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Abstract:

The genus Pseudopedinella has been described as mixotrophic; however, ecological information about this algal stramenopile (Heterokonta) is unclear. We investigate the environmental conditions that determine the presence, abundance and bacterivory rates of this genus in freshwater systems. To this end we analyzed 54 water bodies with different limnological features distributed along a latitudinal and trophic gradient in northern Patagonia (Argentina) and the Antarctic Peninsula. In addition, 14 grazing experiments were carried out in order to estimate ingestion rates and impact on the bacterioplankton. Our results indicate that this genus is exclusively found in oligotrophic environments, and that it develops well in a wide range of temperatures. Average cell-specific grazing rate was 2.83 bacteria cell-1 h-1, with a maximum value of 6.74 bacteria ml-1 h-1. Interestingly, grazing increased with prey abundance and decreased with increasing nutrient availability. These patterns are common in highly bacterivorous protists that use phagotrophy as a main source of nutrient acquisition. Despite their usually low abundance (avg. 182 cells ml-1), this single genus was responsible for up to 24% (avg. 10%) of the total grazing impact exerted by all phagotrophs in these lakes. Overall, our results support the idea that Pseudopedinella is a highly bacterivorous group of freshwater protists, with the ability to develop well in oligotrophic conditions and with a potentially significant impact on bacterioplankton. © The authors 2016.

Registro:

Documento: Artículo
Título:Presence, abundance and bacterivory of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments
Autor:Gerea, M.; Saad, J.F.; Izaguirre, I.; Queimaliños, C.; Gasol, J.M.; Unrein, F.
Filiación:Laboratorio de Fotobiología, INIBIOMA, CONICET-Universidad Nacional Del Comahue, Quintral,1250, Bariloche, R8400FRD, Argentina
Departamento de Ecología, Genética y Evolución, IEGEBA, UBA-CONICET, Ciudad Universitaria, Buenos Aires, C1428EHA, Argentina
Institut de Ciències Del Mar, CSIC, Passeig Marítim de la Barceloneta, 37-49, Barcelona, Catalonia, 08003, Spain
Laboratorio de Ecología y Fotobiología Acuática, IIB-INTECH, UNSAM-CONICET, Av. Intendente Marino km 8,200, Chascomús, B7130IWA, Argentina
Palabras clave:Antarctic lakes; Bacterivory; Grazing rate; Patagonian lakes; Pseudopedinella
Año:2015
Volumen:76
Número:3
Página de inicio:219
Página de fin:232
DOI: http://dx.doi.org/10.3354/ame01780
Título revista:Aquatic Microbial Ecology
Título revista abreviado:Aquatic Microb. Ecol.
ISSN:09483055
CODEN:MMFWE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09483055_v76_n3_p219_Gerea

Referencias:

  • Biecheler, B., Observation de la capture et de la digestion des protes chez un peridinén vert (1936) C R Séances Soc Biol, 12, pp. 1173-1175
  • Bird, D.F., Kalff, J., Bacterial grazing by planktonic lake algae (1986) Science, 231, pp. 493-495
  • Callieri, C., Corno, G., Bertoni, R., Bacterial grazing by mixotrophic flagellates and Daphnia longispina: A comparison in a fishless alpine lake (2006) Aquat Microb Ecol, 42, pp. 127-137
  • Callieri, C., Modenutti, B., Queimaliños, C., Bertoni, R., Balseiro, E., Production and biomass of picophytoplankton and larger autotrophs in Andean ultraoligotrophic lakes: Differences in light harvesting efficiency in deep layers (2007) Aquat Ecol, 41, pp. 511-523
  • Carstensen, J., Heiskanen, A.S., Phytoplankton res pon - Ses to nutrient status: Application of a screening method to the northern Baltic Sea (2007) Mar Ecol Prog ser, 336, pp. 29-42
  • Carvalho, W.F., Granéli, E., Contribution of phagotrophy versus autotrophy to Prymnesium parvum growth under nitrogen and phosphorus sufficiency and deficiency (2010) Harmful Algae, 9, pp. 105-115
  • De Hoyos, C., Aldasoro, J.J., Toro, M., Comín, F.A., Specific composition and ecology of chrysophyte flagellates in Lake Sanabria (NW Spain) (1998) Hydrobiologia, 369-370, pp. 287-295
  • Epstein, S.S., Shiaris, M.P., Size-selective grazing of coastal bacterioplankton by natural assemblages of pigmented flagellates, colorless flagellates, and ciliates (1992) Microb Ecol, 23, pp. 211-225
  • Fenchel, T., Ecology of heterotrophic microflagellates (1982) II. Bioenergetics and Growth. Mar Ecol Prog ser, 8, pp. 225-231
  • Flöder, S., Hansen, T., Ptacnik, R., Energy-dependent bacterivory in Ochromonas minima - A strategy promot-ing the use of substitutable resources and survival at insufficient light supply (2006) Protist, 157, pp. 291-302
  • Flynn, K.J., Stoecker, D.K., Mitra, A., Raven, J.A., Misuse of the phytoplankton-zooplankton dichotomy: The need to assign organisms as mixotrophs within plankton functional types (2013) J Plankton Res, 35, pp. 3-11
  • Frías-López, J., Thompson, A., Waldbauer, J., Chisholm, S.W., Use of stable isotope-labelled cells to identify active grazers of picocyanobacteria in ocean surface waters (2009) Environ Microbiol, 11, pp. 512-525
  • Gasol, J.M., Pinhassi, J., Alonso-Sáez, L., Ducklow, H., Towards a better understanding of microbial carbon flux in the sea (2008) Aquat Microb Ecol, 53, pp. 21-38
  • Gerea, M., (2013) La Implicancia de Las Algas Mixotróficas en la Trama Trófica Microbiana de Lagos Someros Oligotróficos de Patagonia Norte y de la Península Antártica (Argentina), , PhD thesis, Universidad Nacional del Comahue
  • Gerea, M., Queimalinos, C., Schiaffino, M.R., Izaguirre, I., Forn, I., Massana, R., Unrein, F., In situ prey selection of mixotrophic and heterotrophic flagellates in Antarctic oligotrophic lakes: An analysis of the digestive vacuole content (2013) J Plankton Res, 35, pp. 201-212
  • Guiry, M.D., Guiry, G.M., (2015) AlgaeBase, , www.algaebase.org, National University of Ireland, Galway
  • Hartmann, M., Grob, C., Tarran, G.A., Martin, A.P., Burkill, P.H., Scanlan, D.J., Zubkov, M.V., Mixotrophic basis of Atlantic oligotrophic ecosystems (2012) Proc Natl Acad Sci USA, 109, pp. 5756-5760
  • Havskum, H., Riemann, B., Ecological importance of bacterivorous, pigmented flagellates (mixotrophs) in the Bay of Aarhus, Denmark (1996) Mar Ecol Prog ser, 137, pp. 251-263
  • Hearing, F., Pseudopedinella, un género de las criso - Fíceas de agua dulce (1984) Ann Biol, 2, pp. 101-106
  • Hibberd, D.J., Ultrastructure of the Chrysophyceae: Phylogenetic implications and taxonomy (1986) Chrysophytes: Aspect and Problems, pp. 23-36. , In: Kristiansen J, Andersen RA (eds), Cambridge University Press, Cambridge
  • Hobbie, J.E., Bahr, M., Bettez, N., Rublee, P.A., Microbial food webs in oligotrophic arctic lakes (2000) Microbial Biosystems: New Frontiers. Proc 8th Int Symp Microbial Ecology, Hali - Fax, Aug 9-14, 1998, pp. 293-298. , In: Bell C, Bry - linksy M, Johnson-Green P (eds), Atlantic Canada Society for Microbial Ecology, Halifax
  • Iriondo, M., Quaternary lakes of Argentina (1989) Palaeogeogr Palaeoclimatol Palaeoecol, 70, pp. 81-88
  • Izaguirre, I., Vinocur, A., Mataloni, G., Pose, M., Phytoplankton communities in relation to trophic status in lakes from Hope Bay (Antarctic Peninsula) (1998) Hydro - Biologia, 369-370, pp. 73-87
  • Izaguirre, I., Allende, L.U.Z., Marinone, M.C., Comparative study of the planktonic communities of three lakes of contrasting trophic status at Hope Bay (Antarctic Peninsula) (2003) J Plankton Res, 25, pp. 1079-1097
  • Izaguirre, I., Sinistro, R., Schiaffino, M.R., Sánchez, M.L., Unrein, F., Massana, R., Grazing rates of protists in wetlands under contrasting light conditions due to floating plants (2012) Aquat Microb Ecol, 65, pp. 221-232
  • Jeong, H.J., Seong, K.A., Kang, N.S., Yoo, Y.D., Feeding by raphidophytes on the cyanobacterium Synecho coccus sp (2010) Aquat Microb Ecol, 58, pp. 181-195
  • Jezbera, J., Hornák, K., Simek, K., Food selection by bacterivorous protists: Insight from the analysis of the food vacuole content by means of fluorescence in situ hybridization (2005) FEMS Microbiol Ecol, 52, pp. 351-363
  • Jones, R.I., Mixotrophy in planktonic protist as a spectrum of nutritional strategies (1994) Mar Microb Food Webs, 8, pp. 87-96
  • Jones, R.I., Mixotrophy in planktonic protists: An over - View (2000) Freshw Biol, 45, pp. 219-226
  • Kiørboe, T., Grossart, H., Ploug, H., Tang, K., Auer, B., Particle- associated flagellates: Swimming patterns, colonization rates, and grazing on attached bacteria (2004) Aquat Microb Ecol, 35, pp. 141-152
  • Kristiansen, J., Phylum chrysophyta (1990) Handbook of Protoctista, pp. 438-453. , In: Margulis L, Corliss JO, Melkonian M, Chapman DJ (eds), Jones & Bartlett, Boston, MA
  • Kristiansen, J., Sandgren, C.D., The ultrastructural bases of chrysophyte systematics and phylogeny (1986) Crit Rev Plant Sci, 4, pp. 149-211
  • Lagus, A., Soumela, J., Weithoff, G., Heikkelä, K., Helminen, H., Sipura, J., Species-specific differences in phytoplankton responses to N and P enrichments and the N: P ratio in the Archipelago Sea, northern Baltic Sea (2004) J Plankton Res, 26, pp. 779-798
  • Laybourn-Parry, J., Marshall, W.A., Photosynthesis, mixo trophy and microbial plankton dynamics in two high Arctic lakes during summer (2003) Polar Biol, 26, pp. 517-524
  • Lee, S., Fuhrman, J.A., Relationships between bio volume and biomass of naturally derived marine bacterio - Plankton (1987) Appl Environ Microbiol, 53, pp. 1298-1303
  • Li, A., Stoecker, D.K., Coats, D.W., Mixotrophy in Gyrodi - Nium galatheanum (Dinophyceae): Grazing responses to light intensity and inorganic nutrients (2000) J Phycol, 36, pp. 33-45
  • Maruyama, S., Kim, E., A modern descendant of early green algal phagotrophs (2013) Curr Biol, 23, pp. 1081-1084
  • McKie-Krisberg, Z.M., Gast, R.J., Sanders, R.W., Physio - Logical responses of three species of Antarctic mixo - Trophic phytoflagellates to changes in light and dissolved nutrients (2015) Microb Ecol, 70, pp. 21-29
  • Menden-Deuer, S., Lessard, E.J., Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton (2000) Limnol Oceanogr, 45, pp. 569-579
  • Morabito, G., Oggioni, A., Caravati, E., Panzani, P., Seasonal morphological plasticity of phytoplankton in Lago Maggiore (N. Italy) (2007) Hydrobiologia, 578, pp. 47-57
  • Nygaard, K., Tobiesen, A., Bacterivory in algae: A survival strategy during nutrient limitation (1993) Limnol Oceanogr, 38, pp. 273-279
  • O'Farrell, I., Tezanos Pinto, P., Izaguirre, I., Phytoplankton morphological response to the underwater light conditions in a vegetated wetland (2007) Hydrobiologia, 578, pp. 65-77
  • Olrik, K., Ecology of mixotrophic flagellates with special reference to Chrysophyceae in Danish lakes (1998) Hydrobiologia, 369-370, pp. 329-338
  • Ostroff, C., Karlander, E., Van Valkenburg, S., Growth rates of Pseudopedinella pyriforme (Chrysophyceae) in response to 75 combinations of light, temperature and salinity (1980) J Phycol, 16, pp. 421-423
  • Paruelo, J.M., Beltrán, A., Jobbágy, E., Sala, O.E., Rodolfo, A., The climate of Patagonia: General patterns and controls on biotic processes (1998) Ecología Austral, 8, pp. 85-101
  • Pernthaler, J., Sattler, B., Šimek, K., Schwarzenbacher, A., Psenner, R., Top-down effects on the size-biomass distribution of a freshwater bacterioplankton community (1996) Aquat Microb Ecol, 10, pp. 255-263
  • Pirlot, S., Unrein, F., Descy, J.P., Servais, P., Fate of heterotrophic bacteria in Lake Tanganyika (East Africa) (2007) FEMS Microbiol Ecol, 62, pp. 354-364
  • Porter, K.G., Phagotrophic phytoflagellates in microbial food webs (1988) Hydrobiologia, 159, pp. 89-97
  • Porter, K.G., Feig, Y., The use of DAPI for identifying aquatic microflora (1980) Limnol Oceanogr, 25, pp. 943-948
  • Queimaliños, C., The role of phytoplanktonic size fractions in the microbial food webs in two north Patagonian lakes (Argentina) (2002) Arch Hydrobiol, 28, pp. 1236-1240
  • Queimaliños, C., Diaz, M., Phytoplankton of Andean Patagonian lakes (2014) Freshwater Phytoplankton of Argentina, pp. 235-256. , In: Tell G, Izaguirre I, O'Farrell I (eds), Schweizerbart, Stuttgart
  • Quirós, R., Drago, E., The environmental state of Argentinean lakes: An overview (1999) Lakes Reserv Res Manag, 4, pp. 55-64
  • Raven, J., Phagotrophy in phototrophs (1997) Limnol Oceanogr, 42, pp. 198-205
  • Rice, J.A., (1988) Mathematical Statistics and Data Analysis, , Wadsworth, Belmont, CA
  • Rosén, G., Phytoplankton indicators and their relations to certain chemical and physical factors (1981) Limnologica, 13, pp. 2263-2290
  • Rothhaupt, K.O., Utilization of substitutable carbon and phosphorus sources by the mixotrophic chrysophyte Ochromonas sp? (1996) Ecology, 77, pp. 706-715
  • Rothhaupt, K.O., Laboratory experiments with a mixotrophic chrysophyte and obligately phagotrophic and photo trophic competitors? (1996) Ecology, 77, pp. 716-724
  • Rottberger, J., Gruber, A., Boenigk, J., Kroth, P.G., Influence of nutrients and light on autotrophic, mixotrophic and heterotrophic freshwater chrysophytes (2013) Aquat Microb Ecol, 71, pp. 179-191
  • Saad, J.F., Schiaffino, M.R., Vinocur, A., O'Farrell, I., Tell, G., Izaguirre, I., Microbial planktonic communities of freshwater environments from Tierra del Fuego: Dominant trophic strategies in lakes with contrasting features (2013) J Plankton Res, 35, pp. 1220-1233
  • Sanders, R.W., Porter, K.G., Bennett, S.J., Debiase, A.E., Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community (1989) Limnol Oceanogr, 34, pp. 673-687
  • Sanders, R.W., Porter, K.G., Caron, D.A., Relationship between phototrophy and phagotrophy in the mixo - Trophic chrysophyte Poterioochromonas malhamensis (1990) Microb Ecol, 19, pp. 97-109
  • Schiaffino, M.R., Unrein, F., Gasol, J.M., Massana, R., Balagué, V., Izaguirre, I., Bacterial community structure in a lati - Tudinal gradient of lakes: The roles of spatial versus environmental factors (2011) Freshw Biol, 56, pp. 1973-1991
  • Schmidtke, A., Bell, E.M., Weithoff, G., Potential grazing impact of the mixotrophic flagellate Ochromonas sp. (Chrysophyceae) on bacteria in an extremely acidic lake (2006) J Plankton Res, 28, pp. 991-1001
  • Sekiguchi, H., Kawachi, M., Nakayama, T., Inouye, I., A taxonomic re-evaluation of the Pedinellales (Dictyo - Chophyceae), based on morphological, behavioural and molecular data (2003) Phycologia, 42, pp. 165-182
  • Smalley, G.W., Wayne Coats, D., Stoecker, D.K., Influence of inorganic nutrients, irradiance, and time of day on food uptake by the mixotrophic dinoflagellate Neocera - Tium furca (2012) Aquat Microb Ecol, 68, pp. 29-41
  • Stauffer, B.A., Schaffner, R., Wazniak, C., Caron, D., Immunofluorescence flow cytometry technique for enumeration of the brown-tide alga, Aureococcus anopha - Gefferens (2008) Appl Environ Microbiol, 74, pp. 6931-6940
  • Stoecker, D.K., Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications (1998) Eur J Protistol, 34, pp. 281-290
  • Stoecker, D.K., Mixotrophy among dinoflagellates (1999) J Eukaryot Microbiol, 46, pp. 397-401
  • Stoecker, D.K., Li, A., Coats, D.W., Gustafson, D.E., Nannen, M.K., Mixotrophy in the dinoflagellate Prorocentrum minimum (1997) Mar Ecol Prog ser, 152, pp. 1-12
  • Suikkanen, S., Laamanen, M., Huttunen, M., Long-term changes in summer phytoplankton communities of the open northern Baltic Sea (2007) Estuar Coast Shelf Sci, 71, pp. 580-592
  • Suikkanen, S., Pulina, S., Engström-Öst, J., Lehtiniemi, M., Lehtinen, S., Brutemark, A., Climate change and eutro - Phication induced shifts in northern summer plankton communities? (2013) PLoS ONE, 8, p. e66475
  • Sun, J., Liu, D., Geometric models for calculating cell biovolume and surface area for phytoplankton (2003) J Plankton Res, 25, pp. 1331-1346
  • Thomsen, H., Ultrastructural studies of the flagellate and cyst stages of Pseudopedinella tricostata (Pedinellales, Chrysophyceae) (1988) Br Phycol J, 23, pp. 1-16
  • Tranvik, L.J., Porter, K.G., Sieburth, J.M., Occurrence of bacterivory in Cryptomonas, a common freshwater phyto plankter (1989) Oecologia, 78, pp. 473-476
  • Unrein, F., Izaguirre, I., Massana, R., Balagué, V., Gasol, J.M., Nanoplankton assemblages in maritime Antarctic lakes: Characterisation and molecular fingerprinting comparison (2005) Aquat Microb Ecol, 40, pp. 269-282
  • Unrein, F., Massana, R., Alonso-Sáez, L., Gasol, J.M., Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system (2007) Limnol Oceanogr, 52, pp. 456-469
  • Unrein, F., Gasol, J.M., Massana, R., Dinobryon facu - Liferum (Chrysophyta) in coastal Mediterranean sea - Water: Presence and grazing impact on bacteria (2010) J Plankton Res, 32, pp. 559-564
  • Unrein, F., Gasol, J.M., Not, F., Forn, I., Massana, R., Mixotrophic haptophytes are key bacterial grazers in oligo - Trophic coastal waters (2014) ISME J, 8, pp. 164-176
  • Urabe, J., Gurung, T.B., Yoshida, T., Sekino, T., Nakanishi, M., Maruo, M., Nakayama, E., Diel changes in phago - Trophy by Cryptomonas in Lake Biwa (2000) Limnol Oceanogr, 45, pp. 1558-1563
  • Vähätalo, A.V., Aarnos, H., Hoikkala, L., Lignell, R., Photochemical transformation of terrestrial dissolved organic matter supports hetero- and autotrophic production in coastal waters (2011) Mar Ecol Prog ser, 423, pp. 1-14
  • Zubkov, M.V., Tarran, G.A., High bacterivory by the smallest phytoplankton in the North Atlantic Ocean (2008) Nature, 455, pp. 224-226

Citas:

---------- APA ----------
Gerea, M., Saad, J.F., Izaguirre, I., Queimaliños, C., Gasol, J.M. & Unrein, F. (2015) . Presence, abundance and bacterivory of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments. Aquatic Microbial Ecology, 76(3), 219-232.
http://dx.doi.org/10.3354/ame01780
---------- CHICAGO ----------
Gerea, M., Saad, J.F., Izaguirre, I., Queimaliños, C., Gasol, J.M., Unrein, F. "Presence, abundance and bacterivory of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments" . Aquatic Microbial Ecology 76, no. 3 (2015) : 219-232.
http://dx.doi.org/10.3354/ame01780
---------- MLA ----------
Gerea, M., Saad, J.F., Izaguirre, I., Queimaliños, C., Gasol, J.M., Unrein, F. "Presence, abundance and bacterivory of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments" . Aquatic Microbial Ecology, vol. 76, no. 3, 2015, pp. 219-232.
http://dx.doi.org/10.3354/ame01780
---------- VANCOUVER ----------
Gerea, M., Saad, J.F., Izaguirre, I., Queimaliños, C., Gasol, J.M., Unrein, F. Presence, abundance and bacterivory of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments. Aquatic Microb. Ecol. 2015;76(3):219-232.
http://dx.doi.org/10.3354/ame01780