Comparative molecular evolution of newly discovered picocyanobacterial strains reveals a phylogenetically informative variable region of β-phycoerythrin

Journal of Phycology

Volumn 42, Issue 6, 2006, Pages 1300-1311

  Craig Everroad, R ^a   Michelle Wood, A ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

cpeA; cpeB; Cyanobacteria; Cyanobium; Molecular evolution; Molecular phylogeny; Phycoerythrin; Picocyanobacteria; rpoC1; Synechococcus

Indexed keywords

CONVERGENT EVOLUTION; CYANOBACTERIUM; GENETIC ANALYSIS; MOLECULAR ECOLOGY; PHENOTYPE; PHYLOGENETICS; PIGMENT;

ARABIAN SEA; INDIAN OCEAN;

ALGAE; CYANOBACTERIA; CYANOBIUM; PROCHLOROCOCCUS; SYNECHOCOCCUS; SYNECHOCOCCUS SP.;

EID: 33845594673     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2006.00282.x     Document Type: Article

References (55)

1. Apt, K., Collier, J. & Grossman, A. 1995. Evolution of the phycobiliproteins. J. Mol. Biol. 248:79-96.
2. Brink, K.H, Arnone, R., Coble, P., Flagg, C., Jones, B. H., Kindle, J., Lee, C., Phinney, D. & Wood, M. 1998. Monsoons boost biological productivity in the Arabian Sea. EOS 79:165-9.
3. Coble, P., Hu, C., Gould, R., Chang, G. & Wood, A. M. 2004. Colored dissolved organic matter in the coastal ocean. Oceanography 17:52-9.
4. Cole, J. R., Chai, B., Marsh, T. L., Farris, R. J., Wang, Q., Kulam, S. A., Chandra, S., McGarrell, D. M., Schmidt, T. M., Garrity, G. M. & Tiedje, J. M. 2003. The ribosomal database project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 31:442-3.
5. Crosbie, N. D., Pöeckl, M. & Weisse, T. 2003. Dispersal and phylogenetic diversity of nonmarine picocyanobacteria, inferred from 16S rRNA gene and cpcBA-intergenic spacer sequence analyses. Appl. Environ. Microbiol. 69:5716-21.
6. de Lamballerie, X., Zandotti, C., Vignoli, C., Bollet, C. & de Micco, P. 1992. A one-step microbial DNA extraction method using "Chelex 100" suitable for gene amplification. Res. Microbiol. 143:785-90.
7. de Queiroz, A., Donoghue, M. J. & Kim, J. 1995. Separate versus combined analysis of phylogenetic evidence. Annu. Rev. Ecol. Syst. 26:657-81.
8. Ernst, A., Becker, S., Wollenzien, U. I. A. & Postius, C. 2003. Ecosystem-dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis. Microbiology 149:217-28.
9. Farris, J. S., Källersjö, M., Kluge, A. G. & Bult, C. 1995. Testing significance of incongruence. Cladistics 10:315-9.
10. Fuller, N. J., Marie., D., Partensky, F., Vaulot, D., Post, A. F. & Scanlan, D. J. 2003. Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl. Environ. Microbiol. 69:2430-43.
11. Glazer, A. N. 1999. Cyanobacterial photosynthetic apparatus: an overview. In Charpy, L. & Larkum, A. W. D. [Eds.] Marine Cyanobacteria. Bull. Inst. Oceanogr. (Monaco) 19:419-34.
12. Glover, H. E., Keller, M. D. & Spinrad, R. W. 1987. The effects of light quality and intensity on photosynthesis and growth of marine eukaryotic and prokaryotic phytoplankton clones. J. Exp. Mar. Biol. Ecol. 105:137-59.
13. Guillard, R. R. L. 1975. Culture of phytoplankton for feeding marine invertebrates. In Smith, W. L. & Chanley, M. H. [Eds.] Culture of Marine Invertebrate Animals. Plenum Press, New York, pp. 26-60.
14. Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea cleve. Can. J. Microbiol. 8:229-39.
15. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids. Symp. Ser. 41:95-8.
16. Herdman, M., Castenholz, R. W., Iteman, I., Waterbury, J. B. & Rippka, R. 2001. Subsection I (formerly Chroococcales Wettstein 1924, emend. Rippka, Deruelles, Waterbury, Herdman and Stanier 1979). In Boone, D. R., Castenholz, R. W. & Garrity, G. M. [Eds.] Bergey's Manual of Systematic Bacteriology, The Archaea and the Deeply Branching and Phototrophic Bacteria. 2nd ed. Springer Publishers, New York, pp. 493-514.
17. Hess, W. R., Partensky, F., van der Staay, G. W. M., Garcia-Fernandez, J. M., Börner, T. & Vaulot, D. 1996. Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc. Natl. Acad. Sci. U. S. A. 93:11126-30.
18. Higgins, D. G. & Sharp, P. M. 1988. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237-44.
19. Higgins, D. G. & Sharp, P. M. 1989. Fast and sensitive multiple sequence alignments on a microcomputer. Bioinformatics 5:151-3.
20. Huelsenbeck, J. P. 1998. Systematic bias in phylogenetic analysis: is the strepsiptera problem solved? Syst. Biol. 47:519-37.
21. Huelsenbeck, J. P., Larget, B., Miller, R. E. & Ronquist, F. 2002. Potential applications and pitfalls of Bayesian inference of phylogeny. Syst. Biol. 51:673-88.
22. Huelsenbeck, J. P. & Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754-5.
23. Kluge, A. G. 1989. A concern for evidence and a phylogenetic hypothesis of relationships among epicrates (boidae, serpentes). Syst. Zool. 38:7-25.
24. Lee, C. M., Arnone, R., Brink, K. N. & Fischer, A. S. 2000. The upper ocean response to monsoonal forcing in the Arabian Sea: seasonal and spatial variability. Deep-Sea Res. II 47:1177-226.
25. Li, W. K. W. 1994. Primary production of prochlorophytes, cyanobacteria, and eukaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol. Oceanogr. 39:169-75.
26. Miller, S. R. & Castenholz, R. W. 2000. Evolution of thermotolerance in hot spring cyanobacteria of the genus Synechococcus. Appl. Environ. Microbiol. 66:4222-9.
27. Newman, J., Mann, N. H. & Carr, N. G. 1994. Organization and transcription of the class I phycoerythrin genes of the marine cyanobacterium Synechococcus sp. WH7803. Plant Mol. Biol. 24:679-83.
28. Nubel, U., Garcia-Pichel, F. & Muyzer, G. 1997. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl. Environ. Microbiol. 63:3327-32.
29. Olson, R. J., Chisholm, S. W., Zettler, E. R. & Armbrust, E. V. 1990. Pigments, size, and distributions of Synechococcus in the North Atlantic and Pacific Oceans. Limnol. Oceanogr. 35:45-58.
30. 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. 266:9515-27.
31. Palenik, B. 1994. Cyanobacterial community structure as seen from RNA polymerase gene sequence analysis. Appl. Environ. Microbiol. 60:3212-9.
32. Palenik, B. & Haselkorn, R. 1992. Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355:265-6.
33. Palenik, B. & Swift, H. 1996. Cyanobacterial evolution and prochlorophyte diversity as seen in DNA-dependent RNA polymerase gene sequences. J. Phycol. 32:638-46.
34. Partensky, F., Blanchot, J. & Vaulot, D. 1999. Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In Charpy, L. [Ed.] Marine Cyanobacteria. Bull. Inst. Oceanogr. (Monaco) 19:457-75.
35. Pol, D. & Siddall, M. E. 2001. Biases in maximum likelihood and parsimony: a simulation approach to a 10-taxon case. Cladistics 17:266-81.
36. Poryvkina, L., Babichenko, S., Kaitala, S., Kuosa, H. & Shalapyonok, A. 1994. Spectral fluorescence signatures in the characterization of phytoplankton community composition. J. Plankton Res. 10:1315-28.
37. Posada, D. & Crandall, K. A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-8.
38. Rodriguez, F., Oliver, J. L., Marin, A. & Medina, J. R. 1990. The general stochastic model of nucleotide substitution. J. Theor. Biol. 142:485-501.
39. Six, C., Thomas, J.-C., Thion, L., Lemoine, Y., Zal, F. & Partensky, F. 2005. Two novel phycoerythrin-associated linker proteins in the marine cyanobacterium Synechococcus sp. strain WH8102. J. Bacteriol. 187:1685-94.
40. Steglich, C., Frankenberg-Dinkel, N., Penno, S. & Hess, W. R. 2005. A green light-absorbing phycoerythrin is present in the high-light-adapted marine cyanobacterium Prochlorococcus sp. MED4. Environ. Microbiol. 7:1611-8.
41. Suzuki, Y., Glazko, G. V. & Nei, M. 2002. Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc. Natl. Acad. Sci. U. S. A. 99:16138-43.
42. Swanson, R. V., Ong, L. J., Wilbanks, S. M. & Glazer, A. N. 1991. Phycoerythrins of marine unicellular cyanobacteria II. Characterization of phycobiliproteins with unusually high phycourobilin content. J. Biol. Chem. 266:9528-34.
43. Swofford, D. L. 2003. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
44. Tamura, K. & Nei, M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-26.
45. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. 1997. The clustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-82.
46. Toledo, G., Palenik, B. & Brahamsha, B. 1999. Swimming marine Synechococcus strains with widely different photosynthetic pigment ratios form a monophyletic group. Appl. Environ. Microbiol. 65:5247-51.
47. Urbach, E., Scanlan, D. J., Distel, D. L., Waterbury, J. B. & 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.
48. Waterbury, J. B., Watson, S. W., Valois, F. W. & Franks, D. G. 1986. Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can. Bull. Fish. Aquat. Sci. 214:71-120.
49. Wilbanks, S. M., de Lorimer, R. & Glazer, A. N. 1991. Phycoerythrins of marine unicellular cyanobacteria III. Sequence of a class II phycoerythrin. J. Biol. Chem. 266:9535-9.
50. Wingard, L. L., Miller, S. R., Sellker, J. M. L., Stenn, E., Allen, M. M. & Wood, A. M. 2002. Cyanophycin production in a phycoerythrin-containing marine Synechococcus strain of unusual phylogenetic affinity. Appl. Environ. Microbiol. 68:1772-7.
51. Wood, A. M. 1985. Adaptation of photosynthetic apparatus of marine ultraphytoplankton to natural light fields. Nature 316:253-5.
52. Wood, A. M., Everroad, R. C. & Wingard, L. M. 2005. Measuring growth rates in microalgal cultures. In Anderson, R. A. [Ed.] Algal Culturing Techniques. Elsevier Academic Press, Burlington, MA, pp. 269-85.
53. Wood, A. M., Horan, P. K., Muirhead, K., Phinney, D. A., Yentsch, C. M. & Waterbury, J. B. 1985. Discrimination between types of pigments in marine Synechococcus spp. by scanning spectroscopy, epifluorescence microscopy, and flow cytometry. Limnol. Oceanogr. 30:1303-15.
54. Wood, A. M., Lipsen, M. & Coble, P. 1999. Fluorescence-based characterization of phycoerythrin-containing cyanobacterial communities in the Arabian Sea during the northeast and early southwest monsoon (1994-1995). Deep-Sea Res. II 46:1769-90.
55. Wood, A. M., Phinney, D. A. & Yentsch, C. S. 1998. Water column transparency and the distribution of spectrally distinct forms of phycoerythrin-containing organisms. Mar. Ecol. Prog. Ser. 162:25-31.