1887

Microbiology Society logo

Volume 149, Issue 1

Ecosystem-dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis Free

Abstract

Small, coccoid and rod-shaped -type cyanobacteria with either phycoerythrin or phycocyanin as major accessory pigments were isolated from several large, temperate-zone lakes and the brackish Baltic Sea. The picocyanobacteria had two ribosomal operons with a long internal transcribed spacer (ITS-1) separating the 16S rDNA and 23S rDNA. A 16S rRNA-based phylogenetic analysis assigned all isolates to the picophytoplankton clade [ Urbach, E., Scanlan, D. J., Distel, D. L., Waterbury, J. B. & Chisholm, S. W. ( 1998 ). 46, 188–201], which also comprises marine spp. and spp. The strains assorted to five paraphyletic clusters each containing two or more strains with 99·4–100 % 16S rRNA sequence identity. Five corresponding strain clusters were deduced from analysis of ITS-1 sequences. Sequence divergence in ITS-1 varied between 23 % in the most divergent and 1 % in the phylogenetically most conserved cluster. Clustered strains with low sequence divergence in ITS-1 were frequently isolated from a single ecosystem or hydrographically comparable lakes in the same region. They represent physiologically distinct ecotypes of species which, among other phenotypic variations, frequently differed in their major accessory pigments, the phycobiliproteins. The reproduction of the various pigment traits in different lineages was not correlated with the phylogenetic divergence deduced from 16S rRNA or ITS-1 sequences but rather seemed to be related to characteristics of the ecosystem and habitat from which the strains were isolated. The occurrence of a comparable spectrum of phenotypes in different lineages and ecosystems indicates that different strain clusters developed similar ecotypes during independent adaptive radiations.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): CCA, complementary chromatic adaptation , ITS, internal transcribed spacer , PC, phycocyanin and PE, phycoerythrin
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.25475-0
2003-01-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/1/mic149_22.html?itemId=/content/journal/micro/10.1099/mic.0.25475-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F, Gish W, Miller W, Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
     [Google Scholar]
  2. Barker G. L. A, Handley B. A, Vacharapiyasophon P, Stevens J. R., Hayes P. K. 2001; Allele-specific PCR shows that genetic exchange occurs among genetically diverse Nodularia (cyanobacteria) filaments in the Baltic Sea. Microbiology 146:2865–2875
     [Google Scholar]
  3. Becker S, Fahrbach M, Böger P., Ernst A. 2002; Quantitative tracing, by Taq nuclease assays, of a Synechococcus ecotype in a highly diversified natural population. Appl Environ Microbiol 68:4486–4494
     [Google Scholar]
  4. Boone R, Castenholz R. W., Garrity G. M. (editors) 2001 Bergey's Manual of Systematic Bacteriology, 2nd edn. Vol. 1 New York: Springer;
     [Google Scholar]
  5. Boyer S. L, Flechtner V. R., Johansen J. R. 2001; Is the 16S–23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol 18:1057–1069
     [Google Scholar]
  6. Brass S, Ernst A., Böger P. 1996; An insertion element prevents phycobilisome synthesis in N2-fixing Synechocystis sp. strain BO 8402. Appl Environ Microbiol 62:1964–1968
     [Google Scholar]
  7. Callieri C, Amicucci E, Bertoni R., Vörös L. 1996; Fluorometric characterization of two picocyanobacteria strains from lakes of different underwater light quality. Int Rev Gesamten Hydrobiol 81:13–23
     [Google Scholar]
  8. Chang T.-P. 1980; Zwei neue Synechococcus -Arten aus dem Zürichsee. Schweiz Z Hydrol 42:247–254
     [Google Scholar]
  9. Ernst A, Sandmann G, Postius C, Brass S, Kenter U., Böger P. 1992; Cyanobacterial picoplankton from Lake Constance: II. classification of isolates by cell morphology and pigment composition. Bot Acta 105:161–167
     [Google Scholar]
  10. Ernst A, Marschall P, Postius C. 1995; Genetic diversity among Synechococcus spp. (cyanobacteria) isolated from the pelagial of Lake Constance. FEMS Microbiol Ecol 17:197–204
     [Google Scholar]
  11. Ernst A, Postius C., Böger P. 1996; Glycosylated surface proteins reflect genetic diversity among Synechococcus spp. of Lake Constance. Arch Hydrobiol 48:1–6
     [Google Scholar]
  12. Ernst A, Becker K, Hennes S., Postius C. 2000; Is there a succession in the autotrophic picoplankton of temperate zone lakes?. In Microbial Biosystems: New Frontiers. Proceedings of the 8th International Symposium on Microbial Ecology pp 623–629 Edited by Bell C. R., Brylinski M., Johnson-Green P. Halifax, Canada: Atlantic Canada Society for Microbial Ecology;
     [Google Scholar]
  13. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
     [Google Scholar]
  14. Fox G. E, Wisotzkey J. D., Jurtshuk P. Jr 1992; How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170
     [Google Scholar]
  15. Garcia-Pichel F, Nübel U., Muyzer G. 1998; The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 169:469–482
     [Google Scholar]
  16. Giovannoni S. J, Turner S, Olsen G. J, Barns S, Lane D. J., Pace N. R. 1988; Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592
     [Google Scholar]
  17. Grossman A. R, Schaefer M. R, Chiang G. G., Collier J. L. 1993; The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749
     [Google Scholar]
  18. Gürtler V., Stanisich V. A. 1996; New approaches to typing and identification of bacteria using the 16S–23S rDNA spacer region. Microbiology 142:3–16
     [Google Scholar]
  19. Herdman M, Janvier J. B, Waterbury J. B, Rippka R, Stanier R. Y., Mandel M. 1979; Deoxyribonucleic acid base composition of cyanobacteria. J Gen Microbiol 111:63–71
     [Google Scholar]
  20. Higgins D. G., Sharp P. M. 1988; clustal: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244
     [Google Scholar]
  21. Honda D, Yokota A., Sugiyama J. 1999; Detection of seven major evolutionary lineages in cyanobacteria based on 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48:723–739
     [Google Scholar]
  22. Iteman I, Rippka R, Tandeau de Marsac N., Herdman M. 2000; Comparison of conserved structural and regulatory domains within divergent 16S rRNA–23S rRNA spacer sequences of cyanobacteria. Microbiology 146:1275–1286
     [Google Scholar]
  23. Jain R, Rivera M. C., Lake J. A. 1999; Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 96:3801–3806
     [Google Scholar]
  24. Jukes T. H., Cantor C. R. 1969; Evolution of protein molecules. In Mammalian Protein Metabolism Vol. III pp 21–132 Edited by Muntu H. N. New York: Academic Press;
     [Google Scholar]
  25. Kaneko T, Sato S, Kotani H. 21 other authors 1996; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136
     [Google Scholar]
  26. Lu W, Evans E. H, McColl S. K., Saunders V. A. 1997; Identification of cyanobacteria by polymorphisms of PCR-amplified ribosomal DNA spacer region. FEMS Microbiol Lett 153:141–149
     [Google Scholar]
  27. Lyra C, Suomalainen S, Gugger M, Vezie C, Sundman P, Paulin L., Sivonen K. 2001; Molecular characterization of planktic cyanobacteria of Anabaena , Aphanizomenon , Microcystis and Planktothrix genera. Int J Syst Evol Microbiol 51:513–526
     [Google Scholar]
  28. Maeda H, Kawai A., Tilzer M. M. 1992; The water bloom of cyanobacterial picoplankton in Lake Biwa, Japan. Hydrobiologia 24:93–103
     [Google Scholar]
  29. Miller S. R., Castenholz R. W. 2000; Evolution of thermotolerance in hot spring cyanobacteria of the genus Synechococcus . Appl Environ Microbiol 66:4222–4229
     [Google Scholar]
  30. Mullis K. B., Faloona F. A. 1987; Specific synthesis of DNA in vitro via a polymerase catalyzed chain reaction. Methods Enzymol 155:335–350
     [Google Scholar]
  31. Nelissen B, De Baere R, Wilmotte A., De Wachter R. 1996; Phylogenetic relationships of nonaxenic filamentous cyanobacterial strains based on 16S rRNA sequence analysis. J Mol Evol 42:194–200
     [Google Scholar]
  32. Neuschaefer-Rube O, Westermann M, Bluggel M, Meyer H. E., Ernst A. 2000; The blue-colored linker polypeptide L55 is a fusion protein of phycobiliproteins in the cyanobacterium Synechocystis sp. strain BO 8402. Eur J Biochem 267:3623–3632
     [Google Scholar]
  33. Otsuka S, Suda S, Li R, Watanabe M, Oyaizu H, Matsumoto S., Watanabe M. M. 1999; Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol Lett 172:15–21
     [Google Scholar]
  34. Palenik B., Swift H. 1996; Cyanobacterial evolution and prochlorophyte diversity as seen in DNA-dependent RNA polymerase gene sequences. J Phycol 32:638–646
     [Google Scholar]
  35. Pick F. R. 1991; The abundance and composition of freshwater picocyanobacteria in relation to light penetration. Limnol Oceanogr 36:1457–1462
     [Google Scholar]
  36. Pohl T. M., Maier E. 1995; Sequencing 500 kb of yeast DNA using a GATC1500 direct blotting electrophoresis system. BioTechniques 19:482–486
     [Google Scholar]
  37. Postius C., Ernst A. 1999; Mechanisms of dominance: coexistence of picocyanobacterial genotypes in a freshwater ecosystem. Arch Microbiol 172:69–75
     [Google Scholar]
  38. Postius C, Ernst A, Kenter U., Böger P. 1996; Persistence and genetic diversity among strains of phycoerythrin-rich cyanobacteria from the picoplankton of Lake Constance. J Plankton Res 18:1159–1166
     [Google Scholar]
  39. Rippka R, Deruelles J, Waterbury J. B, Herdman M., Stanier R. Y. 1979; Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
     [Google Scholar]
  40. Rippka R, Castenholz R. W., Herdman M. 2001; Form-genus IV. Cyanobium Rippka and Cohen-Bazire 1983. In Bergey's Manual of Systematic Bacteriology, 2nd edn. Vol. 1 pp 498–499 Edited by Boone D. R., Castenholz R. W., Garrity G. M. New York: Springer;
     [Google Scholar]
  41. Robertson B. R, Tezuka N., Watanabe M. M. 2001; Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. Int J Syst Evol Microbiol 51:861–871
     [Google Scholar]
  42. Rocap G, Distel L, Waterbury J. B., Chrisholm S. W. 2002; Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S–23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68:1180–1191
     [Google Scholar]
  43. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
     [Google Scholar]
  44. Sanger F, Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
     [Google Scholar]
  45. Scheldeman P. B, Baurain D, Bouhy R, Scott M, Muhling M, Whitton B. A, Belay A., Wilmotte A. 1999; Arthrospira (‘ Spirulina ’) strains from four continents are resolved into only two clusters, based on amplified ribosomal DNA restriction analysis of the internally transcribed spacer. FEMS Microbiol Lett 172:213–222
     [Google Scholar]
  46. Stockner J. G, Callieri C., Cronberg C. 2000; Picoplankton and other non-bloom-forming cyanobacteria in lakes. In The Ecology of Cyanobacteria pp 195–231 Edited by Whillon B. A., Potts M. Dordrecht: Kluwer;
     [Google Scholar]
  47. Toledo G, Palenik B., Brahamsha B. 1999; Swimming marine Synechococcus strains with widely different photosynthetic pigment ratios form a monophyletic group. Appl Environ Microbiol 65:6247–5251
     [Google Scholar]
  48. Turner S. 1997; Molecular systematics of oxygenic photosynthetic bacteria. Plant Syst Evol 11:suppl13–52
     [Google Scholar]
  49. 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
     [Google Scholar]
  50. Van de Peer Y., De, Wachter R. 1994; treecon: a software package for the construction and drawing of evolutionary trees. Comput Appl Biosci 9:177–182
     [Google Scholar]
  51. Vincent W. F, Bowman J. B, Powell L. M., McMeekin T. A. 2000; Phylogenetic diversity of picocyanobacteria in Arctic and Antarctic ecosystems. In Microbial Biosystems: New Frontiers. Proceedings of the 8th International Symposium on Microbial Ecology pp 317–322 Edited by Bell C. R., Brylinski M., Johnson-Green P. Halifax, Canada: Atlantic Canada Society for Microbial Ecology;
     [Google Scholar]
  52. Vörös L, Gulyas P., Nemeth J. 1991; Occurrence, dynamics and production of picoplankton in Hungarian shallow lakes. Int Rev Gesamten Hydrobiol 76:617–629
     [Google Scholar]
  53. Ward D. M, Ferris M. J, Nold S. C., Bateson M. M. 1998; A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62:1353–1370
     [Google Scholar]
  54. Waterbury J. B., Rippka R. 1989; Subsection I. Order Chroococcales Wettstein 1924, emend. Rippka et al. , 1979. In Bergey's Manual of Systematic Bacteriology vol. 3 pp 1728–1746 Edited by Staley J. T., Bryant M. P., Pfennig N., Holt J. G. Baltimore: Williams & Wilkins;
     [Google Scholar]
  55. West N. J., Adams D. G. 1997; Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria from a single field site. Appl Environ Micriobiol 63:4479–4484
     [Google Scholar]
  56. Wilmotte A, Turner S, Van de Peer Y., Pace N. R. 1992; Taxonomic study of marine Oscillatorian strains (cyanobacteria) with narrow trichomes. II. Nucleotide sequence analysis of the 16S ribosomal RNA. J Phycol 28:828–838
     [Google Scholar]
  57. Wilmotte A, Van der Auwera G., De Wachter R. 1993; Structure of the 16S ribosomal RNA of the thermophilic cyanobacterium Chlorogloeopsis HTF (‘ Mastigocladus laminosus HTF’) strain PCC 7518 and phylogenetic analysis. FEBS Lett 317:96–100
     [Google Scholar]
  58. Wilmotte A, Neefs J. M., De Wachter R. 1994; Evolutionary affiliation of the marine nitrogen-fixing cyanobacterium Trichodesmium sp. strain NIBB 1067, derived by 16S ribosomal RNA sequence analysis. Microbiology 140:2159–2164
     [Google Scholar]
  59. Wood A. M, Phinney D. A., Jentsch C. S. 1998; Water column transparency and the distribution of spectrally distinct forms of phycoerythrin-containing organisms. Mar Ecol Prog Ser 162:25–31
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.25475-0
Loading
Ecosystem-dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis
Microbiology 149, 217 (2003); https://doi.org/10.1099/mic.0.25475-0
/content/journal/micro/10.1099/mic.0.25475-0
/content/journal/micro/10.1099/mic.0.25475-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error