Plant Molecular Biology

, Volume 46, Issue 6, pp 683–693 | Cite as

Expression and phylogeny of the multiple antenna genes of the low-light-adapted strain Prochlorococcus marinus SS120 (Oxyphotobacteria)

  • Laurence Garczarek
  • Georg W.M. van der Staay
  • Wolfgang R. Hess
  • Florence Le Gall
  • Frédéric Partensky

Abstract

In contrast to typical cyanobacteria, Prochlorococcus strains possess an intrinsic divinyl-chlorophyll (Chl) a/b-protein complex instead of phycobilisomes as the major light-harvesting system. These pigment-protein complexes are encoded by a variable number of pcb genes depending on the ecotype to which the Prochlorococcus strain belongs: low-light-adapted strains possess several pcb gene copies whereas only a single copy is present in high-light-adapted strains. In this study, the light-regulated expression of the seven pcb genes of Prochlorococcus marinus SS120 was examined. The pcbF gene was found to exhibit a high turnover and its mRNA could only be detected as a degraded product under all light conditions. Steady-state levels of transcripts originating from the six other pcb gene copies varied over several orders of magnitude but were not significantly differentially regulated by light intensity. Transcript levels of most pcb genes increased between 4.5 and 8.5 μmol quanta m−2 s−1, peaked at 45 μmol m−2 s−1 and decreased at the highest irradiance (72 μmol m−2 s−1). A phylogenetic analysis of the Pcb proteins and other members of the six-helix Chl protein superfamily revealed that PcbC and PcbG make a separate cluster with regard to the other Pcbs from SS120. In contrast, Pcb sequences from four high-light-adapted Prochlorococcus sp. strains were found to cluster together and to be less variable than SS120 Pcbs. Thus, pcb genes likely evolved at a different rate in the two Prochlorococcus ecotypes. Their early multiplication and diversification is likely a key factor in the successful adaptation of some genotypes to very-low-light conditions.

chlorophyll a/b-binding proteins CP43 light-harvesting complexes light-regulated gene expression marine cyanobacteria Pcb 

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References

  1. Burnap, R.L., Troyan, T. and Sherman, L.A. 1993. The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43′ ) is encoded by the isiA gene. Plant Physiol. 103: 893–902.PubMedGoogle Scholar
  2. Campbell, L. and Vaulot., D. 1993. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA). Deep-Sea Res. 40: 2043–2060.Google Scholar
  3. 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
  4. Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991–1995.PubMedGoogle Scholar
  5. Dayhoff, M.O., Schwartz, R.M. and Orcutt, B.C. 1978. A model of evolutionary change in proteins. In: M.O. Dayhoff (Ed.) Atlas of Protein Sequence and Structure, Natural Biomedical Research Foundation, pp. 345–352.Google Scholar
  6. Durnford, D.G., Deane, J.A., Tan, S., McFadden, G.I., Gantt, E. and Green, B.R. 1999. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol. 48: 59–68.PubMedGoogle Scholar
  7. Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package). version 3.5c. University of Washington, Seattle, WA.Google Scholar
  8. Ferris, M.J. and Palenik, B. 1998. Niche adaptation in ocean cyanobacteria. Nature 396: 226–228.Google Scholar
  9. Franche, C. and Damerval., T. 1988. Test on nif probes and DNA hybridization. Meth. Enzymol. 167: 803–808.Google Scholar
  10. Garczarek, L., Hess, W.R., Holtzendorff, J., van der Staay, G.W.M. and Partensky, F. 2000. Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proc. Natl. Acad. Sci. USA 97: 4098–4101.PubMedGoogle Scholar
  11. Garczarek, L., Partensky, F., Holtzendorff, J., Horst, W., Babin, M., Mary, I., Thomas, J.-C. and Hess, W.R. 2001. Differen-tial expression of antenna and core genes in Prochlorococcus PCC9511 (Oxyphotobacteria) grown under light-dark cycles. Envir. Microbiol., in press.Google Scholar
  12. Green, B.R. and Durnford, D.G. 1996. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 685-714.Google Scholar
  13. Green, B.R., Pichersky, E. and Kloppstech, K. 1991. Chlorophyll a/b-binding proteins: an extended family. Trends Biochem. Sci. 16: 181–186.PubMedGoogle Scholar
  14. 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.PubMedGoogle Scholar
  15. Hess, W.R., Fingerhut, C. and Schon, A. 1998. RNase P RNA from Prochlorococcus marinus: contribution of substrate domains to recognition by a cyanobacterial ribozyme. FEBS Lett. 431: 138–142.PubMedGoogle Scholar
  16. Hess, W.R., Steglich, C., Lichtlé, C. and Partensky, F. 1999. Phycoerythrins of the oxyphotobacterium Prochlorococcus marinus are associated to the thylakoid membrane and are encoded by a single large gene cluster. Plant Mol. Biol. 40: 507–521.Google Scholar
  17. 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. 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.PubMedGoogle Scholar
  18. Leonhardt, K. and Straus, N.A. 1993. Photosystem II genes isiA, psbDI and psbC in Anabaena sp. PCC 7120: cloning, sequencing and the transcriptional regulation in iron-stressed and iron-repleted cells. Plant Mol. Biol. 24: 63–73.Google Scholar
  19. Marie, D., Brussaard, C., Partensky, F. and Vaulot, D. 1999. Flow cytometric analysis of phytoplankton, bacteria and viruses. In: J.P. Robinson (Ed.) Current Protocols in Cytometry, Interna-tional Society of Analytical Cytology/John Wiley, New York, pp. 11.11.11–11.11.15.Google Scholar
  20. Moore, L.R. and Chisholm, S.W. 1999. Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol. Oceanogr. 44: 628–638.Google Scholar
  21. 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
  22. Moore, L.R., Rocap, G. and Chisholm, S.W. 1998. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464–467.Google Scholar
  23. Nikolaitchik, O.A. and Bullerjahn, G.S. 1998. Transcript analysis of the pcbABC genes encoding the antenna apoproteins in the photosynthetic prokaryote, Prochlorothrix hollandica.FEMS Microbiol. Lett. 168: 187–194.PubMedGoogle Scholar
  24. Palenik, B. and Haselkorn, R. 1992. Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355: 265–267.Google Scholar
  25. 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
  26. Partensky, F., Blanchot, J. and Vaulot, D. 1999a. Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In: L. Charpy and A.W.D. Larkum (Eds.) Marine Cyanobacteria, Musée Océanographique, Monaco, pp. 457–475.Google Scholar
  27. Partensky, F., Hess, W.R. and Vaulot, D. 1999b. Prochlorococcus,a marine photosynthetic prokaryote of global significance. Microb. Mol. Biol. Rev. 63: 106–127.Google Scholar
  28. Penno, S., Campbell, L. and Hess, W.R. 2000a. Presence of phycoerythrin in two strains of Prochlorococcus isolated from the sub-tropical North Pacific Ocean. J. Phycol. 36: 723–729.Google Scholar
  29. Penno, S., Lamerdin, J.E., Larimer, F.W. and Hess, W.R. 2000b. Comparative genomics in marine cyanobacteria: evolution of the phycoerythrin gene cluster in Prochlorococcus. Proceedings of the Genomes 2000 Conference, Paris.Google Scholar
  30. Pinevich, A.V., Averina, S.G. and Velichko, N.V. 1997. Another view on the role of photosynthetic pigments in taxonomy of oxygenic-phototrophic bacteria: proposed rejection of the order Prochlorales Florenzano, Balloni, and Materassi 1986 (Emend. Burger-Wiersma, Stal, and Mur 1989), the family Prochloraceae Florenzano, Balloni, and Materassi 1986, and the family Prochlorotrichaceae Burger-Wiersma, Stal, and Mur 1989. Int. J. Syst. Bacteriol. 47: 1264–1267.Google Scholar
  31. Rippka, R., Coursin, T., Hess, W.R., Lichtlé, C., Scanlan, D.J., Palinska, K.A., Iteman, I., Partensky, F., Tandeau de Marsac, N., Houmard, J. and Herdman, M. 2000. Prochlorococcus marinus Chisholm et al. 1992, subsp. nov. pastoris,strainPCC 9511, the first axenic chlorophyll a 2 /b 2-containing cyanobacterium (Oxyphotobacteria). Int. J. Syst. Evol. Microbiol. 50: 1833–1847.PubMedGoogle Scholar
  32. Saitou, N. and Nei, M. 1987. The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.PubMedGoogle Scholar
  33. Scanlan, D.J., Hess, W.R., Partensky, F., Scanlan, J. and Vaulot, D. 1996. High degree of genetic variation in Prochlorococcus (Prochlorophyta) revealed by RFLP analysis. Eur. J. Phycol. 31: 1–9.Google Scholar
  34. Schwartz, E., Shen, D., Aebersold, R., McGrath, J.M., Pichersky, E. and Green, B.R. 1991. Nucleotide sequence and chromosomal location of Cab11 and Cab12, the genes for the fourth polypep-tide of the photosystem I light-harvesting antenna (LHCI). FEBS Lett. 280: 229–234.PubMedGoogle Scholar
  35. Shimada, A., Kanai, S. and Maruyama, T. 1995a. Partial sequence of ribulose-1,5-bisphosphate carboxylase/oxygenase and the phylogeny of Prochloron and Prochlorococcus (Prochlorales). J. Mol. Evol. 40: 671–677.PubMedGoogle Scholar
  36. Shimada, A., Nishijima, M. and Maruyama, T. 1995b. Seasonal abundance of Prochlorococcus in Suruga Bay, Japan in 1992-1993. J. Oceanogr. 51: 289–300.Google Scholar
  37. Shimada, A., Maruyama, T. and Miyachi, S. 1996. Vertical distributions and photosynthetic action spectra of two oceanic picophytoplankters, Prochlorococcus marinus and Synechococcus sp. Mar. Biol. 127: 15–23.Google Scholar
  38. Smith, S.W., Overbeek, R., Woese, C.R. and Gilbert, W. 1994. The Genetic Data Environment: an expandable GUI for multiple sequence analysis. Comput. Appl. Biosci. 10: 671–675.PubMedGoogle Scholar
  39. Ting, C., Rocap, G., King, J. and Chisholm, S.W. 1999. Characterization of phycoerythrin genes in the chlorophyll a 2 /b 2-containing procaryote, Prochlorococcus sp. MIT9303. In: G. Garab (Ed.) Photosynthesis: Mechanisms and Effects. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 225–228.Google Scholar
  40. Urbach, E., and Chisholm, S.W. 1998. Genetic diversity in Prochlorococcus populations flow cytometrically sorted from the Sargasso Sea and Gulf Stream. Limnol. Oceanogr. 43: 1615–1630.Google Scholar
  41. Urbach, E., Robertson, D.L. and Chisholm, S.W. 1992. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355: 267–270.CrossRefPubMedGoogle Scholar
  42. 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 (Cyanobacte-ria). J. Mol. Evol. 46: 188–201.PubMedGoogle Scholar
  43. van der Staay, G.W.M., Moon-van der Staay, S.Y., Garczarek, L. and Partensky, F. 1998a. Characterization of the Photosystem I subunits PsaI and PsaL from two strains of the marine oxyphototrophic prokaryote Prochlorococcus. Photosynth. Res. 57: 183–191.Google Scholar
  44. van der Staay, G.W.M., Yurkova, N. and Green, B.R. 1998b. The 38 kDa chlorophyll a/b protein of the prokaryote Prochlorothrix hollandica is encoded by a divergent pcb gene. Plant Mol. Biol. 36: 709–716.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Laurence Garczarek
    • 1
  • Georg W.M. van der Staay
    • 1
  • Wolfgang R. Hess
    • 2
  • Florence Le Gall
    • 1
  • Frédéric Partensky
    • 1
  1. 1.Observatoire Océanologique de RoscoffCNRS et Université Paris 6, Station BiologiqueRoscoff cedexFrance
  2. 2.Institut für Biologie/GenetikHumboldt-Universität zu BerlinBerlinGermany

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