1887

Abstract

is a major photosynthetic prokaryote in nutrient-limited, open ocean environments and an important participant in the global carbon cycle. This phototroph is distinct from other members of the cyanobacterial lineage to which it belongs because it utilizes a chlorophyll / light-harvesting complex as its major antenna, instead of phycobilisomes. Recently, genes encoding the phycobiliprotein phycoerythrin were identified in several isolates, thus making it the only extant photosynthetic prokaryote to possess a chlorophyll antenna as well as phycobiliprotein genes. In order to understand the evolution of phycobiliproteins in this genus, the authors have sequenced the phycoerythrin genes of two isolates that are the most deeply branching in the lineage and share the highest degree of 16S rDNA sequence similarity to phycobilisome-containing marine . Sequence analyses suggest that within the lineage, the selective forces shaping the evolution of the phycoerythrin gene set have not been uniform. Although strains that are most closely related to marine possess genes (, ) encoding both subunits of phycoerythrin, a more recently evolved strain is shown to lack and to possess a degenerate form of . Differences in phycoerythrin gene sequences between and appear to be consistent with a model of elevated mutation rates rather than relaxed selection. This suggests that although phycoerythrin is not a major constituent of the light-harvesting apparatus in , as it is in , the and genes are still under selection, albeit a different type of selection than in . The evolution of the light-harvesting antenna complex provides an important system for understanding the origins and scope of phylogenetic diversity in ocean ecosystems.

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2001-11-01
2019-10-19
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References

  1. Apt, K. E., Collier, J. L. & Grossman, A. R. ( 1995; ). Evolution of the phycobiliproteins. J Mol Biol 248, 79-96.[CrossRef]
    [Google Scholar]
  2. Ausubel, F., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1995). Short Protocols in Molecular Biology, 3rd edn. New York: Wiley.
  3. Borodovsky, M. & McIninch, J. ( 1993; ). GeneMark: parallel gene recognition for both DNA strands. Comp Chem 17, 123-133.[CrossRef]
    [Google Scholar]
  4. Bryant, D. A. ( 1991; ). Cyanobacterial phycobilisomes: progress toward complete structural and functional analysis via molecular genetics In The Photosynthetic Apparatus: Molecular Biology and Operation , pp. 257-300. Edited by L. Bogorad & K. Vasil. Boston, MA:Academic Press.
  5. Chisholm, S. W., Olson, R. J., Zettler, E. R., Waterbury, J., Goericke, R. & Welschmeyer, N. ( 1988; ). A novel free-living prochlorophyte occurs at high cell concentrations in the oceanic euphotic zone. Nature 334, 340-343.[CrossRef]
    [Google Scholar]
  6. Chisholm, S. W., Frankel, S. L., Goericke, R., Olson, R. J., Palenik, B., Waterbury, J. B., West-Johnsrud, L. & Zettler, E. ( 1992; ). Prochlorococcus marinus nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch Microbiol 157, 297-300.[CrossRef]
    [Google Scholar]
  7. Felsenstein, J. ( 1989; ). phylip – phylogeny inference package (version 3.2). Cladistics 5, 164-166.
    [Google Scholar]
  8. Fields, S. D., Strout, G. W. & Russell, S. D. ( 1997; ). Spray-freezing and freeze substitution (SFFS) of cell suspensions for improved preservation of ultrastructure. Microsc Res Tech 38, 315-328.[CrossRef]
    [Google Scholar]
  9. Gantt, E., Edwards, M. R. & Provasoli, L. ( 1971; ). Chloroplast structure of the Cryptophyceae. Evidence for phycobiliproteins within intrathylakoidal spaces. J Cell Biol 48, 280-290.[CrossRef]
    [Google Scholar]
  10. Goericke, R. & Repeta, D. J. ( 1992; ). The pigments of Prochlorococcus marinus: the presence of divinyl chlorophyll a and b in a marine procaryote. Limnol Oceanogr 37, 425-433.[CrossRef]
    [Google Scholar]
  11. Hess, W. R., Weihe, A., Loiseaux-de Goer, S., Partensky, F. & Vaulot, D. ( 1995; ). Characterization of the single psbA gene of Prochlorococcus marinus CCMP 1375 (Prochlorophyta). Plant Mol Biol 27, 1189-1196.[CrossRef]
    [Google Scholar]
  12. Hess, W. R., Partensky, F., van der Staay, G. W. M., Garcia-Fernandez, J. M., Borner, T. & Vaulot, D. ( 1996; ). Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc Natl Acad Sci USA 93, 11126-11130.[CrossRef]
    [Google Scholar]
  13. Hess, W. R., Steglich, C., Lichtle, C. & Partensky, F. ( 1999; ). The phycoerythrins of Prochlorococcus marinus are associated to the thylakoid membrane and are encoded by a single large gene cluster. Plant Mol Biol 40, 507-521.[CrossRef]
    [Google Scholar]
  14. Ina, Y. ( 1995; ). New methods for estimating the numbers of synonymous and nonsynonymous substitutions. J Mol Evol 40, 190-226.[CrossRef]
    [Google Scholar]
  15. Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M. (2001). mega2: molecular evolutionary genetics analysis software. Bioinformatics (in press).
  16. Lake, J. A. ( 1994; ). Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances. Proc Natl Acad Sci USA 91, 1455-1459.[CrossRef]
    [Google Scholar]
  17. LaRoche, J., van der Staay, G. W. M., Partensky, F. & 8 other authors ( 1996; ). Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93, 15244–15248.[CrossRef]
    [Google Scholar]
  18. Maidak, B. L., Cole, J. R., Lilburn, T. G. & 12 other authors ( 2000; ). The RDP (Ribosomal Database Project) continues. Nucleic Acids Res 28, 173–174.[CrossRef]
    [Google Scholar]
  19. Moore, L. R. & Chisholm, S. W. ( 1999; ). Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol Oceanogr 44, 628-638.[CrossRef]
    [Google Scholar]
  20. Moore, L. R., Rocap, G. & Chisholm, S. W. ( 1998; ). Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393, 464-467.[CrossRef]
    [Google Scholar]
  21. Nei, M. & Gojobori, T. ( 1986; ). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418-426.
    [Google Scholar]
  22. Nei, M. & Kumar, S. (2000). Molecular Evolution and Phylogenetics. New York: Oxford University Press.
  23. Ong, L. J. & Glazer, A. N. ( 1991; ). Phycoerythrins of marine unicellular cyanobacteria. I. Bilin types and locations and energy transfer pathways in Synechococcus spp. phycoerythrins. J Biol Chem 266, 9515-9527.
    [Google Scholar]
  24. Page, R. D. M. ( 1996; ). treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357-358.
    [Google Scholar]
  25. Palenik, B. & Haselkorn, R. ( 1992; ). Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355, 265-267.[CrossRef]
    [Google Scholar]
  26. Partensky, F., LaRoche, J., Wyman, K. & 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.[CrossRef]
    [Google Scholar]
  27. Partensky, F., Hess, W. R. & Vaulot, D. ( 1999; ). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63, 106-127.
    [Google Scholar]
  28. Penno, S., Campbell, L. & Hess, W. R. ( 2000; ). Presence of phycoerythrin in two strains of Prochlorococcus (cyanobacteria) isolated from the subtropical north Pacific ocean. J Phycol 36, 723-729.[CrossRef]
    [Google Scholar]
  29. Rocap, G. (2000). Phylogenetic diversity and ecotypic differentiation in the marine cyanobacteria Prochlorococcus and Synechococcus. PhD thesis, Massachusetts Institute of Technology, Cambridge, MA.
  30. Strimmer, K. & von Haeseler, A. ( 1996; ). Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13, 964-969.[CrossRef]
    [Google Scholar]
  31. Swofford, D. L. (1999). paup*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, MA: Sinauer Associates.
  32. Swofford, D. L., Olsen, G. J., Wadell, P. J. & Hillis, D. M. ( 1996; ). Phylogenetic inference In Molecular Systematics , pp. 407-415. Edited by D. M. Hillis, C. Moritz & B. K. Mable. Sunderland, MA:Sinauer Associates.
  33. Tajima, F. ( 1993; ). Simple methods for testing molecular clock hypothesis. Genetics 135, 599-607.
    [Google Scholar]
  34. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.[CrossRef]
    [Google Scholar]
  35. Ting, C., Rocap, G., King, J. & Chisholm, S. W. ( 1999; ). Characterization of phycoerythrin genes in the chlorophyll a 2 /b 2-containing prokaryote, Prochlorococcus sp. MIT9303 In Photosynthesis: Mechanisms and Effects , pp. 225-228. Edited by G. Garab. Dordrecht:Kluwer.
  36. Urbach, E., Robertson, D. L. & Chisholm, S. W. ( 1992; ). Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355, 267-269.[CrossRef]
    [Google Scholar]
  37. Urbach, E., Scanlan, D. J., Distel, D. L., Waterbury, J. B. & Chisholm, S. W. ( 1998; ). Rapid diversification of marine picoplankton with dissimilar light harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (cyanobacteria). J Mol Evol 46, 188-201.[CrossRef]
    [Google Scholar]
  38. Wilbanks, S. M., de Lorimier, R. & Glazer, A. N. ( 1991; ). Phycoerythrins of marine unicellular cyanobacteria. III. Sequence of a class II phycoerythrin. J Biol Chem 266, 9535-9539.
    [Google Scholar]
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