Abstract:
Heterocytous Cyanobacteria show high trait variation at the cellular, organismal, and population levels. Members of this group can produce specialized cells such as akinetes and heterocytes that influence their ecology, including bloom development and population survival. This study characterizes patterns of variation in the traits of these species, including the traits of specialized cells, to expand our ecological knowledge and predictive capacity for this group. We compiled and synthesized morphological and physiological traits of planktic heterocytous Cyanobacteria from the published literature and experiments, and assessed trait distributions, trait relationships, and their similarities among species. Although the volumes of akinetes and heterocytes were positively related to that of vegetative cells, the shape of cells differed in ways that may reflect their function, and the position of heterocytes within filaments may relate to growth rate. Maximum growth rates differed significantly among genera, yet surprisingly did not correlate with cell volume. Also, despite the high energetic cost of N fixation in low N conditions, our results suggest that growth rate seems unrelated to nitrogen availability. The degree of trait variation within heterocytous Cyanobacteria, which suggests the existence of three functionally distinct subgroups, may offer new insights into which taxa dominate bloom assemblages under different conditions. © 2018, Springer International Publishing AG, part of Springer Nature.
Registro:
Documento: |
Artículo
|
Título: | Assessing patterns of morphological and physiological trait variations across heterocytous cyanobacteria at cellular and population levels |
Autor: | Yema, L.; Kremer, C.T.; O’Farrell, I.; de Tezanos Pinto, P. |
Filiación: | Laboratorio de Limnología, Depto. Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Univ. De Buenos Aires (UBA), Pabellón II, Ciudad Universitaria. Int. Güiraldes 2620, Buenos Aires, C1428EHA, Argentina Kellogg Biological Station, Michigan State University, Hickory Corners, MI 49060, United States Instituto de Botánica Darwinion, Labardén 200, Casilla de Correo 22, San Isidro, Buenos Aires, B1642HYD, Argentina
|
Palabras clave: | Akinete; Growth rate; Heterocyte; Size and shape; assessment method; cell; cyanobacterium; growth rate; life history trait; morphology; nitrogen fixation; nutrient availability; physiology; plankton; shape; size; taxonomy; Cyanobacteria |
Año: | 2018
|
Volumen: | 823
|
Número: | 1
|
Página de inicio: | 93
|
Página de fin: | 107
|
DOI: |
http://dx.doi.org/10.1007/s10750-018-3698-5 |
Título revista: | Hydrobiologia
|
Título revista abreviado: | Hydrobiologia
|
ISSN: | 00188158
|
CODEN: | HYDRB
|
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00188158_v823_n1_p93_Yema |
Referencias:
- Adams, D.G., Duggan, P.S., Heterocyst and akinete differentiation in cyanobacteria (1999) New Phytologist, 144, pp. 3-33
- Bates, D., Mächler, M., Bolker, B., Walker, S., Fitting linear mixed-effects models using lme4 (2015) Journal of Statistical Software, 67, pp. 1-48
- Braune, W., Structural aspects of akinete germination in the cyanobacterium Anabaena variabilis (1980) Archives of Microbiology, 126, pp. 257-261
- Bruggeman, J., A phylogenetic approach to the estimation of phytoplankton traits (2011) Journal of Phycology, 47, pp. 52-65. , PID: 27021710
- Burford, M.A., Beardall, J., Willis, A., Orr, P.T., Magalhaes, V.T., Rangel, L.M., Azevedo, S.M.O.F., Neilan, B.A., Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii (2016) Harmful Algae, 54, pp. 44-53. , PID: 28073481
- de Tezanos Pinto, P., Kust, A., Devercelli, M., Kozlíková-Zapomělová, E., Morphological traits in nitrogen fixing heterocytous cyanobacteria: possible links between morphology and eco-physiology (2016) Hydrobiologia, 764, pp. 271-281
- Dolman, A.M., Rücker, J., Pick, F.R., Fastner, J., Rohrlack, T., Mischke, U., Wiedner, C., Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus (2012) PLoS ONE, 7. , PID: 22719937
- Fogg, G.E., Thake, B., (1987) Algal cultures and phytoplankton ecology, , University of Wisconsin Press, Madison
- Halekoh, U., Højsgaard, S., A Kenward–Roger approximation and parametric bootstrap methods for tests in linear mixed models – The R Package pbkrtest (2014) Journal of Statistical Software, 59, pp. 1-32
- Hense, I., Beckmann, A., Towards a model of cyanobacteria life cycle-effects of growing and resting stages on bloom formation of N2-fixing species (2006) Ecological Modelling, 195, pp. 205-218
- Hillebrand, H., Dürselen, C.-D., Kirschtel, D., Pollingher, U., Zohary, T., Biovolume calculation for pelagic and benthic microalgae (1999) Journal of Phycology, 35, pp. 403-424
- Hindák, F., Akinete development in Anabaena augstumalis Schmidle (Cyanophyta/Cyanobacteria) by fusion of several pro-akinetes (1999) Algological Studies, 94, pp. 147-161
- Hindák, F., (2008) Colour Atlas of Cyanophytes, , Academy of Sciences, Veda Bratislava
- Huang, B., Harper, D.A.T., Hammer, Ø., Introduction to PAST, a comprehensive statistics software package for paleontological data analysis (2013) Acta Palaeontologica Sinica, 52, pp. 161-181
- Kenesi, G., Shafik, H.M., Kovács, A.W., Herodek, S., Présing, M., Effect of nitrogen forms on growth, cell composition and N2 fixation of Cylindrospermopsis raciborskii in phosphorus-limited chemostat cultures (2009) Hydrobiologia, 623, pp. 191-202
- Kerkhoff, A.J., Enquist, B.J., Multiplicative by nature: why logarithmic transformation is necessary in allometry (2009) Journal of Theoretical Biology, 257, pp. 519-521
- Kirk, J.T.O., (1994) Light and photosynthesis in aquatic ecosystems, , 2, Cambridge University Press, Cambridge
- Kokociński, M., Soininen, J., Environmental factors related to the occurence of Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) at the north-eastern limit of its geographical range (2012) European Journal of Phycology, 47, pp. 12-21
- Komárek, J., Cyanoprokaryota 3 Teil/3rd Part: heterocytous genera (2013) Süwasserflora von mitteleuropa/freshwater flora of Central Europe 19/3, , Büdel B, Gaärtner G, Krienitz L, Schagerl M, (eds), Berlin, Heidelberg, Springer Spektrum
- Kremer, C.T., Thomas, M.K., Litchman, E., Temperature- and size-scaling of phytoplankton population growth rates: reconciling the Eppley curve and the metabolic theory of ecology (2017) Limnology and Oceanography, 62, pp. 1658-1670
- Kremer, C.T., Williams, A.K., Finiguerra, M., Fong, A.A., Kellerman, A., Paver, S.F., Tolar, B.B., Toscano, B.J., Realizing the potential of trait-based aquatic ecology: new tools and collaborative approaches (2017) Limnology and Oceanography, 62, pp. 253-271
- Kruk, C., Huszar, V.L.M., Peeters, E.T.H.M., Bonilla, S., Costa, L., LüRling, M., Reynolds, C.S., Scheffer, M., A morphological classification capturing functional variation in phytoplankton (2010) Freshwater Biology, 55, pp. 614-627
- Kruk, C., Devercelli, M., Huszar, V.L.M., Hernández, E., Beamud, G., Diaz, M., Silva, L.H.S., Segura, A.M., Classification of Reynolds phytoplankton functional groups using individual traits and machine learning techniques (2017) Freshwater Biology, 62, pp. 1681-1692
- Kumar, K., Mella-Herrera, R.A., Golden, J.W., Cyanobacterial heterocysts (2010) Cold Spring Harbor Perspective in Biology
- Lang, N.J., Fay, P., The heterocysts of blue-green algae. II. Details of ultrastructure (1971) Proceedings of the Royal Society B: Biological Sciences, 178, pp. 193-203
- Legrand, B., Le Jeune, A.H., Colombet, J., Thouvenot, A., Latour, D., Akinetes may be representative of past Nostocalean blooms: a case study of their benthic spatiotemporal distribution and potential for germination in a Eutrophic lake (2017) Applied and Environmental Microbiology
- Litchman, E., Klausmeier, C.A., Trait-based community ecology of phytoplankton (2008) Annual Review of Ecology, Evolution, and Systematics, 39, pp. 615-639
- Mantzouki, E., Visser, P.M., Bormans, M., Ibelings, B.W., Understanding the key ecological traits of cyanobacteria as a basis for their management and control in changing lakes (2016) Aquatic Ecology Springer, Netherlands, 50, pp. 333-350
- Moore, D., McGregor, G.B., Shaw, G., Morphological changes during akinete germination in Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) (2004) Journal of phycology, 40, pp. 1098-1105
- Nichols, J.M., Adams, D.G., Akinetes (1982) The Biology of Cyanobacteria, pp. 387-412. , Carr NG, Whitton BA, (eds), Blackwell, Oxford
- O’Farrell, I., de Tezanos Pinto, P., Izaguirre, I., Phytoplankton morphological response to the underwater light conditions in a vegetated wetland (2007) Hydrobiologia, 578, pp. 65-77
- O’Farrell, I., Vinocur, A., de Tezanos Pinto, P., Long-term study of bloom-forming cyanobacteria in a highly fluctuating vegetated floodplain lake: a morpho-functional approach (2015) Hydrobiologia, 752, pp. 91-102
- Padisák, J., Crossetti, L.O., Naselli-Flores, L., Use and misuse in the application of the phytoplankton functional classification: a critical review with updates (2009) Hydrobiologia, 621, pp. 1-19
- Paerl, H.W., Huisman, J., Blooms like it hot (2008) Science American Association for the Advancement of Science, 320, pp. 57-58
- Pinheiro, J.D., Bates, S., Debroysarkar, D., (2018) Nlme: Linear and nonlinear mixed effects models, , https://CRAN.R-project.org/package=nlme, R package version 3.1-131.1
- (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, , http://www.R-project.org/, Vienna, Austria
- Reynolds, C.S., (1997) Vegetation Processes in the Pelagic: A Model for Ecosystem Theory, 9. , Ecology Institute, Oldendorf/Luhe
- Reynolds, C.S., (2006) Ecology of Phytoplankton, , Cambridge University Press, New York
- Reynolds, C.S., Huszar, V., Kruk, C., Naselli-Flores, L., Melo, S., Towards a functional classification of the freshwater phytoplankton (2002) Journal of Plankton Research, 24, pp. 417-428
- Sarthou Suárez, F.V., (2016) Floraciones de cianobacterias: efectos de la eutrofización y la variabilidad climática, , Universidad de la República, Uruguay
- Schwaderer, A.S., Yoshiyama, K., de Tezanos Pinto, P., Swenson, N.G., Klausmeier, C.A., Litchman, E., Eco-evolutionary differences in light utilization traits and distributions of freshwater phytoplankton (2011) Limnology and Oceanography, 56, pp. 589-598
- Sukenik, A., Kaplan-Levy, R.N., Welch, J.M., Post, A.F., Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria) (2011) The ISME Journal Nature Publishing Group, 6, pp. 670-679
- Sukenik, A., Kaplan-Levy, R.N., Viner-Mozzini, Y., Quesada, A., Hadas, O., Potassium deficiency triggers the development of dormant cells (akinetes) in Aphanizomenon ovalisporum (Nostocales, Cyanoprokaryota) 1 (2013) Journal of Phycology, 49, pp. 580-587. , PID: 27007046
- Tomitani, A., Knoll, A.H., Cavanaugh, C.M., Ohno, T., The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives (2006) Proceedings of the National Academy of Sciences of the United States of America, 103, pp. 5442-5447. , PID: 16569695
- Uyeda, J.C., Harmon, L.J., Blank, C.E., A comprehensive study of cyanobacterial morphological and ecological evolutionary dynamics through deep geologic time (2016) PLoS ONE, 11, pp. 1-32
- Walsby, A.E., Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange (2007) Trends in Microbiology, 15, pp. 340-349. , PID: 17644394
- Wolk, C.P., Ernst, A., Elhai, J., Heterocyst metabolism and development (1994) The Molecular Biology of Cyanobacteria, pp. 769-823. , Bryant DA, (ed), Springer, Dordrecht
- Yema, L., Litchman, E., de Tezanos Pinto, P., The role of heterocytes in the physiology and ecology of bloom-forming harmful cyanobacteria (2016) Harmful Algae, 60, pp. 131-138. , PID: 28073556
- Zevenboom, W., van der Does, J., Bruning, K., Mur, L.R., A non-heterocystous mutant of Aphanizomenon flosaquae, selected by competition in light-limited continuous culture (1981) FEMS Microbiology Letters, 10, pp. 11-16
- Zhang, C.-C., Laurent, S., Sakr, S., Peng, L., Bédu, S., Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals (2006) Molecular Microbiology, 59, pp. 367-375. , PID: 16390435
Citas:
---------- APA ----------
Yema, L., Kremer, C.T., O’Farrell, I. & de Tezanos Pinto, P.
(2018)
. Assessing patterns of morphological and physiological trait variations across heterocytous cyanobacteria at cellular and population levels. Hydrobiologia, 823(1), 93-107.
http://dx.doi.org/10.1007/s10750-018-3698-5---------- CHICAGO ----------
Yema, L., Kremer, C.T., O’Farrell, I., de Tezanos Pinto, P.
"Assessing patterns of morphological and physiological trait variations across heterocytous cyanobacteria at cellular and population levels"
. Hydrobiologia 823, no. 1
(2018) : 93-107.
http://dx.doi.org/10.1007/s10750-018-3698-5---------- MLA ----------
Yema, L., Kremer, C.T., O’Farrell, I., de Tezanos Pinto, P.
"Assessing patterns of morphological and physiological trait variations across heterocytous cyanobacteria at cellular and population levels"
. Hydrobiologia, vol. 823, no. 1, 2018, pp. 93-107.
http://dx.doi.org/10.1007/s10750-018-3698-5---------- VANCOUVER ----------
Yema, L., Kremer, C.T., O’Farrell, I., de Tezanos Pinto, P. Assessing patterns of morphological and physiological trait variations across heterocytous cyanobacteria at cellular and population levels. Hydrobiologia. 2018;823(1):93-107.
http://dx.doi.org/10.1007/s10750-018-3698-5