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ORIGINAL ARTICLES

Morphology, phylogeny, growth rate and nodularin production of Nodularia spumigena from Brazil

, , , & ORCID Icon
Pages 1095-1107 | Received 25 Oct 2016, Accepted 26 May 2017, Published online: 11 Aug 2017

References

  • Adamec F, Kaftan D, Nedbal L. 2005. Stress-induced filament fragmentation of Calothrix elenkinii (Cyanobacteria) is facilitated by death of high-fluorescence cells. Journal of Phycology 41:835–39. doi: 10.1111/j.1529-8817.2005.00104.x
  • Ahuja G, Khattar JS, Sarma TA. 2008. Interaction between carbon and nitrogen metabolism during akinete development in the cyanobacterium Anabaena torulosa. Journal of Basic Microbiology 48:125–29. doi: 10.1002/jobm.200700302
  • Alvarez SB, Bazán GI. 1994. Cianoficeas continentals de la provincia de la pampa (Argentina) – I. Revista de la Facultad de Agronomía 7:43–62.
  • Birnboim HC, Doly J. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Research 7:1513–23. doi: 10.1093/nar/7.6.1513
  • Blackburn SI, McCausland MA, Bolch CJS, Newman SJ, Jones GJ. 1996. Effect of salinity on growth and toxin production in cultures of the bloom-forming cyanobacterium Nodularia spumigena from Australian waters. Phycologia 35:511–22. doi: 10.2216/i0031-8884-35-6-511.1
  • Bolch CJS, Orr PT, Jones GJ, Blackburn SI. 1999. Genetic, morphological, and toxicological variation among globally distributed strains of Nodularia (Cyanobacteria). Journal of Phycology 35:339–55. doi: 10.1046/j.1529-8817.1999.3520339.x
  • Carmichael WW, An J. 1999. Using an enzyme linked immunosorbent assay (ELISA) and a protein phosphatase inhibition assay (PPIA) for the detection of microcystins and nodularins. Natural Toxins 7:377–85. doi: 10.1002/1522-7189(199911/12)7:6<377::AID-NT80>3.0.CO;2-8
  • Carmichael WW, Eschedor JT, Patterson GML, Moore RE. 1988. Toxicity and partial structure of a hepatotoxic peptide produced by the cyanobacterium Nodularia spumigena Mertens emend. L575 from New Zealand. Applied and Environmental Microbiology 54:2257–63.
  • Costa CM, Fóes GK, Odebrecht C, Poersh L, Wasielesky W. 2013. Impacto da cianobactéria Nodularia spumigena em cultivo de camarões marinhos em sistema de bioflocos. Reunião Latino Americana Sobre Algas Nocivas. 22 pages.
  • Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772. doi: 10.1038/nmeth.2109
  • Dias RA, Maurício GN, Bugoni L. 2017. Birds of the Patos Lagoon Estuary and adjacent coastal waters, Southern Brazil: species assemblages and conservation implications. Marine Biology Research 13:108–20. doi: 10.1080/17451000.2016.1209525
  • Ewing B, Green P. 1998. Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Research 8:186–94. doi: 10.1101/gr.8.3.186
  • Ewing B, Hillier L, Wendl MC, Green P. 1998. Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Research 8:175–85. doi: 10.1101/gr.8.3.175
  • Fay P, Lynn JA, Majer SC. 1984. Akinete development in the planktonic blue-green alga Anabaena circinalis. British Phycological Journal 19:163–73. doi: 10.1080/00071618400650171
  • Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–91. doi: 10.1111/j.1558-5646.1985.tb00420.x
  • Fujii K, Sivonen K, Adachi K, Noguchi K, Sano H, Hirayama K, et al. 1997. Comparative study of toxic and non-toxic cyanobacterial products: novel peptides from toxic Nodularia spumigena AV1. Tetrahedron Letters 38:5525–28. doi: 10.1016/S0040-4039(97)01192-1
  • Galat DL, Verdin JP, Sims LL. 1990. Large-scale patterns of Nodularia spumigena blooms in Pyramid Lake, Nevada, determined from Landsat imagery: 1972–1986. Hydrobiologia 197:147–64. doi: 10.1007/BF00026947
  • Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR. 1988. Evolutionary relationships among cyanobacteria and green chloroplasts. Journal of Bacteriology 170:3584–92. doi: 10.1128/jb.170.8.3584-3592.1988
  • Gordon D, Abajian C, Green P. 1998. Consed: a graphical tool for sequence finishing. Genome Research 8:195–202. doi: 10.1101/gr.8.3.195
  • Guillard RRL. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH, editors. Culture of Marine Invertebrate Animals. New York: Plenum, p 29–60.
  • Haraguchi L, Odebrecht C. 2014. Potentially toxic microalgae in a subtropical estuary and adjacent coast in Brazil with emphasis on the new record of Nodularia spumigena (32°S; 52°W). In: Kim HG, Reguera B, Hallegraeff GM, Lee CK, Han MS, Choi JK, editors. Proceedings of the 15th International Conference on Harmful Algae. Gyeongnam, South Korea: International Society for the Study of Harmful Algae, p 37–40.
  • Hašler P, Dvořák P, Ondřej V, Kitner M, Hloušková P, Poulíčková A. 2011. The importance of polyphasic approach in the comparative study on Nodularia Mertens ex Bornet et Flahault (Nostocales, Cyanobacteria). Preslia 83:167–82.
  • Hayes PK, Barker GLA. 1997. Genetic diversity within Baltic Sea populations of Nodularia (Cyanobacteria). Journal of Phycology 33:919–23. doi: 10.1111/j.0022-3646.1997.00919.x
  • Heresztyn T, Nicholson BC. 1997. Nodularin concentrations in Lakes Alexandrina and Albert, South Australia, during a bloom of the cyanobacterium (blue-green alga) Nodularia spumigena and degradation of the toxin. Environmental Toxicology 12: 273–82.
  • Hobson P, Fallowfield H. 2001. Effect of salinity on photosynthetic activity of Nodularia spumigena. Journal of Applied Phycology 13:493–99. doi: 10.1023/A:1012540928506
  • Hobson P, Fallowfield HJ. 2003. Effect of irradiance, temperature and salinity on growth and toxin production by Nodularia spumigena. Hydrobiologia 493:7–15. doi: 10.1023/A:1025447318487
  • Hobson P, Burch M, Fallowfield HJ. 1999. Effect of total dissolved solids and irradiance on growth and toxin production by Nodularia spumigena. Journal of Applied Phycology 11:551–58. doi: 10.1023/A:1008193918189
  • Honkanen RE, Dukelow M, Zwiller J, Moore RR, Khatra BS, Boynton AL. 1991. Cyanobacterial nodularin is a potent inhibitor of type 1 and type 2A protein phosphatases. Molecular Pharmacology 40:577–83.
  • Hübel H, Hübel M. 1980. Nitrogen fixation during blooms of Nodularia in coastal waters and backwaters of the Arkona Sea (Baltic Sea) in 1974. Internationale Revue der Gesamten Hydrobiologie und Hydrographie 65:793–808. doi: 10.1002/iroh.19800650605
  • 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 146:1275–86. doi: 10.1099/00221287-146-6-1275
  • Iteman I, Rippka R, Tandeau de Marsac N, Herdman M. 2002. rDNA analyses of planktonic heterocystous cyanobacteria, including members of the genera Anabaenopsis and Cyanospira. Microbiology 148:481–96. doi: 10.1099/00221287-148-2-481
  • Jodłowska S, Latała A. 2012. Mechanisms of photoaclimation on photosynthesis levels in cyanobacteria. In: Najafpour M, editor. Advances in Photosynthesis –Fundamental Aspects. Rijeka, Croatia: InTech, p 97–108.
  • Jones GJ, Blackburn SI, Parker NS. 1994. A toxic bloom of Nodularia spumigena Mertens in Orielton Lagoon, Tasmania. Australian Journal of Marine and Freshwater Research 45:787–800. doi: 10.1071/MF9940787
  • Kankaanpää HT, Holliday J, Schröder H, Goddard TJ, Fister R, Carmichael WW. 2005. Cyanobacteria and prawn farming in northern New South Wales, Australia – a case study on cyanobacteria diversity and hepatotoxin bioaccumulation. Toxicology and Applied Pharmacology 203:243–56. doi: 10.1016/j.taap.2004.04.012
  • Komárek J. 1985. Do all cyanophytes have a cosmopolitan distribution? Survey of the freshwater cyanophyte flora of Cuba. Algological Studies 71:359–86.
  • Komárek J. 1994. Current trends and species delimitation in the cyanoprokaryote taxonomy. Algological Studies 75:11–29.
  • Komárek J. 2013. Cyanoprokaryota – 3. Part 3: Heterocytous genera. In: Büdel B, Gärtner G, Krienitz L, Schagerl M, editors. Süßwasserflora von Mitteleuropa. Heidelberg: Springer/Spektrum, p 904–19.
  • Komárek J, Hübel M, Hübel H, Šmarda J. 1993. The Nodularia studies. 2. Taxonomy. Algological Studies 68:1–25.
  • Kopprio GA, Freije RH, Strüssmann CA, Kattner G, Hoffmeyer MS, Popovich CA, Lara RJ. 2010. Vulnerability of pejerrey Odontesthes bonariensis populations to climate change in pampean lakes of Argentina. Journal of Fish Biology 77:1856–66. doi: 10.1111/j.1095-8649.2010.02750.x
  • Laamanen MJ, Gugger MF, Lehtimäki JM, Haukka K, Sivonen K. 2001. Diversity of toxic and nontoxic Nodularia isolates (Cyanobacteria) and filaments from the Baltic Sea. Applied and Environmental Microbiology 67:4638–47. doi: 10.1128/AEM.67.10.4638-4647.2001
  • Lane DJ. 1991. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic Acid Techniques in Bacterial Systematics. Chichester: John Wiley and Sons, p 115–75.
  • Lehtimäki J, Moisander P, Sivonen K, Kononen K. 1997. Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Applied and Environmental Microbiology 63:1647–56.
  • Lehtimäki J, Lyra C, Suomalainen S, Sundman P, Rouhiainen L, Paulin L, et al. 2000. Characterization of Nodularia strains, cyanobacteria from brackish waters, by genotypic and phenotypic methods. International Journal of Systematic and Evolutionary Microbiology 50:1043–53. doi: 10.1099/00207713-50-3-1043
  • Lyra C, Laamanen M, Lehtimäki JM, Surakka A, Sivonen K. 2005. Benthic cyanobacteria of the genus Nodularia are non-toxic, without gas vacuoles, able to glide and genetically more diverse than planktonic Nodularia. International Journal of Systematic and Evolutionary Microbiology 55:555–68. doi: 10.1099/ijs.0.63288-0
  • Ma J, Lu N, Qin W, Xu R, Wang Y, Chen X. 2006. Differential responses of eight cyanobacterial and green algal species, to carbamate insecticides. Ecotoxicology and Environmental Safety 63:268–74. doi: 10.1016/j.ecoenv.2004.12.002
  • Mackinney G. 1941. Absorption of light by chlorophyll solutions. The Journal of Biological Chemistry 140:315–22.
  • Mazur-Marzec H, Żeglińska L, Pliński M. 2005. The effect of salinity on the growth, toxin production, and morphology of Nodularia spumigena isolated from the Gulf of Gdańsk, southern Baltic Sea. Journal of Applied Phycology 17:171–79. doi: 10.1007/s10811-005-5767-1
  • Mazur-Marzec H, Kaczkowska MJ, Blaszczyk A, Akcaalan R, Spoof L, Meriluoto J. 2013. Diversity of peptides produced by Nodularia spumigena from various geographical regions. Marine Drugs 11:1–19. doi: 10.3390/md11010001
  • McGregor GB, Stewart I, Sendall BC, Sadler R, Reardon K, Carter S, et al. 2012. First report of a toxic Nodularia spumigena (Nostocales/Cyanobacteria) bloom in sub-tropical Australia. I. Phycological and public health investigations. International Journal of Environmental Research and Public Health 9:2396–411. doi: 10.3390/ijerph9072396
  • Mohlin M, Wulff A. 2009. Interaction effects of ambient UV radiation and nutrient limitation on the toxic cyanobacterium Nodularia spumigena. Microbial Ecology 57:675–86. doi: 10.1007/s00248-008-9427-2
  • Moisander PH, Paerl HW. 2000. Growth, primary productivity, and nitrogen fixation potential of Nodularia spp. (Cyanophyceae) in water from a subtropical estuary in the United States. Journal of Phycology 36:645–58. doi: 10.1046/j.1529-8817.2000.99227.x
  • Myers JH, Beardall J, Allinson G, Salzman S, Robertson S, Gunthorpe L. 2011. Potential triggers of akinete differentiation in Nodularia spumigena (Cyanobacteriaceae) isolated from Australia. Hydrobiologia 671:165–80. doi: 10.1007/s10750-011-0714-4
  • Nehring S. 1993. Mortality of dogs associated with a mass development of Nodularia spumigena (Cyanophyceae) in a brackish lake at the German North Sea coast. Journal of Plankton Research 15:867–72. doi: 10.1093/plankt/15.7.867
  • Nübel U, Garcia-Pichel F, Muyzer G. 1997. PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology 63:3227–332.
  • Oliva MG, Lugo A, Alcocer J, Peralata L, Oseguera LA. 2009. Planktonic bloom-forming Nodularia in the saline Lake Alchichica, Mexico. Natural Resources and Environmental Issues 15:121–26.
  • Pacheco LA, Kunrath N, Costa CM, Costa LDF, Foes GK, Wasielesky W, Yunes JS. 2016. Identification of the toxic pentapeptide nodularin in a cyanobacterial bloom in a shrimp farm in South American Atlantic coast. Pharmaceutica Analytica Acta 7: e479. 3 pages.
  • Pandey KD, Kashyap AK. 1987. Factors affecting formation of spores (akinetes) in cyanobacterium Anabaena doliolum (AdS strain). Journal of Plant Physiology 127:123–34. doi: 10.1016/S0176-1617(87)80046-9
  • Pandey RK. 1989. Induction of akinete formation in Nodularia spumigena by temperature. Journal of Basic Microbiology 29:477–80. doi: 10.1002/jobm.3620290721
  • Pérez MC, Bonilla S, León L, Smarda J, Komárek J. 1999. A bloom of Nodularia báltica-spumigena group (Cyanobacteria) in a shallow coastal lagoon of Uruguay, South America. Algological Studies 93:91–101.
  • Popin RV, Rigonato J, Abreu VAC, Andreote APD, Silveira SB, Odebrecht C, Fiore MF. 2016. Draft genome assembly of the bloom-forming cyanobacterium Nodularia spumigena strain CENA596 in shrimp production ponds. Genome Announcements 4:e00466-16. 2 pages. doi: 10.1128/genomeA.00466-16
  • Repka S, Mehtonen J, Vaitomaa J, Saari L, Sivonen K. 2001. Effects of nutrients on growth and nodularin production of Nodularia strain GR8b. Microbial Ecology 42:606–13. doi: 10.1007/s00248-001-0026-8
  • Rinehart KL, Harada K, Namikoshi M, Chen C, Harvis CA, Munro MHG, et al. 1988. Nodularin, microcystin, and the configuration of Adda. Journal of the American Chemical Society 110:8557–58. doi: 10.1021/ja00233a049
  • Ronquist F, Huelsenbeck J. 2003. Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–74. doi: 10.1093/bioinformatics/btg180
  • Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular Cloning: a Laboratory Manual, 2nd edition. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 1626 pages.
  • Schattner P, Brooks AN, Lowe TM. 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Research 33:W686–89. doi: 10.1093/nar/gki366
  • Seaman MT, Ashton PJ, Williams WD. 1991. Inland salt waters of Southern Africa. Hydrobiologia 210:75–91. doi: 10.1007/BF00014324
  • Šmarda J, Komárek J, Čáslavska J, Hübel M. 1988. The Nodularia studies. 1. Introduction, fine structure. Algological Studies 50–53:109–29.
  • Suikkanen S, Laamanen M, Huttunen M. 2007. Long-term changes in summer phytoplankton communities of the open northern Baltic Sea. Estuarine, Coastal and Shelf Science 71:580–92. doi: 10.1016/j.ecss.2006.09.004
  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28:2731–39. doi: 10.1093/molbev/msr121
  • Taton A, Grubisic S, Brambilla E, De Wit R, Wilmotte A. 2003. Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Applied and Environmental Microbiology 69:5157–69. doi: 10.1128/AEM.69.9.5157-5169.2003
  • Taton A, Grubisic S, Ertz D, Hodgson DA, Piccardi R, Biondi N, et al. 2006. Polyphasic study of Antarctic cyanobacterial strains. Journal of Phycology 42:1257–70. doi: 10.1111/j.1529-8817.2006.00278.x
  • Van Buynder PG, Oughtred T, Kirkby B, Phillips S, Eaglesham G, Thomas K, Burch M. 2001. Nodularin uptake by seafood during a cyanobacterial bloom. Environmental Toxicology 16:468–71. doi: 10.1002/tox.10004
  • Voß B, Bolhuis H, Fewer DP, Kopf M, Möke F, Haas F, et al. 2013. Insights into the physiology and ecology of the brackish-water-adapted cyanobacterium Nodularia spumigena CCY9414 based on a genome-transcriptome analysis. Plos One 8(3):e60224. 22 pages. doi: 10.1371/journal.pone.0060224
  • Werner VR, Rosa ZM. 1992. Cyanophyceae da Estação Ecológica do Taim, Rio Grande do Sul, Brasil. Revista Brasileira de Biologia 52:481–502.
  • Wilmotte A. 1994. Molecular evolution and taxonomy of the cyanobacteria. In: Bryant DA, editor. The Molecular Biology of Cyanobacteria. Antwerp: Kluwer Academic Publishers, p 1–25.
  • Wood AM, Everroad RC, Wingard LM. 2005. Measuring growth rates in microalgal cultures. In: Andersen R, editor. Algal Culturing Techniques. Amsterdam: Elsevier Academic Press, p 269–85.
  • Yunes JS, De La Rocha S, Giroldo D, Silveira SB, Comin R, Bicho MS, et al. 2009. Release of carbohydrates and proteins by a subtropical strain of Raphidiopsis brookii (Cyanobacteria) able to produce saxitoxin at three nitrate concentrations. Journal of Phycology 45:585–91. doi: 10.1111/j.1529-8817.2009.00673.x
  • Zar JH. 2010. Biostatistical Analysis, 5th edition. Upper Saddle River, NJ: Pearson. 944 pages.
  • Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31:3406–15. doi: 10.1093/nar/gkg595

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