Polyphasic Characterization of Benthic Cyanobacterial Diversity from Biofilms of the Guadarrama River (Spain): Morphological, Molecular, and Ecological Approaches1

Journal of Phycology

Volumn 49, Issue 2, 2013, Pages 282-297

  Loza, Virginia ^a   Berrendero, Esther ^a   Perona, Elvira ^a   Mateo, Pilar ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

16S rRNA gene; Canonical correspondence analysis; Cyanobacterial community composition; Guadarrama river; Phylogenetic relationships; Streams; Water quality

Indexed keywords

APHANOCAPSA; APHANOCAPSA RIVULARIS; CHAMAESIPHON; CHAMAESIPHON INVESTIENS; CHROOCOCCUS; CHROOCOCCUS MINOR; CYANOBACTERIA; CYANOBIUM; LEPTOLYNGBYA; LEPTOLYNGBYA BORYANA; LEPTOLYNGBYA TENUIS; NOSTOC; NOSTOC COMMUNE; NOSTOC PISCINALE; NOSTOC PUNCTIFORME; PHORMIDIUM; PHORMIDIUM AUTUMNALE; PHORMIDIUM SP.; PLEUROCAPSA; POLYMORPHUS; PSEUDANABAENA CATENATA; TOLYPOTHRIX;

EID: 84875959294     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/jpy.12036     Document Type: Article

References (78)

1. Allen, M. B. & Arnon, D. I. 1955. Studies on nitrogen-fixing bluegreen algae. I. Growth and nitrogen fixation by Anabaena cylindrical Lemm. Plant Physiol. 30:366-72.
2. APHA 1992. Standard Methods for the Examination of Waters and Wastewater, 18th ed. American Public Health Asssociation, Washington, DC.
3. Ashelford, K. E., Chuzhanova, N. A., Fry, J. C., Jones, A. J. & Weightman, A. J. 2006. New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl. Environ. Microbiol. 72:5734-41.
4. Becares, E. & Romo, S. 1994. Selective predation of Thecamoeba sphaeronucleolus (Greeff, 1891) on filamentous algae in natural conditions. J. Gen. Appl. Microbiol. 40:15-21.
5. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. 2011. GenBank. Nucleic Acids Res. 39:D32-7.
6. Berrendero, E., Perona, E. & Mateo, P. 2011. Phenotypic variability and phylogenetic relationships of Tolypothrix and Calothrix (Nostocales, Cyanobacteria) from running water. Int. J. Syst. Evol. Microbiol. 61:3039-51.
7. Cantonati, M. 2008. Cyanoprokaryotes and algae other than diatoms in springs and streams of the Dolomiti Bellunesi National Park (Northern Italy). Algol. Stud. 126:113-36.
8. Casamatta, D. A., Johansen, J. R., Vis, M. L. & Broadwater, S. T. 2005. Molecular and morphological characterization of ten polar and near-polar strains within the Oscillatoriales (cyanobacteria). J. Phycol. 41:421-38.
9. Chu, S. P. 1942. The influence of the mineral composition of the medium on the growth of planktonic algae. Part 1. Methods and culture media. J. Ecol. 30:284-325.
10. Cohen, Y. & Gurevitz, M. 2006. The Cyanobacteria-Ecology, physiology and molecular genetics. Prokaryotes 4:1074-98.
11. Cuzman, O. A., Ventura, S., Sili, C., Mascalchi, C., Turchetti, T., D'Acqui, L. P. & Tiano, P. 2010. Biodiversity of phototrophic biofilms dwelling on monumental fountains. Microb. Ecol. 60:81-95.
12. Douterelo, I., Perona, E. & Mateo, P. 2004. Use of cyanobacteria to assess water quality in running waters. Environ. Pollut. 127:377-84.
13. Downing, J. A., Watson, S. B. & McCauley, E. 2001. Predicting cyanobacteria dominance in lakes. Can. J. Fish. Aquat. Sci. 58:1905-8.
14. Edwards, U., Rogall, T., Blöcker, H., Emde, M. & Böttger, E. C. 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 17:7843-53.
15. EN, European Committee for Standardization, 2009. Water quality-guidance standard for the surveying, sampling and laboratory analysis of phytobenthos in shallow running water. EN 15708:2009.
16. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-91.
17. Fewer, D., Friedl, T. & Büdel, B. 2002. Chroococcidiopsis and heterocyst-differentiating Cyanobacteria are each other's closest living relatives. Mol. Phylogenet. Evol. 23:82-90.
18. Fleming, E. D. & Prufert-Bebout, L. 2010. Characterization of cyanobacterial communities from high-elevation lakes in the Bolivian Andes. J. Geophys. Res. 115:G00D07. doi:10.1029/2008JG000817.
19. Flynn, K.J. 2001. A mechanistic model for describing dynamic multi-nutrient, light, temperature interactions in phytoplankton. J. Plankton Res. 23:977-97.
20. Geitler, L. 1932. Cyanophyceae. Reprinted 1985. Koeltz Scientific Books, Koenigsteim, Germany, 1196 pp.
21. Gkelis, S., Rajaniemi, E., Vardaka, M., Moustaka-Gouni, M., Lanaras, T. & Sivonen, K. 2005. Limnothrix redekei (Van Goor) Meffert (Cyanobacteria) strains from lake Kastoria, Greece from a separate phylogenetic group. Microb. Ecol. 49:176-82.
22. Gutowski, A. & Foerster, J. 2009. Benthische Algen ohne Diatomeen und Characeen. Bestimmungshilfe, LANUV-Arbeitsblatt 9, LANUV NRW, Recklinghausen, 474 pp.
23. Hall, T. A. 1999. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41:95-8.
24. 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 Garrity, E., Booner, D. R. & Castenholz, R. W. [Eds.] Bergey's Manual of Systematic Bacteriology. Springer, New York, pp. 493-514.
25. Herschy, R. W. 1995. Streamflow measurement. 2nd ed. E & FN Spon, London, pp. 524.
26. Hoffmann, L., Komárek, J. & Kaštovský, J. 2005. System of cyanoprokaryotes (Cyanobacteria) - state in 2004. Algol. Stud. 117:95-115.
27. Hrouzek, P., Šimek, M. & Komárek, J. 2003. Nitrogenase activity (acetylene reduction activity) and diversity of six soil Nostoc strains. Arch. Hydrobiol. Suppl. 146:87-101.
28. Kauff, F. & Büdel, B. 2011. Phylogeny of cyanobacteria: an overview. Prog. Bot. 72:209-24.
29. Komárek, J. 2010a. Recent changes (2008) in cyanobacteria taxonomy based on a combination of molecular background with phenotype and ecological consequences (genus and species concept). Hydrobiol. 639:245-59.
30. Komárek, J. 2010b. Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera. Hydrobiol. 639:231-43.
31. Komárek, J. & Anagnostidis, K. 1999. Cyanoprocaryota 1. Teil: Chroococcales. In Ettl, H., Gärtner, G., Heynig, H. & Mollenhauer, D. [Eds.] Sußwasserflora Von mitteleuropa 19/1. Gustav Fischer, Jena-Stuttgart-Lübeck-Ulm, Germany, pp. 548.
32. nd Part: Oscillatoriales In Büdel, B., Krienitz, L., Gärtner, G. & Schagerl, M. [Eds.] Süsswasserflora von Mitteleuropa 19/2. Spektrum Akademischer Verlag, Elsevier, Heidelberg, pp. 759.
33. Komárek, J., Kaštovský, J. & Jezberová, J. 2011. Phylogenetic and taxonomic delimitation of the cyanobacterial genus Aphanothece and description of Anathece gen. nov. Eur. J. Phycol. 46:315-26.
34. Komárek, J., Kopecký, J. & Cepák, V. 1999. Generic characters of the simplest cyanoprokaryotes Cyanobium, Cyanobacterium and Synechococcus. Cryptogam. Algol. 20:209-22.
35. 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. 51:513-26.
36. Mateo, P., Perona, E., Berrendero, E., Leganés, F., Martín, M. & Golubić, S. 2011. Life cycle as a stable trait in the evaluation of diversity of Nostoc from biofilms in rivers. FEMS Microbiol. Ecol. 76:185-98.
37. Mollenhauer, D., Mollenhauer, R. & Kluge, M. 1996. Studies on initiation and development of the partner association in Geosiphon pyriforme (Kutz) v Wettstein, a unique endocytobiotic system of a fungus (Glomales) and the cyanobacterium Nostoc punctiforme (Kutz) Hariot. Protoplasma 193:3-9.
38. Mulholland, P. J. & Rosemond, A. D. 1992. Periphyton response to longitudinal nutrient depletion in a woodland stream: evidence of upstream - downstream linkage. J. N. Am. Benthol. Soc. 11:405-19.
39. Noguerol-Seoane, A. & Rifón-Lastra, A. 1999. Some new or poor known Chroococcales in the Iberian Peninsula: Gloeocapsa aeruginosa Kützing, Eucapsis terrestris Akiyama, Aphanocapsa cf. rivularis (Carmichael) Rabenhorst and Pseudocapsa dubia Ercegovic. Bot. Complutensis 23:91-8.
40. Olsson-Francis, K., de la Torre, R. & Cockell, C. S. 2010. Isolation of novel extreme-tolerant Cyanobacteria from a Rock-Dwelling microbial community by using exposure to low Earth Orbit. Appl. Environ. Microbiol. 76:2115-21.
41. Palinska, K. A. & Marquardt, J. 2008. Genotypic and phenotypic analysis of strains assigned to the widespread cyanobacterial morphospecies Phormidium autumnale (Oscillatoriales). Arch. Microbiol. 189:325-35.
42. Palinska, K. A., Thomasius, C. F., Marquardt, J. & Golubić, S. 2006. Phylogenetic evaluation of cyanobacteria preserved as historic herbarium exsiccata. Int. J. Syst. Evol. Microbiol. 56:2253-63.
43. Perona, E., Bonilla, I. & Mateo, P. 1998. Epilithic cyanobacteria communities and water quality: an alternative tool for monitoring eutrophication in the Alberche River (Spain). J. Appl. Phycol. 10:183-91.
44. Perona, E., Bonilla, I. & Mateo, P. 1999. Spatial and temporal changes in water quality in a Spanish river. Sci. Total Environ. 241:75-90.
45. Rajaniemi, P., Hrouzek, P., Kaštovská, K., Willame, R., Rantala, A., Hoffmann, L., Komárek, J. & Sivonen, K. 2005. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int. J. System. Evol. Microbiol. 55:11-26.
46. Rasmussen, U. & Svenning, M. M. 2001. Characterization by genotypic methods of symbiotic Nostoc strains isolated from five species of Gunnera. Arch. Microbiol. 176:204-10.
47. Rejmánková, E., Komárek, J. & Komárková, J. 2004. Cyanobacteria - a neglected component of biodiversity: patterns of species diversity in inland marshes of northern Belize (Central America). Divers. Distrib. 10:189-99.
48. Reynolds, C. S. 1999. Non-determinism to probability, or N:P in the community ecology of phytoplankton: nutrient ratios. Arch. Hydrobiol. 146:23-35.
49. Richter, D., Matula, J. & Pietryka, M. 2009. Cyanobacteria and algae of selected tundra habitats in the Hornsund fiord area (Spitsbergen) Oceanol. Hydrobiol. Stud. 38:65-70.
50. Rippka, R. & Cohen-Bazire, G. 1983. The Cyanobacteriales: a legitímate order based on the type strain Cyanobacterium stanieri? - Ann. Microbiol. (Inst. Pasteur) 134B:21-36.
51. 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.
52. Rodríguez, V., Aguirre de Cárcer, D., Loza, V., Perona, E. & Mateo, P. 2007. A molecular fingerprint technique to detect pollution-related changes in river cyanobacterial diversity. J. Environ. Qual. 36:464-8.
53. Rott, E., Pfister, P., Van Dam, H., Pipp, E., Pall, K., Binder, N. & Ortler, K. 1999. Indikationslisten für Aufwuchsalgen in österreichischen Fließgewässern, Teil 2: Trophieindikation sowie geochemische Präferenz, taxonomische und toxikologische Anmerkungen. Bundesministerium für Land- und Forstwirtschaft, Wien, 248 pp.
54. Saitou, N. & Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-25.
55. Schneider, S. C. & Lindstrøm, E. A. 2011. The periphyton index of trophic status PIT: a new eutrophication metric based on non-diatomaceous benthic algae in Nordic rivers. Hydrobiol. 665:143-55.
56. Scott, J. T. & Marcarelli, A.M. 2012. Cyanobacteria in freshwater benthic environments. In Whitton, B.A. [Ed.] Ecology of Cyanobacteria II. Their Diversity in Space and Time. Springer, Dordrecht, The Netherlands, pp. 271-89.
57. Sheath, R. G. & Burkholder, J. 1985. Characteristics of softwater streams in Rhode Island II: composition and seasonal dynamics of macroalgae communities. Hydrobiol. 128:109-18.
58. Smith, V. H. 2003. Eutrophication of freshwater and coastal marine ecosystems: a global problem. Environ. Sci. Pollut. Res. 10:1-14.
59. Stackebrandt, E. & Ebers, J. 2006. Microbiology today. Taxonomic parameters revisited: tarnished gold standards. Microbiol. Today 33:152-5.
60. Stackebrandt, E. & Goebel, B. M. 1994. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44:846-9.
61. Stanier, R. Y., Kunisawa, R., Mandel, M. & Cohen-Bazire, G. 1971. Purification and properties of unicellular blue-green algae (Order Chroococcales). Bacteriol. Rev. 35:171-205.
62. Stevenson, R. J. & Smol, J. P. 2003. Use of algae in environmental assessments. In Wehr, J. D. & Sheath, R. G. [Eds.] Freshwater Algae in North America: Classification and Ecology. Academic Press, San Diego, pp. 775-804.
63. Strunecký, O., Elster, J. & Komárek, J. 2010. Phylogenetic relationships between geographically separate Phormidium cyanobacteria: is there a link between north and south polar regions?. Polar Biol. 33:1419-28.
64. Tajima, F. & Nei, M. 1984. Estimation of evolutionary distance between nucleotide sequences. Mol. Biol. Evol. 1:269-85.
65. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-9.
66. Taton, A., Grubisic, S., Ertz, D., Hodgson, D. A., Piccardi, R., Biondi, N., Tredici, M. R., Mainini, M., Losi, D., Marinelli, F. & Wilmotte, A. 2006. Polyphasic study of Antarctic cyanobacterial strains. J. Phycol. 42:1257-70.
67. Ter Braak, C. J. F. & Šmilauer, P. 2002. Canoco reference manual and Cano-Draw for Windows user′s guide: Software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, New York, 352 pp.
68. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-80.
69. Tindall, B. J., Rosselló-Móra, R., Busse, H. J., Ludwig, W. & Kämpfer, P. 2010. Notes on the characterization of prokaryote strains for taxonomic purposes. Int. J. Syst. Evol. Microbiol. 60:249-66.
70. Turner, S. 1997. Molecular systematics of oxygenic photosynthetic bacteria. Plant Sys. Evol. Suppl. 11:13-52.
71. Turner, S., Pryer, K. M., Miao, V. P. W. & Palmer, J. D. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J. Eukaryot. Microbiol. 46:327-38.
72. Urbach, E., Robertson, D. & Chisholm, S. W. 1992. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355:267-70.
73. Vicente, J., Colmenarejo, M. F., Sánchez, E., Rubio, A., García, M. G., Borja, R. & Jimenez, A. M. 2011. Evaluation of the water quality in the Guadarrama river at the section of Las Rozas-Madrid, Spain. Water Environ. J. 25:55-66.
74. Waterbury, J. B. 2006. The Cyanobacteria-Isolation, purification and identification. Prokaryotes 4:1053-73.
75. Whitton, B. A. 1992. Diversity, ecology and taxonomy of the cyanobacteria. In Mann, N. H. & Carr, N. G. [Eds.] Photosynthetic Prokaryotes. Biotechnology Handbooks, Plenum, London, pp. 1-51.
76. Whitton, B.A. 2011. Phylum Cyanobacteria. In John, D. M., Whitton, B. A. & Brook, A. J. [Eds.] The Freshwater Algal Flora of the British Isles. An Identification Guide to Freshwater and Terrestrial Algae, 2nd ed. Cambridge University Press, Cambridge, pp. 31-158.
77. Wilmotte, A. 1994. Molecular evolution and taxonomy of the cyanobacteria. In Bryant, D. A. [Ed.] The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Netherlands, pp. 1-25.
78. Wilmotte, A. & Herdman, M. 2001. Phylogenetic relationships among the cyanobacteria based on 16S rRNA sequences. In Boone, D. R. & Castenholz, R. W. [Eds.] Bergey's Manual of Systematic Bacteriology. Springer, New York, pp. 487-93.