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http://dx.doi.org/10.4490/algae.2018.33.11.25

Polyphasic delimitation of a filamentous marine genus, Capillus gen. nov. (Cyanobacteria, Oscillatoriaceae) with the description of two Brazilian species  

Caires, Taiara A. (Programa de Pos-Graduacao em Botanica, Universidade Estadual de Feira de Santana)
Lyra, Goia de M. (Laboratorio de Algas Marinhas (LAMAR), Instituto de Biologia, Universidade Federal da Bahia)
Hentschke, Guilherme S. (Universidade Luterana do Brasil (ULBRA))
da Silva, Aaron Matheus S. (Laboratorio de Algas Marinhas (LAMAR), Instituto de Biologia, Universidade Federal da Bahia)
de Araujo, Valter L. (Laboratorio de Algas Marinhas (LAMAR), Instituto de Biologia, Universidade Federal da Bahia)
Sant'Anna, Celia L. (Instituto de Botanica, Nucleo de Pesquisa em Ficologia)
Nunes, Jose Marcos de C. (Laboratorio de Algas Marinhas (LAMAR), Instituto de Biologia, Universidade Federal da Bahia)
Publication Information
ALGAE / v.33, no.4, 2018 , pp. 291-304 More about this Journal
Abstract
Lyngbya C. Agardh ex Gomont is a nonheterocytous cyanobacterial genus whose evolutionary history is still poorly known. The traditionally defined Lyngbya has been demonstrated to be polyphyletic, including at least five distinct clades, some of which have been proposed as new genera. Intraspecific diversity is also clearly underestimated in Lyngbya due to the lack of unique morphological characters to differentiate species. In this study, we describe the new genus Capillus T. A. Caires, C. L. Sant'Anna et J. M. C. Nunes from benthic marine environments, including two new Brazilian species (here described as C. salinus T. A. Caires, C. L. Sant'Anna et J. M. C. Nunes, and C. tropicalis T. A. Caires, C. L. Sant'Anna et J. M. C. Nunes), and two species yet to be described, one of them from India (Capillus sp. 2.1), and the other from United States of America, based on strain PCC 7419. Capillus species presented cross-wise diagonal fragmentation, assisted or not by necridic cells, which has not been previously mentioned for Lyngbya. Ultrastructural analyses showed that C. salinus and C. tropicalis have numerous gas vesicles, which are rarely described for benthic marine species. The new genus formed a well-supported clade, and the D1-D1' and Box B secondary structures of internal transcribed spacer also supported the proposal of its new species. These findings help to clarify the diversity of species in the Lyngbya complex and the taxonomy of the group, and highlight the need of further floristic surveys in tropical coastal environments, which remain poorly studied.
Keywords
Brazil; Cyanobacteria; diversity; new genus; polyphasic evaluation;
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1 Engene, N., Rottacker, E. C., Kastovsky, J., Byrum, T., Choi, H., Ellisman, M. H., Komarek, J. & Gerwick, W. H. 2012. Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int. J. Syst. Evol. Microbiol. 62(Pt. 5):1171-1178.   DOI
2 Fiore, M. F., Moon, D. H., Tsai, S. M., Lee, H. & Trevors, J. T. 2000. Miniprep DNA isolation from unicellular and filamentous cyanobacteria. J. Microbiol. Methods 39:159-169.   DOI
3 Genuario, D. B., Vaz, M. G. M. V., Hentschke, G. S., Sant'Anna, C. L. & Fiore, M. F. 2015. Halotia gen. nov., a phylogenetically and physiologically coherent cyanobacterial genus isolated from marine coastal environments. Intern. J. Syst. Evol. Microbiol. 65:663-675.   DOI
4 Komarek, J. 2018. Delimitation of the family Oscillatoriaceae (Cyanobacteria) according to the modern polyphasic approach (introductory review). Braz. J. Bot. 41:449-456.   DOI
5 Komarek, J. & Anagnostidis, K. 2005. Cyanoprokaryota-2. Teil/2nd part: Oscillatoriales. In Budel, B., Gartner, G., Krienitz, L. & Schagerl, M. (Eds.) Susswasserflora von Mitteleuropa 19 ⁄ 778 2. Elsevier/Spektrum, Heidelberg, pp. 1-759.
6 Komarek, J., Kastovsky, J., Mares, J. & Johansen, J. R. 2014. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86:295-335.
7 Komarek, J., Zapomelova, E., Smarda, J., Kopecky, J., Rejmankova, E., Woodhouse, J., Neilan, B. A. & Komarkova, J. 2013. Polyphasic evaluation of Limnoraphis robusta, a water-bloom forming cyanobacterium from Lake Atitlan, Guatemala, with a description of Limnoraphis gen. nov. Fottea 13:39-52.   DOI
8 Posada, D. & Buckley, T. R. 2004. Model selection and model averaging in phylogenetics: analysis advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53:793-808.   DOI
9 Nylander, J. A. A. 2008. MrModeltest 2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
10 Porta, D. & Hernandez-Marine, M. 2005. Structural and ultrastructural characterization of several culture strains assigned to Oscillatoria and Lyngbya (Cyanophyta/Cyanoprokaryota/Cyanobacteria). Algol. Stud. 117:349-370.   DOI
11 Rehakova, K., Johansen, J. R., Casamatta, D. A., Xuesong, L. & Vincent, J. 2007. Morphological and molecular characterization of selected desert soil cyanobacteria: three species new to science including Mojavia pulchra gen. et sp. nov. Phycologia 46:481-502.   DOI
12 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.
13 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.   DOI
14 Werner, V. R., Cabezudo, M. M., Neuhaus, E. B., Caires, T. A., Sant'Anna, C. L., Azevedo, M. T. P., Malone, C., Gama, W. A. Jr., Santos, K. R. S. & Menezes, M. 2017. Cyanophyceae in Lista de Especies da Flora do Brasil. Jardim Botanico do Rio de Janeiro. Available from: http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB108025. Accessed Aug 27, 2017.
15 Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.   DOI
16 Stoyanov, P., Moten, D., Mladenov, R., Dzhambazov, B. & Teneva, I. 2014. Phylogenetic relationships of some filamentous cyanoprokaryotic species. Evol. Bioinform. Online 10:39-49.
17 Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542.   DOI
18 Sambrook, J. F. & Russell, D. W. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, 2100 pp.
19 Baeta-Neves, M. H. C. 1991. Estudo das Cianoficeas Marinhas Bentonicas da Regiao de Cabo Frio (Estado do Rio de Janeiro, Brasil). II-Hormogonae. Rev. Bras. Biol. 52:641-659.
20 Birnboim, H. C. & Doly, J. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7:1513-1518.   DOI
21 Boyer, S. L., Johansen, J. R., Flechtner, V. R. & Howard, G. L. 2002. Phylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species based on sequence analysis of the 16S rRNA gene and associated 16S-23S ITS region. J. Phycol. 38:1222-1235.   DOI
22 Brito, A., Ramos, V., Mota, R., Lima, S., Santos, A., Vieira, J., Vieira, C. P., Kastovsky, J., Vasconcelos, V. M. & Tamagnini, P. 2017. Description of new genera and species of marine cyanobacteria from the Portuguese Atlantic coast. Mol. Phylogenet. Evol. 111:18-34.   DOI
23 Caires, T. A., de Mattos Lyra, G., Hentschke, G. S., de Gusmao Pedrini, A., Sant'Anna, C. L. & de Castro Nunes, J. M. 2018. Neolyngbya gen. nov. (Cyanobacteria, Oscillatoriaceae): a new filamentous benthic marine taxon widely distributed along the Brazilian Coast. Mol. Phylogenet. Evol. 120:196-211.   DOI
24 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(Pt. 2):481-496.   DOI
25 Caires, T. A., Sant'Anna, C. L. & de Castro Nunes, J. M. C. 2013. A new species of marine benthic cyanobacteria from the infralittoral of Brazil: Symploca infralitoralis sp. nov. Braz. J. Bot. 36:159-163.   DOI
26 Castenholz, R. W., Rippka, R. & Herdman, M. 2001. Formgenus VII. Lyngbya. Oxygenic photosynthetic bacteria. In Boone, D. R., Castenholz, R. W. & Garrity, G. M. (Eds.) Bergey's Manual of Systematic Bacteriology. Springer, New York, pp. 473-599.
27 Gomont, M. 1892. Monographie des Oscillariees (Nostocacees Homocystees). Deuxième partie. - Lyngbyees. Ann. Sci. Nat. Bot. Ser. 7. 16:91-264.
28 Hentschke, G. S., Johansen, J. R., Pietrasiak, N., Fiore, M. F., Rigonato, J., Sant'Anna, C. L. & Komarek, J. 2016. Phylogenetic placement of Dapisostemon gen. nov. and Streptostemon, two tropical heterocytous genera (Cyanobacteria). Phytotaxa 245:129-143.   DOI
29 Hentschke, G. S., Johansen, J. R., Pietrasiak, N., Rigonato, J., Fiore, M. F. & Sant'Anna, C. L. 2017. Komarekiella atlantica gen. et sp. nov. (Nostocaceae, Cyanobacteria): a new subaerial taxon from the Atlantic Rainforest and Kauai, Hawaii. Fottea 17:178-190.   DOI
30 Lane, D. J. 1991. 16S/23S rRNA sequencing. In Stackebrandt, E. & Goodfellow, M. (Eds.) Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons, Chichester, pp. 115-175.
31 Lipkin, Y. & Silva, P. C. 2002. Marine algae and seagrasses of the Dahlak Archipelago, southern Red Sea. Nova Hedwigia 75:1-90.   DOI
32 Martins, M. D. & Branco, L. H. Z. 2016. Potamolinea gen. nov. (Oscillatoriales, Cyanobacteria): a phylogenetically and ecologically coherent cyanobacterial genus. Int. J. Syst. Evol. Microbiol. 66:3632-3641.   DOI
33 Mau, B., Newton, M. A. & Larget, B. 1999. Bayesian phylogenetic inference via Markov chain Monte Carlo methods. Biometrics 55:1-12.   DOI
34 McGregor, G. B. & Sendall, B. C. 2014. Phylogeny and toxicology of Lyngbya wollei (Cyanobacteria, Oscillatoriales) from north-eastern Australia, with a description of Microseira gen. nov. J. Phycol. 51:109-119.
35 Sciuto, K. & Moro, I. 2016. Detection of the new cosmopolitan genus Thermoleptolyngbya (Cyanobacteria, Leptolyngbyaceae) using the 16S rRNA gene and 16S-23S ITS region. Mol. Phylogenet. Evol. 105:15-35.   DOI
36 Sant'Anna, C. L. 1995. Cyanophyceae marinhas bentonicas do Parque Estadual da Ilha do Cardoso, SP, Brasil. Hoehnea 22:197-216.
37 Sant'Anna, C. L. 1997. Cyanophyceae marinhas bentonicas da regiao de Ubatuba, SP, Brasil. Hoehnea 24:57-74.
38 Sant'Anna, C. L., Cordeiro-Marino, M., Braga, M. R. A. & Guimaraes, S. M. P. B. 1985. Cianoficeas marinhas bentonicas das Praias de Peruibe e dos Sonhos, Municipio de Itanhaem, Sao Paulo, Brasil. Rickia 12:89-112.
39 Sharp, K., Arthur, K. E., Gu, L., Ross, C., Harrison, G., Gunasekera, S. P., Meickle, T., Matthew, S., Luesch, H., Thacker, R. W., Sherman, D. H. & Paul, V. J. 2009. Phylogenetic and chemical diversity of three chemotypes of bloomforming Lyngbya species (Cyanobacteria: Oscillatoriales) from reefs of southeastern Florida. Appl. Environ. Microbiol. 75:2879-2888.   DOI
40 Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.   DOI
41 Stamatakis, A., Hoover, P. & Rougemont, J. 2008. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57:758-771.   DOI
42 Engene, N., Coates, R. C. & Gerwick, W. H. 2010. 16S rRNA gene heterogeneity in the filamentous marine cyanobacterial genus Lyngbya. J. Phycol. 46:591-601.   DOI
43 Crispino, L. M. B. & Sant'Anna, C. L. 2006. Cianobacterias marinhas bentonicas de ilhas costeiras do Estado de Sao Paulo, Brasil. Rev. Bras. Bot. 29:639-656.
44 Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. & Wilson, A. 2011. Geneious v6.0.6. Available from: http://www.geneious.com. Accessed Oct 8, 2017.
45 Engene, N., Choi, H., Esquenazi, E., Rottacker, E. C., Ellisman, M. H., Dorrestein, P. C. & Gerwick, W. H. 2011. Underestimated biodiversity as a major explanation for the perceived rich secondary metabolite capacity of the cyanobacterial genus Lyngbya. Environ. Microbiol. 13:1601-1610.   DOI
46 Engene, N., Gunasekera, S. P., Gerwick, W. H. & Paul, V. J. 2013. Phylogenetic inferences reveal a large extent of novel biodiversity in chemically rich tropical marine cyanobacteria. Appl. Environ. Microbiol. 79:1882-1888.   DOI
47 Komarek, J. 2016. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. Eur. J. Phycol. 51:346-353.   DOI
48 Jacinavicius, F. R., Gama, W. A. Jr., Azevedo, M. T. P. & Sant'Anna, C. L. 2012. Manual para cultivo de cianobacterias. Publicacoes Online do Instituto de Botanica de Sao Paulo, Sao Paulo, 32 pp.
49 Johansen, J. R., Kovacik, L., Casamatta, D. A., Fucikova, K. & Kastovsky, J. 2011. Utility of 16S-23S ITS sequence and secondary structure for recognition of intrageneric and intergeneric limits within cyanobacterial taxa: Leptolyngbya corticola sp. nov. (Pseudanabaenaceae, Cyanobacteria). Nova Hedwigia 92:283-302.   DOI
50 Karnovsky, M. J. 1965. A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J. Cell. Biol. 27:1A-149A.   DOI
51 Vaz, M. G. M. V., Genuario, D. B., Andreote, A. P. D., Malone, C. F. S., Sant'Anna, C. L., Barbiero, L. & Fiore, M. F. 2014. Pantanalinema gen. nov. and Alkalinema gen. nov.: novel pseudanabaenacean genera (Cyanobacteria) isolated from saline-alkaline lakes. Int. J. Syst. Evol. Microbiol. 65:298-308.
52 Muhlsteinova, R., Johansen, J. R., Pietrasiak, N., Martin, M. P., Osorio-Santos, K. & Warren, S. D. 2014. Polyphasic characterization of Trichocoleus desertorum sp. nov. (Pseudanabaenales, Cyanobacteria) from desert soils and phylogenetic placement of the genus Trichocoleus. Phytotaxa 163:241-261.   DOI
53 Mukherjee, C., Chowdhury, R., Sutradhar, T., Begam, M., Ghosh, S. M., Basak, S. K. & Ray, K. 2015. Parboiled rice effluent: a wastewater niche for microalgae and cyanobacteria with growth coupled to comprehensive remediation and phosphorus biofertilization. Algal Res. 19:225-236.
54 Neilan, B. A., Jacobs, D., Del Dot, T., Blackall, L. L., Hawkins, P. R., Cox, P. T. & Goodman, A. E. 1997. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int. J. Syst. Bacteriol. 47:693-697.   DOI
55 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. Appl. Environ. Microbiol. 69:5157-5169.   DOI