Abstract
The taxonomy of four isolated strains of Anabaenopis elenkinii and A. arnoldii from North and South America were investigated using a polyphasic approach. The studied populations were collected from seven alkaline lakes of the Brazilian Pantanal and Nabor Carrillo Lake, Texcoco region (Mexico), between 2004 and 2012, where they frequently formed blooms during the dry season. The morphological plasticity of the populations, from natural and culture conditions, was described based on 200 individuals of each species. The 16S rRNA and the cpc-BA-IGS phylogenetic analyses show Anabaenopsis as a sister-taxon of Cyanospira. The Anabaenopsis clade has three strongly supported subclusters related to the origin of strains: Pantanal+Mexico, Kenya+Australia and one European clade. Although these data indicate that the currently known Anabaenopsis strains belong to more than one species, we are being conservative and not describing them as new species due to the lack of more molecular data. We highlight the need of a revision of the genus, considering also that Anabaenopsis sp. PCC 9215, the current reference strain used for the genus, is not identified as A. elenkinii and it is phylogenetically grouped with Anabaenopsis strains identified as A. circularis, A. arnoldii, A. nadsonii and A. elenkinii.
References
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https://doi.org/10.1111/j.1529-8817.1968.tb04667.x
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https://doi.org/10.1007/s00248-007-9304-4
Ballot, A., Fastner, J., Lentz, M. & Wiedner, C. (2010) First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany. Toxicon 56 (6): 964–971.
https://doi.org/10.1016/j.toxicon.2010.06.021
Ballot, A., Krienitz, L., Kotut, K., Wiegand, C. & Pflugmacher, S. (2005) Cyanobacteria and cyanobacterial toxins in the alkaline crater lakes Sonachi and Simbi, Kenya. Harmful Algae 4: 139–150.
https://doi.org/10.1016/j.hal.2004.01.001
Ballot, A., Krienitz, L., Kotut, K., Wiegand, C., Metcalf, J.S. Codd, G.A. & Pflugmacher, S. (2004) Cyanobacteria and Cyanobacterial toxins in three alkaline Rift Valley lakes of Kenya–Lakes Bogoria, Nakuru and Elmenteita. Journal of Plankton Research 26: 925–935.
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https://doi.org/10.1016/j.ympev.2016.12.032
Hentschke, G.S., Johansen, J.R., Pietrasiak, N., Fiore, M.F., Rigonato, J., Sant’Anna, C.L. & Komárek, J. (2016) Phylogenetic placement of Dapisostemon gen. nov. and Streptostemon, two tropical heterocytous genera (Cyanobacteria). Phytotaxa 245 (2): 129–143.
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https://doi.org/10.1099/00221287-148-2-481
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Komárek, J. (2005) Phenotypic diversity of the heterocytous cyanoprokaryotic genus Anabaenopsis. Czech Phycology, Olomouc 5: 1–35.
Komárek, J. (2010) Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera. Hydrobiologia 639: 231–243.
https://doi.org/10.1007/s10750-009-0030-4
Kotai, J. (1972) Instructions for preparation of modified nutrient solution Z8 for Algae. Norwegian Institute for Water Research, Oslo, Norway, pp. 1–5.
Lanaras, T. & Cook, C.M. (1994) Toxin extraction from an Anabaenopsis milleri-dominated bloom. Science of the Total Environment 142 (3): 163–169.
<a href="https://doi.org/10.1016/0048-9697(94)90324-7">https://doi.org/10.1016/0048-9697(94)90324-7</a>
Malone, C.F.S., Santos, K.R.S. & Sant’Anna, C.L. (2012) Algas e cianobactérias de ambientes extremos do Pantanal Brasileiro. Oecologia Australis 16: 745–755.
https://doi.org/10.4257/oeco.2012.1604.02
Miller, V.V. (1923) K sistematike roda Anabaena Bory [Zur Systematik der Gattung Anabaena Bory]. Arch. Russk. Protistol 2: 116–126.
Mohamed, Z. & Shehri, A. (2009) Microcystin-producing blooms of Anabaenopsis arnoldi in a potable mountain lake in Saudi Arabia. FEMS Microbiology Ecology 69: 98–105.
https://doi.org/10.1111/j.1574-6941.2009.00683.x
Morales, E.A., Wetzel, C.E., Rivera, S.F., Novais, M.H., Hoffmann, L. & Ector, L. (2014) Craticula strelnikoviana sp. nov. and Craticula guaykuruorum sp. nov. (Bacillariophyta) from South American saline lakes. Nova Hedwigia 143: 223–238.
Mourão, G.M., Ishii I.H. & Campos, Z.M.S. (1988) Alguns fatores limmnológicos relacionados com a ictiofauna de baías e salinas do Pantanal da Nhecolândia, MS, Brasil. Acta Limnologica Brasiliensia 2: 181–198.
Neilan, B.A., Jacobs, D., Dot, T.D., 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. International Journal of Systematic Bacteriology 47: 693–697.
https://doi.org/10.1099/00207713-47-3-693
Neilan, B.A., Jacobs, D., Goodman, A.E., Cox, P.T. & Hawkins, P. (1995) Genetic diversity and phylogeny of toxic cyanobacteria determined by DNA polymorphism within the phycocyanin locus. Applied and Environmental Microbiology 61: 3875–3583.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (12): 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Santos, K.R.S. & Sant’Anna, C.L. (2010) Cianobactérias de diferentes tipos de lagoas (“salina”, “salitrada” e “baía”) representativas do Pantanal da Nhecolândia, MS, Brasil. Brazilian Journal of Botany 33: 61–83.
https://doi.org/10.1590/S0100-84042010000100007
Santos, K.R.S., Jacinavicius, F.R. & Sant’Anna, C.L. (2011) Effects of the pH on growth and morphology of Anabaenopsis elenkinii Miller (Cyanobacteria) isolated from the alkaline shallow lake of the Brazilian Pantanal. Fottea 11 (1): 119–126.
https://doi.org/10.5507/fot.2011.012
Santos, K.R.S., Rocha, A.C.R. & Sant’Anna, C.L. (2012) Diatoms from shallow lakes in the Pantanal of Nhecolândia, Brazilian wetland. Oecologia Australis 16 (4): 795–808.
https://doi.org/10.4257/oeco.2012.1604.03
Santos, K.R.S., Sakamoto, A.Y., Neto, M.J., Barbiero, L. & Queiroz Neto, J.P. (2004) Ficoflora do Pantanal da Nhecolândia, MS, Brasil: um levantamento preliminar em três lagoas salinas e uma salitrada. In: Soriano, B.M.A., Sallis, S.M., Mourão, G.M. & Pellegrin, L.A. (Orgs.) Anais do IV Simpósio sobre Recursos Naturais e Sócio-econômicos do Pantanal. Corumbá (meio eletrônico).
Sili, C., Mascalchi, C. & Ventura, S. (2011) Evolutionary differentiation of the sister cyanobacterial genera Cyanospira Florenzano, Sili, Pelosi et Vincenzini and Anabaenopsis (Woloszy?ska) Miller in response to extreme life conditions. Fottea 11 (1): 107–117.
https://doi.org/10.5507/fot.2011.011
Smith, T.E. (2010) Revised list of algae from Arkansas, U.S.A. and new additions. International Journal on Algae 12 (3): 230–256.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.
https://doi.org/10.1093/molbev/mst197
Werner, V.R., Laughinghouse, IV H.D., Fiore, M.F., Sant’Anna, C.L., Hoff, C., Santos, K.R.d.S., Neuhaus, E.B., Molica, R.J.R., Honda, R.Y. & Echenique, R.O. (2012) Morphological and molecular studies of Sphaerospermopsis torques-reginae (Cyanobacteria, Nostocales) from South American water blooms. Phycologia 51: 228–238.
https://doi.org/10.2216/11-32.1
West, G.S. (1907) Report of the freshwater algae incl. phytoplankton of the Third Tanganyika Expedition. Journal of the Linnean Society. Botany 38: 81–197.
Wo?oszy?ska, J. (1912) Das Phytoplankton einiger javanischer Seen, mit Berücksichtigung des Sawa-Planktons. Bull. Acad. Sci. Cracovie, mat.-nat. ser. B 1912: 649–709.
https://doi.org/10.11646/phytotaxa.272.3.1
Allen, M.M. (1968) Simple conditions for growth of unicellular blue-green algae on plates. Journal of Phycology 4: 1–4.
https://doi.org/10.1111/j.1529-8817.1968.tb04667.x
Andreote, A.P.D., Dini-Andreote, F., Rigonato, J., Silva, G.M., Souza, B.C.E., Barbiero, L., Rezende-Filho, A.T. & Fiore, M.F. (2018) Contrasting the genetic patterns of microbial communities in soda lakes with and without cyanobacterial bloom. Frontiers in Microbiology 9: 244.
https://doi.org/10.3389/fmicb.2018.00244
Ballot, A., Dadheech, P.K., Haande, S. & Krienitz, L. (2008) Morphological and Phylogenetic Analysis of Anabaenopsis abijatae and Anabaenopsis elenkinii (Nostocales, Cyanobacteria) from Tropical Inland Water Bodies. Microbial Ecology 55 (4): 608–618.
https://doi.org/10.1007/s00248-007-9304-4
Ballot, A., Fastner, J., Lentz, M. & Wiedner, C. (2010) First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany. Toxicon 56 (6): 964–971.
https://doi.org/10.1016/j.toxicon.2010.06.021
Ballot, A., Krienitz, L., Kotut, K., Wiegand, C. & Pflugmacher, S. (2005) Cyanobacteria and cyanobacterial toxins in the alkaline crater lakes Sonachi and Simbi, Kenya. Harmful Algae 4: 139–150.
https://doi.org/10.1016/j.hal.2004.01.001
Ballot, A., Krienitz, L., Kotut, K., Wiegand, C., Metcalf, J.S. Codd, G.A. & Pflugmacher, S. (2004) Cyanobacteria and Cyanobacterial toxins in three alkaline Rift Valley lakes of Kenya–Lakes Bogoria, Nakuru and Elmenteita. Journal of Plankton Research 26: 925–935.
https://doi.org/10.1093/plankt/fbh084
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.
https://doi.org/10.1038/nmeth.2109
Genuario, D.B., Andreote, A.P.D., Vaz, M.G.M.V. & Fiore, M.F. (2017) Heterocyte-forming cyanobacteria from Brazilian saline-alkaline lakes. Molecular Phylogenetics and Evolution 109: 105–112.
https://doi.org/10.1016/j.ympev.2016.12.032
Hentschke, G.S., Johansen, J.R., Pietrasiak, N., Fiore, M.F., Rigonato, J., Sant’Anna, C.L. & Komárek, J. (2016) Phylogenetic placement of Dapisostemon gen. nov. and Streptostemon, two tropical heterocytous genera (Cyanobacteria). Phytotaxa 245 (2): 129–143.
https://doi.org/10.11646/phytotaxa.245.2.4
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 (2): 481–496.
https://doi.org/10.1099/00221287-148-2-481
Jeeji-Bai, N., Hegewald, E. & Soeder, C.J. (1980) Taxonomic studies on the genus Anabaenopsis (Wolosz.) Miller. In: Desikachary T.V. & Rajarao, V.N. (Eds.) Taxonomy of Algae. University of Madras, pp. 115–145.
Komárek, J. (2005) Phenotypic diversity of the heterocytous cyanoprokaryotic genus Anabaenopsis. Czech Phycology, Olomouc 5: 1–35.
Komárek, J. (2010) Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera. Hydrobiologia 639: 231–243.
https://doi.org/10.1007/s10750-009-0030-4
Kotai, J. (1972) Instructions for preparation of modified nutrient solution Z8 for Algae. Norwegian Institute for Water Research, Oslo, Norway, pp. 1–5.
Lanaras, T. & Cook, C.M. (1994) Toxin extraction from an Anabaenopsis milleri-dominated bloom. Science of the Total Environment 142 (3): 163–169.
<a href="https://doi.org/10.1016/0048-9697(94)90324-7">https://doi.org/10.1016/0048-9697(94)90324-7</a>
Malone, C.F.S., Santos, K.R.S. & Sant’Anna, C.L. (2012) Algas e cianobactérias de ambientes extremos do Pantanal Brasileiro. Oecologia Australis 16: 745–755.
https://doi.org/10.4257/oeco.2012.1604.02
Miller, V.V. (1923) K sistematike roda Anabaena Bory [Zur Systematik der Gattung Anabaena Bory]. Arch. Russk. Protistol 2: 116–126.
Mohamed, Z. & Shehri, A. (2009) Microcystin-producing blooms of Anabaenopsis arnoldi in a potable mountain lake in Saudi Arabia. FEMS Microbiology Ecology 69: 98–105.
https://doi.org/10.1111/j.1574-6941.2009.00683.x
Morales, E.A., Wetzel, C.E., Rivera, S.F., Novais, M.H., Hoffmann, L. & Ector, L. (2014) Craticula strelnikoviana sp. nov. and Craticula guaykuruorum sp. nov. (Bacillariophyta) from South American saline lakes. Nova Hedwigia 143: 223–238.
Mourão, G.M., Ishii I.H. & Campos, Z.M.S. (1988) Alguns fatores limmnológicos relacionados com a ictiofauna de baías e salinas do Pantanal da Nhecolândia, MS, Brasil. Acta Limnologica Brasiliensia 2: 181–198.
Neilan, B.A., Jacobs, D., Dot, T.D., 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. International Journal of Systematic Bacteriology 47: 693–697.
https://doi.org/10.1099/00207713-47-3-693
Neilan, B.A., Jacobs, D., Goodman, A.E., Cox, P.T. & Hawkins, P. (1995) Genetic diversity and phylogeny of toxic cyanobacteria determined by DNA polymorphism within the phycocyanin locus. Applied and Environmental Microbiology 61: 3875–3583.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (12): 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Santos, K.R.S. & Sant’Anna, C.L. (2010) Cianobactérias de diferentes tipos de lagoas (“salina”, “salitrada” e “baía”) representativas do Pantanal da Nhecolândia, MS, Brasil. Brazilian Journal of Botany 33: 61–83.
https://doi.org/10.1590/S0100-84042010000100007
Santos, K.R.S., Jacinavicius, F.R. & Sant’Anna, C.L. (2011) Effects of the pH on growth and morphology of Anabaenopsis elenkinii Miller (Cyanobacteria) isolated from the alkaline shallow lake of the Brazilian Pantanal. Fottea 11 (1): 119–126.
https://doi.org/10.5507/fot.2011.012
Santos, K.R.S., Rocha, A.C.R. & Sant’Anna, C.L. (2012) Diatoms from shallow lakes in the Pantanal of Nhecolândia, Brazilian wetland. Oecologia Australis 16 (4): 795–808.
https://doi.org/10.4257/oeco.2012.1604.03
Santos, K.R.S., Sakamoto, A.Y., Neto, M.J., Barbiero, L. & Queiroz Neto, J.P. (2004) Ficoflora do Pantanal da Nhecolândia, MS, Brasil: um levantamento preliminar em três lagoas salinas e uma salitrada. In: Soriano, B.M.A., Sallis, S.M., Mourão, G.M. & Pellegrin, L.A. (Orgs.) Anais do IV Simpósio sobre Recursos Naturais e Sócio-econômicos do Pantanal. Corumbá (meio eletrônico).
Sili, C., Mascalchi, C. & Ventura, S. (2011) Evolutionary differentiation of the sister cyanobacterial genera Cyanospira Florenzano, Sili, Pelosi et Vincenzini and Anabaenopsis (Woloszy?ska) Miller in response to extreme life conditions. Fottea 11 (1): 107–117.
https://doi.org/10.5507/fot.2011.011
Smith, T.E. (2010) Revised list of algae from Arkansas, U.S.A. and new additions. International Journal on Algae 12 (3): 230–256.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.
https://doi.org/10.1093/molbev/mst197
Werner, V.R., Laughinghouse, IV H.D., Fiore, M.F., Sant’Anna, C.L., Hoff, C., Santos, K.R.d.S., Neuhaus, E.B., Molica, R.J.R., Honda, R.Y. & Echenique, R.O. (2012) Morphological and molecular studies of Sphaerospermopsis torques-reginae (Cyanobacteria, Nostocales) from South American water blooms. Phycologia 51: 228–238.
https://doi.org/10.2216/11-32.1
West, G.S. (1907) Report of the freshwater algae incl. phytoplankton of the Third Tanganyika Expedition. Journal of the Linnean Society. Botany 38: 81–197.
Wo?oszy?ska, J. (1912) Das Phytoplankton einiger javanischer Seen, mit Berücksichtigung des Sawa-Planktons. Bull. Acad. Sci. Cracovie, mat.-nat. ser. B 1912: 649–709.