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Abstract:

Cells of Halamphora luciae were isolated from the mudflat of the Bahía Blanca estuary. Unialgal axenic cultures were grown in f/2 with limiting concentrations of N or P and in f/2 medium deprived of one or both macronutrients. On the one hand, limited macronutrient supply did not affect growth rate, but final cell yield was lower than in the complete medium. On the other hand, N or P deprivation reduced growth rates as well as final cell yield in the stationary phase. P deficiency enhanced the secretion of soluble extracellular polymeric substances (EPS), the percentage and speed of gliding cells, as well as the activity of alkaline phosphatase, especially after a previous prolonged P starvation. Regarding the morphology of the frustules, P deprivation reduced areola size but did not alter cell biovolume. N deficiency had a deleterious effect on the motility of the cells, and reduced the secretion of soluble EPS and cell biovolume. After incubation in N-deprived media for 10 days, cells exhibited enhanced protease activity. © 2016 International Phycological Society.

Registro:

Documento: Artículo
Título:Changes in motility and induction of enzymatic activity by nitrogen and phosphate deficiency in benthic Halamphora luciae (Bacillariophyceae) from Argentina
Autor:Daglio, Y.; Maidana, N.I.; Matulewicz, M.C.; Rodríguez, M.C.
Filiación:Departamento de Química Orgánica-CIHIDECAR (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 3er piso. (1428), Buenos Aires, Argentina
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4to piso. (1428), Buenos Aires, Argentina
IBBEA (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4to piso. (1428), Buenos Aires, Argentina
Palabras clave:Alkaline phosphatase; Biovolume; EPS; Frustule morphology; Halamphora; Motility; Nitrogen and phosphorus deficiency; Protease
Año:2016
Volumen:55
Número:5
Página de inicio:493
Página de fin:505
DOI: http://dx.doi.org/10.2216/15-134.1
Título revista:Phycologia
Título revista abreviado:Phycologia
ISSN:00318884
CODEN:PYCOA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00318884_v55_n5_p493_Daglio

Referencias:

  • Abdullahi, A., Underwood, G.J.C., Gretz, M., Extracellular matrix assembly in diatoms (Bacillariophyceae). V. Environmental effects on polysaccharide synthesis in the model diatom Phaeodactylum (2006) Journal of Phycology, 42, pp. 363-378
  • Alcoverro, T., Conte, E., Mazzella, L., Production of mucilage by the Adriatic epipelic diatom Cylindroteca closterium (Bacillariophyceae) under nutrient limitation (2000) Journal of Phycology, 36, pp. 1087-1095
  • Alipanah, L., Rohloff, J., Winge, P., Bones, A.M., Brembu, T., Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum (2015) Journal of Experimental Botany, 66, pp. 6281-6296
  • Apoya-Horton, M.D., Yin, L., Underwood, G.J.C., Gretz, M.R., Movement modalities and responses to environmental changes of the mudflat diatom Cylindrotheca closterium (Bacillariophyceae) (2006) Journal of Phycology, 42, pp. 379-390
  • Armbretch, L., Roughan, M., Rossi, V., Schaeffer, A., Davies, P., Waite, A., Armand, L., Phytoplankton composition under contrasting oceanographic conditions: Upwelling and downwelling (eastern Australia) (2014) Continental Shelf Research, 75, pp. 54-67
  • Battarbee, E.W., Diatom analysis (1986) Handbook of Holocene Palaeoecology and Palaeohydrology, pp. 527-570. , Ed. by B. E. Berglund, J. Wiley & Sons, New York
  • Brandini, F.P., Silva, E.T., Pellizzari, F.M., Fonseca, A., Fernandes, L.F., Production and biomass accumulation of periphytic diatoms growing on glass slides during a 1-year cycle in a subtropical estuarine environment (Bay of Paranagua, southern Brazil) (2001) Marine Biology, 138, pp. 163-171
  • Charney, J., Tomarelli, R., A colorimetric method for the determination of the proteolytic activity of duodenal juice (1947) Journal of Biological Chemistry, 171, pp. 501-505
  • Chiovitti, A., Bacic, A., Burke, J., Wetherbee, R., Heterogeneous xylose-rich glycans are associated with extracellular glycoproteins from the biofouling diatom Craspedostauros australis (Bacillariophyceae) (2003) European Journal of Phycology, 38, pp. 351-360
  • Chiovitti, A., Higgins, M.J., Harper, R., Wetherbee, R., Bacic, A., The complex polysaccharides of the raphid diatom Pinnularia viridis (Bacillariophyceae) (2003) Journal of Phycology, 39, pp. 543-554
  • Chiovitti, A., Dugdale, T.M., Wetherbee, R., Diatom adhesives: Molecular and mechanical properties (2006) Biological Adhesives, pp. 79-103. , Ed. by A. M. Smith & J. A. Callow, Springer-Verlag, Berlin, Germany
  • Cohn, S.A., Disparti, N.C., Environmental factors influencing diatom cell motility (1994) Journal of Phycology, 30, pp. 818-828
  • Cohn, S.A., Farrell, J., Munro, J., Ragland, R., Weitzell, R., Wibisono, B., The effect of temperature and mixed species composition on diatom motility and adhesion (2003) Diatom Research, 18, pp. 225-243
  • Cohn, S.A., Bahena, M., Davis, J., Ragland, R., Rauschenberg, C., Smith, B., Characterisation of the diatom photophobic response to high irradiance (2004) Diatom Research, 196, pp. 167-179
  • Consalvey, M., Paterson, D.M., Underwood, G.J.C., The ups and downs of life in a benthic biofilm: Migration of benthic diatoms (2004) Diatom Research, 19, pp. 181-202
  • Cooksey, B., Cooksey, K., Chemical signal-response in diatoms of the genus Amphora (1988) Journal of Cell Science, 91, pp. 523-529
  • Coquillé, N., Jan, G., Moreira, A., Morin, S., Use of diatom motility features as endpoints of metolachlor toxicity (2015) Aquatic Toxicology, 158, pp. 202-210
  • De Brouwer, J.F.C., Stal, L.J., Daily fluctuations of exopolymer in cultures of the benthic diatoms Cylindrotheca closterium and Nitzschia sp. (Bacillariophyceae) (2002) Journal of Phycology, 38, pp. 464-472
  • De Brouwer, J.F.C., Wolfstein, K., Stal, L.J., Physical characterization and diel dynamics of different fractions of extracellular polysaccharides in an axenic culture of a benthic diatom (2002) European Journal of Phycology, 37, pp. 37-44
  • De Brouwer, J.F.C., Neu, L.J., Stal, L.J., On the function of secretion of extracellular polymeric substances by benthic diatoms and their role in intertidal mudflats: A review of recent insights and views (2006) Functioning of Microphytobenthos in Estuaries, pp. 45-61. , Ed. by J. C. Kromkamp, J. F. C. de Brouwer, G. F. Blanchard, R. M. Forster & V. Créach, Royal Netherlands Academy of Arts and Sciences, Amsterdam
  • Decho, A., Microbial biofilms in intertidal systems: An overview (2000) Continental Shelf Research, 20, pp. 1257-1273
  • Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., Colorimetric method for determination of sugar and related substances (1956) Analytical Chemistry, 28, pp. 350-356
  • Dyhrman, S.T., Palenik, B., A characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi (2003) Journal of Plankton Research, 25, pp. 1-11
  • Dyhrman, S.T., Jenkins, B., Rynearson, T., Saito, M., Mercier, M., Alexander, H., Whitney, L., Heithoff, A., The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response (2012) PlosOne
  • Eixler, S., Karsten, U., Selig, U., Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cells and its dependence on phosphate supply (2006) Phycologia, 45, pp. 53-60
  • Ezequiel, J., Laviale, M., Frankenbach, S., Cartaxana, P., Serôdio, J., Photoacclimation state determines the photobehaviour of motile microalgae: The case of a benthic diatom (2015) Journal of Experimental Marine Biology and Ecology, 468, pp. 11-20
  • Gonzalez, M., Parra, O., Cifuentes, A., Técnicas de cultivo de microalgas en el laboratorio (1995) Manual de Métodos Ficológicos, pp. 238-239. , Ed. by K. Alveal, M. E. Ferrario, E. Oliveira & E. Sar, A. Pinto SA, Concepción, Chile
  • Guerrini, F., Cangini, M., Boni, L., Metabolic responses of the diatom Achnanthes brevipes (Bacillariophyceae) to nutrient limitation (2000) Journal of Phycology, 36, pp. 882-890
  • Guillard, R.R.L., Culture of phytoplankton for feeding marine invertebrates (1975) Culture of Marine Invertebrate Animals, pp. 26-60. , Ed. by W. L. Smith & M. H. Chanley, Plenum Press, New York
  • Hasle, G.R., Fryxell, G.A., Diatoms: Cleaning and mounting for light and electron microscopy (1970) Transactions of the American Microscopical Society, 89, pp. 469-474
  • Hernández, I., Whitton, B.A., Retention of p-nitrophenol and 4-methylumbelliferone by marine macroalgae and implications for measurement of alkaline phosphatase activity (1996) Journal of Phycology, 32, pp. 819-825
  • Hernández, I., Niell, X., Whitton, B.A., Phosphatase activity of benthic marine algae. An overview (2002) Journal of Applied Phycology, 14, pp. 475-487
  • Hoppe, H.G., Gocke, K., Koppe, R., Begler, C., Bacterial growth and primary production along a north-south transect of the Atlantic Ocean (2002) Nature (London), 416, pp. 168-171
  • Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., Darzins, A., Microalgal triacylglycerols as feedstocks for biofuel production: Perspectives and advances (2008) Plant Journal, 4, pp. 621-639
  • Leandro, S., Gil, M.C., Delgadillo, I., Partial characterisation of exopolysaccharides exudated by planktonic diatoms maintained in batch cultures (2003) Acta Oecologica, 24, pp. S49-S55
  • Leonardos, N., Geider, R., Responses of elemental and biochemical composition of Chaetoceros muelleri to growth under varying light and nitrate: Phosphate supply ratios and their influence on critical N:P (2004) Limnology and Oceanography, 49, pp. 2105-2114
  • Lev, S., Crossett, B., Cha, S.Y., Desmarini, D., Li, C., Chayakulkeeree, M., Wilson, C.F., Djordjevic, J.T., Identification of Aph1, a phosphateregulated, secreted, and vacuolar acid phosphatase in Cryptococcus neoformans (2014) MBio, 5 (5), p. e0164914
  • Levkov, Z., Amphora sensu lato (2009) Diatoms of Europe: Diatoms of the European Inland Waters and Comparable Habitats, 5, p. 916. , Ed. by H. Lange-Bertalot. A. R. Gantner Verlag, Ruggell, Liechtenstein
  • Levitan, O., Dinamarca, J., Zelzion, E., Lun, D., Guerra, L.T., Kim, M.K., Kim, J., Falkowski, P., Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress (2015) Proceedings of the National Academy of Sciences of the United States of America, 112, pp. 412-417
  • Leynaert, A., Longphuirt, N.S., Claquin, P., Chauvaud, L., Ragueneau, O., No limit? The multiphasic uptake of silicic acid by benthic diatoms (2009) Limnology and Oceanography, 54, pp. 571-576
  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent (1951) Journal of Biological Chemistry, 193, pp. 265-275
  • Lundkvist, M., Gangelhof, U., Lunding, J., Flindt, M.R., Production and fate of extracellular polymeric substances produced by benthic diatoms and bacteria: A laboratory study (2007) Estuarine Coastal Shelf Science, 75, pp. 337-346
  • Lynn, S.G., Kilham, S., Kreeger, D., Interlandi, S.J., Effect of nutrient availability on the biochemical and elemental stoichiometry in the fresh water diatom Stephanodiscus minutulus (Bacillariophyceae) (2000) Journal of Phycology, 36, pp. 510-522
  • Magaletti, E., Urbani, R., Sist, P., Ferrari, C.R., Cicero, A.M., Abundance and chemical characterization of extracellular carbohydrates released by the marine diatom Cylindrotheca fusiformis under N and P limitation (2004) European Journal of Phycology, 39, pp. 133-142
  • Martin, P., Van Mooy, B.A.S., Heithoff, A., Dyhrman, S.T., Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana (2011) ISME Journal, 5, pp. 1057-1060
  • McLachlan, D., Brownlee, C., Taylor, A., Geider, R., Underwood, G.J.C., Light-induced motile responses of the estuarine benthic diatoms Navicula perminuta and Cylindrotheca closterium (Bacillariophyceae) (2009) Journal of Phycology, 45, pp. 592-599
  • Middleburg, J.J., Barranguet, C., Boschker, H.T., Herman, P.M., Moens, T., Heip, C.H., The fate of intertidal microphytobenthos carbon: An in situ 13C-labelling study (2000) Limnology and Oceanography, 45, pp. 1224-1234
  • Mitbavkar, S., Anil, A.C., Vertical migratory rhythms of benthic diatoms in a tropical intertidal sand flat: Influence of irradiance and tides (2004) Marine Biology, 145, pp. 9-20
  • Molino, P.J., Wetherbee, R., The biology of biofouling diatoms and their role in the development of microbial slimes (2008) Biofouling, 24, pp. 365-379
  • Mulholland, M.R., Lee, C., Peptide hydrolysis and the uptake of dipeptides by phytoplankton (2009) Limnology and Oceanography, 54, pp. 856-868
  • Mulholland, M.R., Glibert, P., Berg, G., Van Heukelem, L., Pantoja, S., Lee, C., Extracellular amino acid oxidation by microplankton: A cross-ecosystem comparison (1998) Aquatic Microbial Ecology, 15, pp. 141-152
  • Mulholland, M.R., Lee, C., Glibert, P., Extracellular enzyme activity and uptake of carbon and nitrogen along an estuarine salinity and nutrient gradient (2003) Marine Ecology Progress Series, 258, pp. 3-17
  • Mulholland, M.R., Boneillo, G., Minor, E.C., A comparison of N and C uptake during brown tide (Aureococcus anophagefferens) blooms from two coastal bays on the east coast of the USA (2004) Harmful Algae, 3, pp. 361-376
  • Myklestad, S., Release of extracellular products by phytoplankton with special emphasis on polysaccharides (1995) Science of the Total Environment, 165, pp. 155-164
  • Myklestad, S., Haug, A., Production of carbohydrates by the marine Chaetoceros affinis var willei (Gran) Hustedt. I. Effect of the concentration of nutrients in the culture medium (1972) Journal of Experimental Marine Biology and Ecology, 9, pp. 125-136
  • Myklestad, S., Holm-Hansen, O., Varum, K.M., Volcani, B.E., Rate of release of extracellular amino acids and carbohydrates from the marine diatom Chaetoceros affinis (1989) Journal of Plankton Research, 11, pp. 763-773
  • Nielsen, P.H., Jahn, P., Extraction of EPS (1999) Microbial Extracellular Polymeric Substances: Characterization, Structure and Function, pp. 49-72. , Ed. by J. Wingender, T. R. Neu, H. C. Flemming, Springer, Berlin, Germany
  • Palenik, B., Morel, F.M., Amino acid utilization by marine phytoplankton: A novel mechanism (1990) Limnology and Oceanography, 35, pp. 260-269
  • Palenik, B., Morel, F.M., Comparison of cell-surface Lamino acid oxidases from several marine phytoplankton (1990) Marine Ecology Progress Series, 59, pp. 195-201
  • Palenik, B., Kieber, D.J., Morel, F.M., Dissolved organic nitrogen use by phytoplankton: The role of cell-surface enzymes (1989) Biological Oceanography, 6, pp. 347-354
  • Pantoja, S., Lee, C., Cell-surface oxidation of amino acids in seawater (1994) Limnology and Oceanography, 39, pp. 1718-1726
  • Patel, A.B., Fukami, K., Nishijima, T., Regulation of seasonal variability of aminopeptidase activities in surface and bottom of Uranouchi Inlet, Japan (2000) Aquatic Microbial Ecology, 21, pp. 139-149
  • Penna, A., Berluti, S., Penna, N., Magnani, M., Influence of nutrient ratios on the in vitro extracellular polysaccharide production by marine diatoms from the Adriatic Sea (1999) Journal of Plankton Research, 21, pp. 1681-1690
  • Pérez-Lloréns, L., Benítez, E., Vergara, J., Berges, J., Characterization of ptoteolytic enzyme activities in macroalgae (2003) European Journal of Phycology, 38, pp. 55-64
  • Perry, M.J., Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in oligotrophic waters of central North-Pacific (1976) Limnology and Oceanography, 21, pp. 88-107
  • Pistocchi, R., Trigari, G., Serrazanetti, G.P., Taddei, P., Monti, G., Palamidesi, S., Guerrini, F.A., Borgatti, A.R., Chemical and biochemical parameters of cultured diatoms and bacteria from the Adriatic Sea as possible biomarkers of mucilage production (2005) Science of the Total Environment, 353, pp. 287-299
  • Popovich, C.A., Marcovecchio, J.E., Spatial and temporal variability of phytoplankton and environmental factors in a temperate estuary of South America (Atlantic coast, Argentina) (2008) Continental Shelf Research, 28, pp. 236-244
  • Popovich, C.A., Damiani, C., Constenla, D., Martínez, A.M., Freije, H., Giovanardi, M., Pancaldi, S., Leonardi, P.I., Neochloris oleoabundans grown in enriched natural seawater for biodiesel feedstock: Evaluation of its growth and biochemical composition (2012) Bioresource Technology, 114, pp. 287-293
  • Powell, N., Shilton, A., Chistia, Y., Pratt, S., Towards a luxury uptake process via microalgae - Defining the polyphosphate dynamics (2009) Water Research, 43, pp. 4207-4213
  • Pulz, O., Gross, W., Valuable products from biotechnology of microalgae (2004) Applied Microbiology and Biotechnology, 65, pp. 635-648
  • Reynolds, C.S., Phytoplankton periodicity: The interactions of form, function and environmental variability (1984) Freshwater Biology, 14, pp. 111-142
  • Ruddy, G., Turley, C.M., Jones, T.E.R., Ecological interaction and sediment transport on an intertidal mudflat I: Evidence for a biologically mediated sediment-water interface (1998) Sedimentary Processes in the Intertidal Zone, pp. 135-148. , Ed. by K. S. Black, D. M. Paterson & A. Cramp, Geological Society, Special Publications, London
  • Saburova, M., Polikarpov, I., Diatom activity within soft sediments: Behavioural and physiological processes (2003) Marine Ecology Progress Series, 251, pp. 115-126
  • Sala, M., Karner, M., Arin, L., Marrasé, C., Measurement of ectoenzyme activities as an indication of inorganic nutrient imbalance in microbial communities (2001) Aquatic Microbial Ecology, 23, pp. 301-311
  • Sarthou, G., Timmermans, K.R., Blain, S., Tréguer, P., Growth physiology and fate of diatoms in the ocean: A review (2005) Journal of Sea Research, 53, pp. 25-42
  • Scholz, B., Liebezeit, G., Growth responses of 25 benthic marine Wadden Sea diatoms isolated from the Solthörn tidal flat (southern North Sea) in relation to varying culture conditions (2012) Diatom Research, 27, pp. 65-73
  • Smith, D., Underwood, G.J.C., Exopolymer production by intertidal epipelic diatoms (1998) Limnology and Oceanography, 43, pp. 1578-1591
  • Staats, N., Stal, L.J., Mur, L.R., Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: Effects of nutrient conditions (2000) Journal of Experimental Marine Biology and Ecology, 249, pp. 13-27
  • Stoecker, D., Autio, R., Rintala, J.M., Kuosa, H., Ectocellular enzyme activity associated with filamentous cyanobacteria (2005) Aquatic Microbial Ecology, 40, pp. 151-161
  • Sun, J., Liu, D., Geometric models for calculating cell biovolume and surface area for phytoplankton (2003) Journal of Plankton Research, 25, pp. 1331-1346
  • Underwood, G.J.C., Paterson, D., The importance of extracellular carbohydrate production by marine epipelic diatoms (2003) Advances in Botanical Research, 40, pp. 183-233
  • Underwood, G.J.C., Boulcott, M., Raines, C., Waldron, K., Environmental effects on exopolymer production by marine benthic diatoms: Dynamics, changes in composition, and pathways of production (2004) Journal of Phycology, 40, pp. 293-304
  • Urbani, R., Magaletti, E., Sist, P., Cicero, A.M., Extracellular carbohydrates released by the marine diatoms Cylindrotheca closterium, Thalassiosira pseudonana and Skeletonema costatum: Effect of P-depletion and growth status (2005) Science of the Total Environment, 353, pp. 300-306
  • Van Duyl, F.C., De Winder, B., Kop, A.J., Wollenzien, U., Tidal coupling between carbohydrate concentrations and bacterial activities in diatom-inhabited intertidal mudflats (1999) Marine Ecology Progress Series, 191, pp. 19-32
  • Van Mooy, B.A.S., Fredricks, H.F., Pedler, B.E., Dyhrman, S.T., Karl, D.M., Koblízek, M., Lomas, M.W., Webb, E., Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity (2009) Nature (London), 458, pp. 69-72
  • Witkowski, A., Brehm, U., Palińska, K., Rhiel, E., Swarmlike migratory behaviour in the laboratory of a pennate diatom isolated from North Sea sediments (2012) Diatom Research, 27, pp. 95-100
  • Wood, A.M., Everroad, R.C., Wingard, L.M., Measuring growth rates in microalgal cultures (2005) Algal Culturing Techniques, pp. 269-286. , Ed. by R. A. Andersen, Elsevier Academic Press, San Diego, California
  • Yamamoto, T., Suzuki, M., Kim, K., Asaoka, S., Growth and uptake kinetics of phosphate by benthic microalga Nitzschia sp isolated from Hiroshima Bay, Japan (2012) Phycological Research, 60, pp. 223-228

Citas:

---------- APA ----------
Daglio, Y., Maidana, N.I., Matulewicz, M.C. & Rodríguez, M.C. (2016) . Changes in motility and induction of enzymatic activity by nitrogen and phosphate deficiency in benthic Halamphora luciae (Bacillariophyceae) from Argentina. Phycologia, 55(5), 493-505.
http://dx.doi.org/10.2216/15-134.1
---------- CHICAGO ----------
Daglio, Y., Maidana, N.I., Matulewicz, M.C., Rodríguez, M.C. "Changes in motility and induction of enzymatic activity by nitrogen and phosphate deficiency in benthic Halamphora luciae (Bacillariophyceae) from Argentina" . Phycologia 55, no. 5 (2016) : 493-505.
http://dx.doi.org/10.2216/15-134.1
---------- MLA ----------
Daglio, Y., Maidana, N.I., Matulewicz, M.C., Rodríguez, M.C. "Changes in motility and induction of enzymatic activity by nitrogen and phosphate deficiency in benthic Halamphora luciae (Bacillariophyceae) from Argentina" . Phycologia, vol. 55, no. 5, 2016, pp. 493-505.
http://dx.doi.org/10.2216/15-134.1
---------- VANCOUVER ----------
Daglio, Y., Maidana, N.I., Matulewicz, M.C., Rodríguez, M.C. Changes in motility and induction of enzymatic activity by nitrogen and phosphate deficiency in benthic Halamphora luciae (Bacillariophyceae) from Argentina. Phycologia. 2016;55(5):493-505.
http://dx.doi.org/10.2216/15-134.1