PCR primers for selective detection of intra-species variations in the bloom-forming cyanobacterium, Microcystis

Harmful Algae

Volumn 23, Issue , 2013, Pages 46-54

  Kataoka, Takafumi ^a   Homma, Takamitsu ^a   Nakano, Shin Ichi ^b   Hodoki, Yoshikuni ^b   Ohbayashi, Kako ^b   Kondo, Ryuji ^a  

^a FUKUI PREFECTURAL UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

16S 23S rDNA ITS region; Intra species variation; Microcystis aeruginosa; Quantitative PCR; Selective detection

Indexed keywords

CYANOBACTERIA; MICROCYSTIS; MICROCYSTIS AERUGINOSA; MICROCYSTIS VIRIDIS; MICROCYSTIS WESENBERGII;

EID: 84873703206     PISSN: 15689883     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hal.2012.12.003     Document Type: Article

References (57)

1. Anagnostidis K., Komárek J. Modern approach to the classification system of Cyanophytes. 1. Introduction. Archiv für Hydrobiologie, Supplement 1985, 71(Algological Studies 38-39):327-472.
2. Anagnostidis K., Komárek J. Modern approach to the classification system of Cyanophytes. 3. Oscillatoriales. Archiv für Hydrobiologie, Supplement 1988, 80(Algological Studies 51-53):291-302.
3. Anagnostidis K., Komárek J. Modern approach to the classification system of Cyanophytes. 5. Stigonematales. Archiv für Hydrobiologie, Supplement 1990, 86(Algological Studies 59):1-73.
4. Bittencourt-Oliveira M.D., de Oliveira M.C., Bolch C.J.S. Genetic variability of Brazilian strains of the Microcystis aeruginosa complex (Cyanobacteria/Cyanophyceae) using the phycocyanin intergenic spacer and flanking regions (cpcBA). Journal of Psychology 2001, 37(5):810-818.
5. Bolch C.J.S., Blackburn S.I., Neilan B.A., Grewe P.M. Genetic characterization of strains of cyanobacteria using PCR-RFLP of the cpcBA intergenic spacer and flanking regions. Journal of Psychology 1996, 32(3):445-451.
6. Briand E., Gugger M., Francois J.C., Bernard C., Humbert J.F., Quiblier C. Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (cyanobacterium) population. Applied and Environment Microbiology 2008, 74(12):3839-3848.
7. Briand E., Escoffier N., Straub C., Sabart M., Quiblier C., Humbert J.F. Spatiotemporal changes in the genetic diversity of a bloom-forming Microcystis aeruginosa (cyanobacteria) population. ISME Journal 2009, 3(4):419-429.
8. Bustin S.A., Nolan T. Pitfalls of quantitative real-time reverse-transcription polymerase chain reaction. Journal of Biomolecular Techniques 2004, 15(3):155-166.
9. Carmichael W.W. Toxic Microcystis and the environment. Toxic Microcystis 1996, 1-11. CRC Press, Florida. M.F. Watanabe, K. Harada, W.W. Carmichael, H. Fujiki (Eds.).
10. Chen Y.W., Gao X.Y., Chen W.M., Qin B.Q. Growth characters and pure culture of Microcystis from Taihu lake. Journal of Lake Science 1999, 11:352-356. (in Chinese).
11. Cohan F.M. What are bacterial species?. Annual Review of Microbiology 2002, 56:457-487.
12. Galey F.D., Beasley V.R., Carmichael W.W., Kleppe G., Hooser S.B., Haschek W.M. Blue-green algae (Microcystis aeruginosa) hepatotoxicosis in dairy cows. American Journal of Veterinary Research 1987, 48(9):1415-1420.
13. Geitler L. Cyanophceae. Kryptogamen-Flora von Deutschland, österreich und der Schweiz 1932, Akademische Verlagsgesellschft, Leipzig. L. Rabenhorst (Ed.).
14. Humbert J.F., Duris-Latour D., Le Berre B., Giraudet H., Salençon M.J. Genetic diversity in Microcystis populations of a French storage reservoir assessed by sequencing of the 16S-23S rRNA intergenic spacer. Microbial Ecology 2005, 49(2):308-314.
15. Ichimura T. Media for blue-green algae. Methods in Algological Studies 1979, 294-305. Kyouritsu, Tokyo. K. Nishizawa, M. Chihara (Eds.).
16. Imai H., Chang K., Kusaba M., Nakano S. Temperature-dependent dominance of Microcystis (Cyanophyceae) species: M. aeruginosa and M. wesenbergii. Journal of Plankton Research 2009, 31(2):171-178.
17. Janse I., Meima M., Kardinaal W.E.A., Zwart G. High-resolution differentiation of cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Applied and Environment Microbiology 2003, 69(11):6634-6643.
18. Janse I., Kardinaal W.E.A., Meima M., Fastner J., Visser P.M., Zwart G. Toxic and nontoxic microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Applied and Environment Microbiology 2004, 70(7):3979-3987.
19. Kardinaal W.E.A., Tonk L., Janse I., Hol S., Slot P., Huisman J., Visser P.M. Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis. Applied and Environment Microbiology 2007, 73(9):2939-2946.
20. Komárek J., Anagnostidis K. Modern approach to the classification system of Cyanophytes. 2. Chroococcales. Archiv für Hydrobiologie, Supplement 1986, 72(Algological Studies 43):157-226.
21. Komárek J., Anagnostidis K. Modern approach to the classification system of Cyanophytes. 4. Nostocales. Archiv für Hydrobiologie, Supplement 1989, 82(Algological Studies 56):247-345.
22. Komárek J. A review of water-bloom forming Microcystis species, with regard to populations from Japan. Archiv für Hydrobiologie, Supplement 1991, 92:115-127.
23. Kondo R., Yoshida T., Yuki Y., Hiroishi S. DNA-DNA reassociation among a bloom-forming cyanobacterial genus, Microcystis. Int. J. Syst. Evol. Microbiol. 2000, 50(2):767-770.
24. Kurmayer R., Kutzenberger T. Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Applied and Environment Microbiology 2003, 69(11):6723-6730.
25. Leuko S., Goh F., Ibáñezz-Peral R., Burns B.P., Walter M.R., Neilan B.A. Lysis efficiency of standard DNA extraction methods for Halococcus spp. in an organic rich environment. Extremophiles 2008, 12(2):301-308.
26. MacKintosh C., Beattie K.A., Klumpp S., Cohen P., Codd G.A. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Letters 1990, 264(2):187-192.
27. Moisander P.H., Lehman P.W., Ochiai M., Corum S. Diversity of Microcystis aeruginosa in the Klamath River and San Francisco Bay delta, California, USA. Aquatic Microbial Ecology 2009, 57(1):19-31.
28. Namikoshi M., Rinehart K.L., Sakai R., Stotts R.R., Dahlem A.M., Beasley V.R., Carmichael W.W., Evans W.R. Identification of 12 Hepatotoxins from a Homer Lake bloom of the cyanobacteria Microcystis-aeruginosa, Microcystis-Viridis, and Microcystis-Wesenbergii - 9 new microcystins. Journal of Organic Chemistry 1992, 57(3):866-872.
29. Neilan B.A. Identification and phylogenetic analysis of toxigenic cyanobacteria by multiplex randomly amplified polymorphic DNA PCR. Applied and Environment Microbiology 1995, 61(6):2286-2291.
30. Neilan B.A., Jacobs D., Del Dot T., Blakall L.L., Hawkins P.R., Cox P.T., Goodman A.E. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. International Journal of Systematic Bacteriology 1997, 47(3):693-697.
31. Nishiwaki-Matsushima R., Ohta T., Nishiwaki S., Suganuma M., Kohyama K., Ishikawa T., Carmichael W.W., Fujiki H. Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. Journal of Cancer Research and Clinical Oncology 1992, 118(6):420-424.
32. Nishizawa T., Nishizawa A., Asayama M., Harada K., Shirai M. Diversity within the microcystin biosynthetic gene clusters among the genus Microcystis. Microbes and Environments 2007, 22(4):380-390.
33. Otsuka S., Suda S., Li R., Watanabe M., Oyaizu H., Matsumoto S., Watanabe M.M. 16S rDNA sequences and phylogenetic analyses of Microcystis strains with and without phycoerythrin. FEMS Microbiology Letters 1998, 164(1):119-124.
34. Otsuka S., Suda S., Li R., Watanabe M., Oyaizu H., Matsumoto S., Watanabe M.M. Characterization of morphospecies and strains of the genus Microcystis (Cyanobacteria) for a reconsideration of species classification. Psychological Research 1999, 47(3):189-197.
35. Otsuka S., Suda S., Li R.H., Watanabe M., Oyaizu H., Matsumoto S., Watanabe M.M. Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiology Letters 1999, 172(1):15-21.
36. Otsuka S., Suda S., Li R.H., Matsumoto S., Watanabe M.M. Morphological variability of colonies of Microcystis morphospecies in culture. Journal of General and Applied Microbiology 2000, 46(1):39-50.
37. Otsuka S., Suda S., Shibata S., Oyaizu H., Matsumoto S., Watanabe M.M. A proposal for the unification of five species of the cyanobacterial genus Microcystis Kutzing ex Lemmermann 1907 under the Rules of the Bacteriological Code. International Journal of Systematic and Evolutionary Microbiology 2001, 51(3):873-879.
38. Rasmussen R. Quantification on the light cycler. Rapid Cycle Real-Time PCR, Methods and Applications 2001, 21-34. Spring Press, Germany. S. Meuer, C.T. Wittwer, K. Nakagawara (Eds.).
39. Sabart M., Pobel D., Latour D., Robin J., Salençon M.J., Humbert J.F. Spatiotemporal changes in the genetic diversity in French bloom-forming populations of the toxic cyanobacterium, Microcystis aeruginosa. Environmental Microbiology Reports 2009, 1(4):263-272.
40. Shirai M., Takamura Y., Sakuma H., Kojima M., Nakano M. Toxicity and delayed type hypersensitivity caused by Microcystis blooms from Lake Kasumigaura. Microbiology and Immunology 1986, 30(7):731-735.
41. Sivonen K., Jones G. Cyanobacterial toxins. Toxic Cyanobacteria in Water 1999, 41-111. E & FN Spon, London. I. Chorus, J. Bartram (Eds.).
42. Speksnijder A.G.C.L., Kowalchuk G.A., De Jong S., Kline E., Stephen J.R., Laanbroekm H.J. Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Applied and Environment Microbiology 2001, 67:469-472.
43. Tan W., Liu Y., Wu Z., Lin S., Yu G., Yu B., Li R.H. cpcBA-IGS as an effective marker to characterize Microcystis wesenbergii (Komárek) Komárek in Kondrateva (cyanobacteria). Harmful Algae 2010, 9:607-612.
44. Tanabe Y., Kasai F., Watanabe M.M. Multilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosa. Microbiology 2007, 153:3695-3703.
45. Thompson J.D., Higgins D.G., Gibson T.J. Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22(22):4673-4680.
46. Tillett D., Neilan B.A. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. Journal of Psychology 2000, 36(1):251-258.
47. Untergasser A., Nijveen H., Rao X., Bisseling T., Geurts R., Leunissen J.A. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research 2007, 35(Web Server issue):W71-W74.
48. Van Gremberghe I., Leliaert F., Mergeay J., Vanormelingen P., Van der Gucht K., Debeer A.E., Lacerot G., De Meester L., Vyverman W. Lack of phylogeographic structure in the freshwater cyanobacterium Microcystis aeruginosa suggests global dispersal. PLoS ONE 2011, 6(5):e19561.
49. Watanabe M.F., Harada K., Matsuura K., Watanabe M., Suzuki M. Heptapeptide toxin production during the batch culture of two Microcystis species (Cyanobacteria). Journal of Applied Phycology 1989, 1(2):161-165.
50. Wilson A.E., Sarnelle O., Neilan B.A., Salmon T.P., Gehringer M.M., Hay M.E. Genetic variation of the bloom-forming cyanobacterium Microcystis aeruginosa within and among lakes: Implications for harmful algal blooms. Applied and Environment Microbiology 2005, 71(10):6126-6133.
51. Wintzingerode F.V., Göbel U.B., Stackebrandt E. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiology Review 1997, 21:213-229.
52. Xu Y., Wu Z.X., Yu B.S., Peng X., Yu G.L., Wei X.H., Wang G.X., Li R.H. Non-microcystin producing Microcystis wesenbergii (Komárek) Komárek (cyanobacteria) presenting a main waterbloom-forming species in Chinese waters. Environmental Pollution 2008, 156:162-167.
53. Yoshida T., Maki M., Okamoto H., Hiroishi S. Coordination of DNA replication and cell division in cyanobacteria Microcystis aeruginosa. FEMS Microbiology Letters 2005, 251(1):149-154.
54. Yoshida M., Yoshida T., Takashima Y., Hosoda N., Hiroishi S. Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiology Letters 2007, 266(1):49-53.
55. Yoshida M., Yoshida T., Satomi M., Takashima Y., Hosoda N., Hiroishi S. Intra-specific phenotypic and genotypic variation in toxic cyanobacterial Microcystis strains. Journal of Applied Microbiology 2008, 105(2):407-415.
56. Yoshizawa S., Matsushima R., Watanabe M.F., Harada K., Ichihara A., Carmichael W.W., Fujiki H. Inhibition of protein phosphatases by microcystins and nodularin associated with hepatotoxicity. Journal of Cancer Research and Clinical Oncology 1990, 116(6):609-614.
57. Zweifel U.L., Hagström Å. Total counts of marine-bacteria include a large fraction of non-nucleoid-containing bacteria (Ghosts). Applied and Environment Microbiology 1995, 61(6):2180-2185.