Plant Molecular Biology

, Volume 40, Issue 3, pp 507–521 | Cite as

Phycoerythrins of the oxyphotobacterium Prochlorococcus marinus are associated to the thylakoid membrane and are encoded by a single large gene cluster

  • Wolfgang R. Hess
  • Claudia Steglich
  • Christiane Lichtlé
  • Frédéric Partensky
Article

Abstract

An intrinsic divinyl-chlorophyll a/b antenna and a particular form of phycobiliprotein, phycoerythrin (PE) III, coexist in the marine oxyphotobacterium Prochlorococcus marinus CCMP 1375. The genomic region including the cpeB/A operon of P. marinus was analysed. It encompasses 10 153 nucleotides that encode three structural phycobiliproteins and at least three (possibly five) different polypeptides analogous to cyanobacterial or red algal proteins involved either in the linkage of subunits or the synthesis and attachment of chromophoric groups. This gene cluster is part of the chromosome and is located within a distance of less than 110 kb from a previously characterized region containing the genes aspA-psbA-aroC. Whereas the Prochlorococcus phycobiliproteins are characterized by distinct deletions and amino acid replacements with regard to analogous proteins from other organisms, the gene arrangement resembles the organization of phycobiliprotein genes in some other cyanobacteria, in particular marine Synechococcus strains. The expression of two of the Prochlorococcus polypeptides as recombinant proteins in Escherichia coli allowed the production of individual homologous antisera to the Prochlorococcus α and β PE subunits. Experiments using these sera show that the Prochlorococcus PEs are specifically associated to the thylakoid membrane and that the protein level does not significantly vary as a function of light irradiance or growth phase.

cyanobacteria immunogold labelling light-harvesting complexes photosynthesis phycobilins phytoplankton 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Apt, K.E., Collier, J.L. and Grossman, R. 1995. Evolution of the phycobiliproteins. J. Mol. Biol. 248: 79–96.Google Scholar
  2. Bierne, H., Seigneur, M., Ehrlich, S.D. and Michel, B. 1997. uvrD mutations enhance tandem repeat deletion in the Escherichia coli chromosome via SOS induction of the RecF recombination pathway. Mol. Microbiol. 26: 557–567.Google Scholar
  3. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M. and Rochaix, J.D. 1997. The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16: 6095–6104.Google Scholar
  4. Bryant, D.A. 1982. Phycoerythrocyanin and phycoerythrin: properties and occurrence in cyanobacteria. J. Gen. Microbiol. 128: 835–844.Google Scholar
  5. Bullerjahn, G.S. and Post, A.F. 1993. The prochlorophytes: are they more than just chlorophyll a/b-containing cyanobacteria? Crit. Rev. Microbiol. 19: 43–59.Google Scholar
  6. Cassier-Chauvat, C., Poncelet, M. and Chauvat, F. 1997. Three insertion sequences from the cyanobacterium Synechocystis PCC6803 support the occurrence of horizontal DNA transfer among bacteria. Gene 195: 257–66.Google Scholar
  7. Chisholm, S.W., Olson, R.J., Zettler, E.R., Waterbury, J., Goericke, R. and Welschmeyer, N. 1988. A novel free-living prochlorophyte occurs at high cell concentrations in the oceanic euphotic zone. Nature 334: 340–343.Google Scholar
  8. Chisholm, S.W., Frankel, S.L., Goericke, R., Olson, R.J., Palenik, B., Waterbury, J.B., West-Johnsrud, L. and Zettler, E.R. 1992. Prochlorococcus marinus nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch. Microbiol. 157: 297–300.Google Scholar
  9. De Lorimier, R., Wilbanks, S.M. and Glazer, A.N. 1993. Genes of the R-phycocyanin II locus of marine Synechococcus spp., and comparison of protein-chromophore interactions in phycocyanins differing in bilin composition. Plant Mol. Biol. 21: 225–237.Google Scholar
  10. Dubbs, J.M. and Bryant, D.A. 1991. Molecular cloning and transcriptional analysis of the cpeBA operon of the cyanobacterium Pseudanabaena species PCC7409. Mol. Microbiol. 5: 3073–3085.Google Scholar
  11. Gantt, E., Edwards, M.R. and Provasoli, L. 1971. Chloroplast structure of the Cryptophyceae. Evidence for phycobiliproteins within intrathylakoidal spaces. J. Cell. Biol. 48: 280–290.Google Scholar
  12. Goericke, R. and Repeta, D.J. 1992. The pigments of Prochlorococcus marinus: the presence of divinyl chlorophyll a and b in a marine prochlorophyte. Limnol. Oceanogr. 37: 425–433.Google Scholar
  13. Grossman, A.R., Bhaya, D., Apt, K.E. and Kehoe, D.M. 1995. Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu. Rev. Genet. 29: 231–288.Google Scholar
  14. Hess, W.R. 1997. Localization of an open reading frame with homology to human aspartoacylase upstream from psbA in the prokaryote Prochlorococcus marinus CCMP 1375. DNA Sequence 7: 301–306.Google Scholar
  15. Hess, W.R., Weihe, A., Loiseaux-de Goër, S., Partensky, F. and Vaulot, D. 1995. Characterization of the single psbA gene of Prochlorococcus marinus CCMP 1375 (Prochlorophyta). Plant Mol. Biol. 27: 1189–1196.Google Scholar
  16. Hess, W.R., Partensky, F., van der Staay, G.W.M., Garcia-Fernandez, J.M., Börner, T. and Vaulot, D. 1996. Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc. Natl. Acad. Sci. USA 93: 11126–11130.Google Scholar
  17. Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gartner, W., Wilde, A. and Börner, T. 1997. A prokaryotic phytochrome. Nature 386: 663.Google Scholar
  18. Kahn, K., Mazel, D., Houmard, J., Tandeau de Marsac, N. and Schaefer, M.R. 1997. A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis. J. Bact. 179: 998–1006.Google Scholar
  19. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, N., Okumura, S., Shimpo, S., Takeuchi, C., Wada, Z., Watanabe, A., Yamada, M., Yasuda, M. and Tabata, S. 1996. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3: 109–136.Google Scholar
  20. Kehoe, D.M. and Grossman, A.R. 1996. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273: 1409–1412.Google Scholar
  21. Koonin, E.V. and Galperin, M.Y. 1997. Prokaryotic genomes: the emerging paradigm of genome-based microbiology. Curr. Opin. Genet. Dev. 7: 757–763.Google Scholar
  22. Laroche, J., van der Staay, G.W.M., Partensky, F., Ducret, A., Aebersold, R., Li, R., Golden, S.S., Hiller, R.G., Wrench, P.M., Larkum, A.W.D. and Green, B.R. 1996. Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc. Natl. Acad. Sci. USA 93: 15244–15248.Google Scholar
  23. Lawrence, J.G. and Ochman, H. 1998. Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci. USA 95: 9413–9417.Google Scholar
  24. LeBlanc, H.N. and Beatty, J.T. 1996. Topological analysis of the Rhodobacter capsulatus PucC protein and effects of Cterminal deletions on light-harvesting complex II. J. Bact. 178: 4801–4806.Google Scholar
  25. Lichtlé, C., McKay, R.M. and Gibbs, S.P. 1992. Immunogold localization of photosystem I and photosystem II light-harvesting complexes in cryptomonad thylakoids. Biol. Cell 74: 187–194.Google Scholar
  26. Lichtlé, C., Thomas, J.C., Spilar, A. and Partensky, F. 1995. Immunological and ultrastructural characterization of the photosynthetic complexes of the prochlorophyte Prochlorococcus (Oxychlorobacteria). J. Phycol. 31: 934–941.Google Scholar
  27. Lokstein, H., Steglich, C. and Hess, W.R. 1999. Light-harvesting antenna function of phycoerythrin in Prochlorococcus marinus. Biochim. Biophys. Acta 1410: 97–98.Google Scholar
  28. Marquardt, J., Senger, H., Miyashita, H., Miyachi, S. and Mörschel, E. 1997. Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett. 410: 428–432.Google Scholar
  29. Mazel, D., Guglielmi, G., Houmard, J., Sidler, W., Bryant, D.A. and Tandeau de Marsac, N. 1986. Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucl. Acids Res. 14: 8279–8290.Google Scholar
  30. Meurer, J., Plüchken, H., Kowallik, K.V. and Westhoff, P. 1998. A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J. 17: 5286–5297.Google Scholar
  31. Moore, L.R., Goericke, R. and Chisholm, S.W. 1995. Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Mar. Ecol. Prog. Ser. 116: 259–275.Google Scholar
  32. Moore, L.R., Rocap, G. and Chisholm, S.W. 1998. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464–467.Google Scholar
  33. Newman, J., Mann, N.H. and Carr, N.G. 1994. Organization and transcription of the class I phycoerythrin genes of the marine cyanobacterium Synechococcus sp. WH7803. Plant Mol. Biol. 24: 679–683.Google Scholar
  34. Oeda, K., Horiuchi, T. and Sekiguchi, M. 1982. The uvrD gene of E. coli encodes a DNA-dependent ATPase. Nature 298: 98–100.Google Scholar
  35. Ong, L.J., Glazer, A.N. and Waterbury, J.B. 1984. An unusual phycoerythrin from a marine cyanobacterium. Science 224: 80–83.Google Scholar
  36. Palenik, B. and Haselkorn, R. 1992. Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355: 265–267.Google Scholar
  37. Partensky, F., Hoepffner, N., Li, W.K.W., Ulloa, O. and Vaulot, D. 1993. Photoacclimation of Prochlorococcus sp. (Prochlorophyta) strains isolated from the North Atlantic and the Mediterranean Sea. Plant Physiol. 101: 285–296.Google Scholar
  38. Partensky, F., LaRoche, J., Wyman, K. and Falkowski, P.G. 1997. The divinyl-chlorophyll a/b-protein complexes of two strains of the oxyphototrophic marine prokaryote Prochlorococcus: characterization and response to changes in growth irradiance. Photosynth. Res. 51: 209–222.Google Scholar
  39. Partensky, F., Blanchot, J. and Vaulot, D. 1999a. Differential distribution of Prochlorococcus and Synechococcus: a review. In: L. Charpy and A.W.D. Larkum (eds.), Marine Cyanobacteria. Bull. Inst. Océanogr., Monaco, in press.Google Scholar
  40. Partensky, F., Hess, W.R. and Vaulot, D. 1999b. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63: 106–127.Google Scholar
  41. Petit, M.A., Dervyn, E., Rose, M., Entian, K.D., McGovern, S., Ehrlich, S.D. and Bruand, C. 1998. PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling-circle replication. Mol. Microbiol. 29: 261–273.Google Scholar
  42. Pichard, S.L., Campbell, L. and Paul, J.H. 1997. Diversity of the ribulose bisphosphate carboxylase/oxygenase Form I gene (rbcL) in natural phytoplankton communities. Appl. Environ. Microbiol. 63: 3600–3606.Google Scholar
  43. Reichelt, B.Y. and Delaney, S.F. 1983. The nucleotide sequence for the large subunit of ribulose 1,5-bisphosphate carboxylase from a unicellular cyanobacterium, Synechococcus PCC6301. DNA 2: 121–129.Google Scholar
  44. Rhiel, E., Kunz, J. and Wehrmeyer, W. 1989. Immunocytochemical localization of phycoerythrin-545 and of a chlorophyll a/c light harvesting comlex in Cryptomonas maculata (Cryptophyceae). Bot. Acta 102: 46–53.Google Scholar
  45. Roth, J. 1982. The protein A-gold (pAg) technique: a qualitative and quantitative approach for antigen localization on thin sections. In: G.R. Bullock and P. Petruz (Eds.), Techniques in Immunocytochemistry, Vol. I, Academic Press, New York, pp. 107–133.Google Scholar
  46. Ruf, S., Kössel, H. and Bock, R. 1997. Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast-encoded photosystem I-related gene. J. Cell. Biol. 139: 95–102.Google Scholar
  47. Shimada, A., Kanai, S. and Maruyama, T. 1995. Partial sequence of ribulose-1,5-bisphosphate caboxylase/oxygenase and the physiology of Prochloron and Prochlorococcus (Prochlorales). J.Mol. Evol. 40: 671–677.Google Scholar
  48. Sidler, W.A. 1994. Phycobilisome and phycobiliprotein structures. In: D.A. Bryant (ed.), The Molecular Biology of Cyanobacteria, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 139–216.Google Scholar
  49. Stanier, R.Y. 1988. Fine structure of cyanobacteria. Meth. Enzymol. 167: 157–172.Google Scholar
  50. Strimmer, K. and von Haeseler, A. 1997. Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc. Natl. Acad. Sci. USA 94: 6815–6819.Google Scholar
  51. Tichy, H.V., Albien, K.U., Gadon, N. and Drews, G. 1991. Analysis of the Rhodobacter capsulatus puc operon: the pucC gene plays a central role in the regulation of LHII (B800–850 complex) expression. EMBO J. 10: 2949–2955.Google Scholar
  52. Ting, C., Rocap, G., King, J. and Chisholm, S.W. 1998. Characterization of phycoerythrin genes in the chlorophyll a 2/b 2-containing prokaryote Prochlorococcus sp. MIT9303. Abstracts 11th International Photosynthesis Congress, Budapest, p. 29.Google Scholar
  53. Urbach, E. and Chisholm, S.W. 1999. Genetic diversity in uncultured Prochlorococcus populations flow cytometrically sorted from the Sargasso Sea and the Gulf Stream. Limnol. Oceanogr., in press.Google Scholar
  54. Urbach, E., Robertson, D.L. and Chisholm, S.W. 1992. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355: 267–269.Google Scholar
  55. Urbach, E., Scanlan, D.J., Distel, D.L., Waterbury, J.B. and Chisholm, S.W. 1998. Rapid diversification of marine picophytoplankton with dissimilar light harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (cyanobacteria). J. Mol. Evol. 46: 188–201.Google Scholar
  56. Watson, G.M.F. and Tabita, F.R. 1996. Regulation, unique gene organization, and unusual primary structure of carbon fixation genes from a marine phycoerythrin-containing cyanobacterium. Plant Mol. Biol. 32: 1103–1116.Google Scholar
  57. Whitman, W.B., Coleman, D.C. and Wiebe,W.J. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95: 6578–6583.Google Scholar
  58. Wilbanks, S.M. and Glazer, A.N. 1993a. Rod structure of a phycoerythrin II-containing phycobilisome I. Organization and sequence of the gene cluster encoding the major phycobiliprotein rod components in the genome of the marine Synechococcus sp. WH 8020. J. Biol. Chem. 268: 1226–1235.Google Scholar
  59. Wilbanks, S.M. and Glazer, A.N. 1993b. Rod structure of a phycoerythrin II-containing phycobilisome. II. Complete sequence and bilin attachment site of a phycoerythrin subunit. J. Biol. Chem. 268: 1236–1241.Google Scholar
  60. Young, C.S. and Beatty, J.T. 1998. Topological model of the Rhodobacter capsulatus light-harvesting complexI assembly protein LhaA (previously known as ORF1696). J. Bact. 180: 4742–4755.Google Scholar
  61. Young, C.S., Reyes, R.C. and Beatty, J.T. 1998. Genetic complementation and kinetic analyses of Rhodobacter capsulatus ORF1696 mutants indicate the ORF1696 protein enhances assembly of the light-harvesting I complex. J. Bact. 180: 1759–1765.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Wolfgang R. Hess
    • 1
  • Claudia Steglich
    • 2
  • Christiane Lichtlé
    • 2
  • Frédéric Partensky
    • 3
  1. 1.Department of BiologyHumboldt-UniversityBerlinGermany
  2. 2.Laboratoire de Photorégulation et Dynamique des Membranes VégétalesEcole Normale Supérieure, CNRS URA 1810Paris Cedex 05France
  3. 3.Station Biologique, CNRSINSU et Université Pierre et Marie CurieRoscoff CedexFrance

Personalised recommendations