Abstract
Sphaerocavum is a typical planktonic coccoid cyanobacterium that co-occurs with Microcystis species, and it is commonly found in blooms. Sphaerocavum is a morphogenus distinguishable from Microcystis, as it presents hollow colonies and two-plane cell division. However, Sphaerocavum phylogenetic position based on marker gene(s) has not yet been established. Here, we combined morphological and molecular analyses to address the taxonomic and phylogenetic placement of Sphaerocavum isolated from Brazilian eutrophic lakes. Phylogenetic analysis revealed that Sphaerocavum and Microcystis clustered together in a well-established clade, thus not supporting the Sphaerocavum designation as a divergent genus. The type strain and isolated lineages from Brazilian tropical regions were grouped in the ITS phylogenetic analysis apart from other Microcystis strains. As such, although the infrageneric recognition of Microcystis by molecular markers is still unclear, our analyses strongly indicate that Sphaerocavum must be considered as a morphotype of Microcystis. Thus, taking together our morphological and molecular analyses, we propose the inclusion of Sphaerocavum within the genus Microcystis. In addition, we suggest that the strains used in this study should be named as Microcystis brasiliensis (Azevedo & Sant’Anna) Rigonato et al. comb. nov., with CCIBt3094 as the type strain.




Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Allen, M. M., 1968. Simple conditions for growth of unicellular blue- green algae on plates. Journal of Phycology 4: 1–4.
Altschul, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman, 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.
Azevedo, M. T. P. & Sant’Anna, C. L. 2003. Sphaerocavum, a new genus of planktic Cyanobacteria from continental water bodies in Brazil. Algological Studies 79: 79–92.
Baker, J. A., B. Entsch, B. A. Neilan & D. B. McKay, 2002. Monitoring changing toxigenicity of a cyanobacterial bloom by molecular methods. Applied and Environmental Microbiology 68: 6070–6076.
Boyer, S. L., V. R. Flechtner & Jr Johansen, 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. Molecular Biology and Evolution 18(6): 1057–1069.
Carvalho, L. R. D., F. Pipole, V. R. Werner, D. H. Laughinghouse, A. C. M. D. Camargo, M. Rangel, K. Konno & C. L. Sant’Anna, 2008. A toxic cyanobacterial bloom in an urban coastal lake, Rio Grande do Sul State, Southern Brazil. Brazilian Journal of Microbiology 39(4): 761–769.
Cohan, F. M. & D. M. Ward, 2005. Microbial diversity in hot spring cyanobacterial mats: pattern and prediction. In: Inskeep, W. P. & , T. R. McDermott (eds), Geothermal biology and geochemistry in Yellowstone National Park: proceeding of the Thermal Biology Institute workshop, Yellowstone National Park, WY, October 2003. 352 pp. Montana State University Publications. Bozeman, MT, USA.
Comas, A., A. Moreira González & L. Toledo, 2010. Adiciones a la ora de algas y cianoprocariotas dulciacuícolas de Cuba. Algas 44: 20–29.
Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.
Ewing, B. & P. Green, 1998. Base-calling of automated sequencer traces using Phred: II. Error probabilities. Genome Research 8: 186–194.
Ewing, B., L. Hillier, M. C. Wendl & P. Green, 1998. Base-calling of automated sequencer traces using Phred: I. Accuracy assessment. Genome Research 8: 175–185.
Fonseca, B. M. & C. E. D. M. Bicudo, 2008. Phytoplankton seasonal variation in a shallow stratified eutrophic reservoir (Garças Pond, Brazil). Hydrobiologia 600(1): 267–282.
Fonseca, B. M., C. Ferragut, A. Tucci, L. O. Crossetti, F. Ferrari, D. D. C. Bicudo, C. L. Sant’Anna & C. E. D. M. Bicudo, 2014. Biovolume of Cyanobacteria and algae from Brazilian tropical reservoirs with different trophic status. Hoehnea 41(1): 9–30.
Fox, G. E., J. D. Wisotzkey & P. Jurtshuk Jr, 1992. How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. International Journal of Systematic Bacteriology 42: 166–170.
Gaget, V., M. Welker, R. Rippka, & de N. T. Marsac, 2015. A polyphasic approach leading to the revision of the genus Planktothrix (Cyanobacteria) and its type species, P. agardhii, and proposal for integrating the emended valid botanical taxa, as well as three new species, Planktothrix paucivesiculata sp. nov. ICNP, Planktothrix tepida sp. nov. ICNP, and Planktothrix serta sp. nov. ICNP, as genus and species names with nomenclatural standing under the ICNP. Systematic and Applied Microbiology 38(3): 141–158.
Gordon, D., C. Abajian & P. Green, 1998. Consed: a graphical tool for sequence finishing. Genome Research 8: 195–202.
Guillard, R. R. & C. J. Lorenzen, 1972. Yellow-green algae with chlorophyllide c. Journal of Phycology 8: 10–14.
Hoffmann, L., J. Komárek & J. Kaštovský, 2005. System of cyanoprokaryotes (cyanobacteria)—state in 2004. Algological Studies (Cyanobacterial Research 6) 117:95–115.
Huelsenbeck, J. P. & F. Ronquist, 2005. Bayesian analysis of molecular evolution using MrBayes. In Statistical methods in molecular evolution (pp. 183–226). Springer, New York.
Iteman, I., R. Rippka, N. T. de Marsac & M. Herdman, 2000. Comparison of conserved structural and regulatory domains within divergent 16S rRNA–23S rRNA spacer sequences of cyanobacteria. Microbiology 146(6): 1275–1286.
Komárek J. & Anagnostidis K. 1998. Cyanoprokaryota1. Chroococcales. In: Ettl H., Gärtner G., Heynig H. & Mollenhauer D. (eds), Süsswasserflora von Mitteleuropa 19/1, p. 548, Gustav Fischer, Jena-Stuttgart- Lübeck-Ulm.
Komárek, J., 2016. Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia 764(1): 259–270.
Komárek, J., J. Komárková-Legnerová, C. L. Sant’Anna, M. T. P. Azevedo & P. A. C. Senna, 2002. Two common Microcystis species (Chroococcales, Cyanobacteria) from tropical America, including M. panniformis sp. nov. Cryptogamie, Algologie 23(2): 159–177.
Kováčik, L., J. Jezberová, J. Komárková, J. Kopecký & J. Komárek, 2011. Ecological characteristics and polyphasic taxonomic classification of stable pigment-types of the genus Chroococcus (Cyanobacteria). Preslia 83: 145–166.
Lane, D. J., 1991. 16S/23S rRNA sequencing. In Stackebrandt, E. & M. Goodfellwon (eds), Nucleic acid techniques in bacterial systematics. Wiley, Chichester: 115–175.
Lepère, C., A. Wilmotte & B. Meyer, 2000. Molecular diversity of Microcystis strains (Cyanophyceae, Chroococcales) based on 16S rDNA sequences. Systematics and Geography of Plants Fresh Water Algae: Taxonomy, Biogeography and Conservation 70(2): 275–283.
Lodders, N., E. Stackebrandt & U. Nübel, 2005. Frequent genetic recombination in natural populations of the marine cyanobacterium Microcoleus chthonoplastes. Environmental Microbiology 7(3): 434–442.
Lowe, T. M. & S. R. Eddy, 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25: 955–964.
Mazard, S., M. Ostrowski, F. Partensky & D. J. Scanlan, 2012. Multilocus sequence analysis, taxonomic resolution and biogeography of marine Synechococcus. Environmental Microbiology 14(2): 372–386.
Mendoza-Carbajal, L. H., 2016. El género Sphaerocavum y dominancia de S. brasiliense y Microcystis wesenbergii (Microcystaceae, Cyanophyceae) en la floración algal de la laguna Huacachina, Perú. Revista Peruana de Biología 23(1): 53–60.
Neilan, B. A., D. Jacobs, T. del Dot, L. L. Blackall, P. R. Hawkins, P. T. Cox & A. E. Goodman, 1997. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. International Journal of Systematic Bacteriology 47: 693–697.
Nguyen, V., Y. Tanabe, H. Matsuura, K. Kaya & M. M. Watanabe, 2012. Morphological, biochemical and phylogenetic assessments of water bloom forming tropical morphospecies of Microcystis (Chroococcales, Cyanobacteria). Phycological Research 60(3): 208–222.
Nogueira, I. S., W. A. Gama Jr. & E. B. D’Alessandro, 2011. Cianobactérias planctônicas de um lago artificial urbano na cidade de Goiânia, GO. Revista Brasileira de Botânica 34(4): 575–592.
Otsuka, S., S. Suda, R. Li, M. Watanabe, H. Oyaizu, S. Matsumoto & M.M. Watanabe, 1998. 16S rDNA Sequences and phylogenetic analyses of Microcystis strains with and without phycoerythrin. FEMS Microbiology Letters 164: 119–124
Otsuka, S., S. Suda, R. Li, M. Watanabe, H. Oyaizu, S. Matsumoto & M. M. Watanabe, 1999. Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiology Letters 172(1): 15–21.
Otsuka, S., S. Suda, S. Shibata, H. Oyaizu, S. Matsumoto & M. M. Watanabe, 2001. A proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the rules of the Bacteriological Code. International Journal of Systematic and Evolutionary Microbiology 51(3): 873–879.
Otten, T. G. & H. W. Paerl, 2011. Phylogenetic inference of colony isolates comprising seasonal Microcystis blooms in Lake Taihu, China. Microbial Ecology 62(4): 907–918.
Salusso, M. M. & L. B. Moraña, 2014. Fitoplancton de embalses subtropicales del noroeste argentino. Gestión y Ambiente 17(1): 209–222.
Silva-Stenico, M. E., J. Rigonato, A. S. Lorenzi, M. T. P. Azevedo, C. L. Sant’Anna & M. F. Fiore, 2015. Bioactive Cyanopeptides Produced by Sphaerocavum brasiliense Strains (Cyanobacteria). Journal of the Brazilian Chemical Society 26(10):2088-2096.
Stamatakis, A., 2006. RaxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.
Tan, W., Y. Liu, Z. Wu, S. Lin, G. Yu, B. Yu & R. Li, 2010. cpcBA-IGS as an effective marker to characterize Microcystis wesenbergii (Komárek) Komárek in Kondrateva (cyanobacteria). HarmfulAlgae 9(6): 607–612.
Tanabe, Y., F. Kasai & M. M. Watanabe, 2007. Multilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosa. Microbiology 153(11): 3695–3703.
Taton, A., S. Grubisic, E. Brambilla, R. de Wit & A. Wilmotte, 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(9): 5157–5169.
Tillett, D., D. L. Parker & B. A. Neilan, 2001. Detection of toxigenicity by a probe for the microcystin synthetase A gene (mcyA) of the cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies. Applied and Environmental Microbiology 67(6): 2810–2818.
Vilgalys, R., 2003. Taxonomic misidentification in public DNA databases. New Phytologist 160(1): 4–5.
Wood, S. A., A. L. M. Crowe, J. G. Ruck & R. G. Wear, 2005. New records of planktonic cyanobacteria in New Zealand freshwaters. New Zealand Journal of Botany 43(2): 479–492.
Wu, Z. X., N. Q. Gan & L. R. Song, 2007. Genetic diversity: geographical distribution and toxin profiles of Microcystis strains (Cyanobacteria) in China. Journal of Integrative Plant Biology 49(3): 262–269.
Zapomělová, E., P. Hrouzek, T. Řezanka, J. Jezberová, K. Řeháková, D. Hisem & J. Komárková, 2011. Polyphasic characterization of Dolichospermum spp. and Sphaerospermopsis spp. (Nostocales, Cyanobacteria): morphology, 16S rRNA gene sequences and fatty acid and secondary metabolite profiles. Journal of Phycology 47(5): 1152–1163.
Zuker, M., 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31(13): 3406–3415.
Acknowledgements
The authors wish to thank Francisco Dini Andreote for English revisions and suggestions. J. Rigonato received a postdoctoral fellowship from the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES-PNPD20131744 USP/CENA program). W. A. Gama was supported by graduate scholarship FAPESP2012/16430-1. A. Giani acknowledges the financial support provided by CNPq and FAPEMIG.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: Eugen Rott, Allan Pentecost & Jan Mares / Aspects of cyanobacterial biogeography, molecular ecology, functional ecology and systematics
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rigonato, J., Sant’Anna, C.L., Giani, A. et al. Sphaerocavum: a coccoid morphogenus identical to Microcystis in terms of 16S rDNA and ITS sequence phylogenies. Hydrobiologia 811, 35–48 (2018). https://doi.org/10.1007/s10750-017-3312-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-017-3312-2


