR (1992) Taxonomic study of marine oscillatoriacean strains (cyanobacteria) with narrow trichomes. II. Nucleotide sequence analysis of the 16S ribosomal RNA. J Phycol 28: 828–838

    Google Scholar 

  • Wilmotte A, Van derAuwera G, and DeWachter R (1993) Structure of the 16S ribosomal RNA of the thermophilic cyanobacteriumChlorogloeopsis HTF (‘Mastigocladus laminosus HTF’) strain PCC7518, and phylogenetic analysis. FEBS Lett 317: 96–100

    Google Scholar 

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

    Google Scholar 

  • Woese CR, Debrunner-Vossbrinck BA, Oyaizu H, Stackebrandt E and Ludwig W (1985) Gram-positive bacteria: Possible photosynthetic ancestry. Science 229: 762–765

    Google Scholar 

  • Youvan DC, Bylina EJ, Alberti M, Begusch H and Hearst JE (1984) Nucleotide and deduced polypeptide sequences of the photosynthetic reaction-center, B870 antenna, and flanking polypeptides fromR. capsulata Cell 37: 949–957

    Google Scholar 

  • Zuber H and Brunisholz RA (1991) Structure and function of antenna polypeptides and chlorophyll-protein complexes: principles and variability. In: Scheer H (ed) Chlorophylls, pp 627–703. CRC Press, Boca Raton, FL

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, Arizona State University, 85287-1601, Tempe, AZ, USA

    Wim F. J. Vermaas

  2. Center for the Study of Early Events in Photosynthesis, Arizona State University, 85287-1601, Tempe, AZ, USA

    Wim F. J. Vermaas

Authors
  1. Wim F. J. Vermaas
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vermaas, W.F.J. Evolution of heliobacteria: Implications for photosynthetic reaction center complexes. Photosynth Res 41, 285–294 (1994). https://doi.org/10.1007/BF02184169

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02184169

Key words

Search

Navigation