Skip to main content
SpringerLink
Log in

Assessing patterns of morphological and physiological trait variations across heterocytous cyanobacteria at cellular and population levels

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams, D. G. & P. S. Duggan, 1999. Heterocyst and akinete differentiation in cyanobacteria. New Phytologist 144: 3–33.

    Article  Google Scholar 

  • Bates, D., M. Mächler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

    Article  Google Scholar 

  • Braune, W., 1980. Structural aspects of akinete germination in the cyanobacterium Anabaena variabilis. Archives of Microbiology 126: 257–261.

    Article  Google Scholar 

  • Bruggeman, J., 2011. A phylogenetic approach to the estimation of phytoplankton traits. Journal of Phycology 47: 52–65.

    Article  PubMed  Google Scholar 

  • Burford, M. A., J. Beardall, A. Willis, P. T. Orr, V. T. Magalhaes, L. M. Rangel, S. M. O. F. Azevedo & B. A. Neilan, 2016. Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 54: 44–53.

    Article  PubMed  Google Scholar 

  • de Tezanos Pinto, P., A. Kust, M. Devercelli & E. Kozlíková-Zapomělová, 2016. Morphological traits in nitrogen fixing heterocytous cyanobacteria: possible links between morphology and eco-physiology. Hydrobiologia 764: 271–281.

    Article  CAS  Google Scholar 

  • Dolman, A. M., J. Rücker, F. R. Pick, J. Fastner, T. Rohrlack, U. Mischke & C. Wiedner, 2012. Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLoS ONE 7: e38757.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fogg, G. E. & B. Thake, 1987. Algal cultures and phytoplankton ecology. University of Wisconsin Press, Madison.

    Google Scholar 

  • Halekoh, U. & S. Højsgaard, 2014. A Kenward–Roger approximation and parametric bootstrap methods for tests in linear mixed models – The R Package pbkrtest. Journal of Statistical Software 59: 1–32.

    Article  Google Scholar 

  • Hense, I. & A. Beckmann, 2006. Towards a model of cyanobacteria life cycle-effects of growing and resting stages on bloom formation of N2-fixing species. Ecological Modelling 195: 205–218.

    Article  Google Scholar 

  • Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.

    Article  Google Scholar 

  • Hindák, F., 1999. Akinete development in Anabaena augstumalis Schmidle (Cyanophyta/Cyanobacteria) by fusion of several pro-akinetes. Algological Studies 94: 147–161.

    Google Scholar 

  • Hindák, F., 2008. Colour Atlas of Cyanophytes. Academy of Sciences, Veda Bratislava.

    Google Scholar 

  • Huang, B., D. A. T. Harper & Ø. Hammer, 2013. Introduction to PAST, a comprehensive statistics software package for paleontological data analysis. Acta Palaeontologica Sinica 52: 161–181.

    Google Scholar 

  • Kenesi, G., H. M. Shafik, A. W. Kovács, S. Herodek & M. Présing, 2009. Effect of nitrogen forms on growth, cell composition and N2 fixation of Cylindrospermopsis raciborskii in phosphorus-limited chemostat cultures. Hydrobiologia 623: 191–202.

    Article  CAS  Google Scholar 

  • Kerkhoff, A. J. & B. J. Enquist, 2009. Multiplicative by nature: why logarithmic transformation is necessary in allometry. Journal of Theoretical Biology 257: 519–521.

    Article  Google Scholar 

  • Kirk, J. T. O., 1994. Light and photosynthesis in aquatic ecosystems, 2nd ed. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Kokociński, M. & J. Soininen, 2012. Environmental factors related to the occurence of Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) at the north-eastern limit of its geographical range. European Journal of Phycology 47: 12–21.

    Article  Google Scholar 

  • Komárek, J., 2013. Cyanoprokaryota 3 Teil/3rd Part: heterocytous genera. In Büdel, B., G. Gaärtner, L. Krienitz & M. Schagerl (eds), Süwasserflora von mitteleuropa/freshwater flora of Central Europe 19/3. Berlin, Heidelberg, Springer Spektrum.

    Google Scholar 

  • Kremer, C. T., M. K. Thomas & E. Litchman, 2017a. Temperature- and size-scaling of phytoplankton population growth rates: reconciling the Eppley curve and the metabolic theory of ecology. Limnology and Oceanography 62: 1658–1670.

    Article  Google Scholar 

  • Kremer, C. T., A. K. Williams, M. Finiguerra, A. A. Fong, A. Kellerman, S. F. Paver, B. B. Tolar & B. J. Toscano, 2017b. Realizing the potential of trait-based aquatic ecology: new tools and collaborative approaches. Limnology and Oceanography 62: 253–271.

    Article  Google Scholar 

  • Kruk, C., V. L. M. Huszar, E. T. H. M. Peeters, S. Bonilla, L. Costa, M. LüRling, C. S. Reynolds & M. Scheffer, 2010. A morphological classification capturing functional variation in phytoplankton. Freshwater Biology 55: 614–627.

    Article  Google Scholar 

  • Kruk, C., M. Devercelli, V. L. M. Huszar, E. Hernández, G. Beamud, M. Diaz, L. H. S. Silva & A. M. Segura, 2017. Classification of Reynolds phytoplankton functional groups using individual traits and machine learning techniques. Freshwater Biology 62: 1681–1692.

    Article  CAS  Google Scholar 

  • Kumar, K., R. A. Mella-Herrera & J. W. Golden, 2010. Cyanobacterial heterocysts. Cold Spring Harbor Perspective in Biology. https://doi.org/10.1101/cshperspect.a000315.

    Article  Google Scholar 

  • Lang, N. J. & P. Fay, 1971. The heterocysts of blue-green algae. II. Details of ultrastructure. Proceedings of the Royal Society B: Biological Sciences 178: 193–203.

    Article  Google Scholar 

  • Legrand, B., A. H. Le Jeune, J. Colombet, A. Thouvenot & D. Latour, 2017. Akinetes may be representative of past Nostocalean blooms: a case study of their benthic spatiotemporal distribution and potential for germination in a Eutrophic lake. Applied and Environmental Microbiology. https://doi.org/10.1128/AEM.01571-17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Litchman, E. & C. A. Klausmeier, 2008. Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution, and Systematics 39: 615–639.

    Article  Google Scholar 

  • Mantzouki, E., P. M. Visser, M. Bormans & B. W. Ibelings, 2016. Understanding the key ecological traits of cyanobacteria as a basis for their management and control in changing lakes. Aquatic Ecology Springer, Netherlands 50: 333–350.

    Article  CAS  Google Scholar 

  • Moore, D., G. B. McGregor & G. Shaw, 2004. Morphological changes during akinete germination in Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria). Journal of phycology 40: 1098–1105.

    Article  Google Scholar 

  • Nichols, J. M. & D. G. Adams, 1982. Akinetes. In Carr, N. G. & B. A. Whitton (eds), The Biology of Cyanobacteria. Blackwell, Oxford: 387–412.

    Google Scholar 

  • O’Farrell, I., P. de Tezanos Pinto & I. Izaguirre, 2007. Phytoplankton morphological response to the underwater light conditions in a vegetated wetland. Hydrobiologia 578: 65–77.

    Article  Google Scholar 

  • O’Farrell, I., A. Vinocur & P. de Tezanos Pinto, 2015. Long-term study of bloom-forming cyanobacteria in a highly fluctuating vegetated floodplain lake: a morpho-functional approach. Hydrobiologia 752: 91–102.

    Article  CAS  Google Scholar 

  • Padisák, J., L. O. Crossetti & L. Naselli-Flores, 2009. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621: 1–19.

    Article  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2008. Blooms like it hot. Science American Association for the Advancement of Science 320: 57–58.

    Article  CAS  Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Core Team, 2018. nlme: linear and nonlinear mixed effects models. R package version 3.1-131.1. https://CRAN.R-project.org/package=nlme.

  • R Development Core Team, 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

  • Reynolds, C. S., 1997. Vegetation Processes in the Pelagic: A Model for Ecosystem Theory, Vol. 9. Ecology Institute, Oldendorf/Luhe.

    Google Scholar 

  • Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge University Press, New York.

    Book  Google Scholar 

  • Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Melo, 2002. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24: 417–428.

    Article  Google Scholar 

  • Sarthou Suárez, F. V., 2016. Floraciones de cianobacterias: efectos de la eutrofización y la variabilidad climática. Universidad de la República, Uruguay.

    Google Scholar 

  • Schwaderer, A. S., K. Yoshiyama, P. de Tezanos Pinto, N. G. Swenson, C. A. Klausmeier & E. Litchman, 2011. Eco-evolutionary differences in light utilization traits and distributions of freshwater phytoplankton. Limnology and Oceanography 56: 589–598.

    Article  Google Scholar 

  • Sukenik, A., R. N. Kaplan-Levy, J. M. Welch & A. F. Post, 2011. Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria). The ISME Journal Nature Publishing Group 6: 670–679.

    Google Scholar 

  • Sukenik, A., R. N. Kaplan-Levy, Y. Viner-Mozzini, A. Quesada & O. Hadas, 2013. Potassium deficiency triggers the development of dormant cells (akinetes) in Aphanizomenon ovalisporum (Nostocales, Cyanoprokaryota) 1. Journal of Phycology 49: 580–587.

    Article  PubMed  CAS  Google Scholar 

  • Tomitani, A., A. H. Knoll, C. M. Cavanaugh & T. Ohno, 2006. The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proceedings of the National Academy of Sciences of the United States of America 103: 5442–5447.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uyeda, J. C., L. J. Harmon & C. E. Blank, 2016. A comprehensive study of cyanobacterial morphological and ecological evolutionary dynamics through deep geologic time. PLoS ONE 11: 1–32.

    Article  Google Scholar 

  • Walsby, A. E., 2007. Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends in Microbiology 15: 340–349.

    Article  PubMed  CAS  Google Scholar 

  • Wolk, C. P., A. Ernst & J. Elhai, 1994. Heterocyst metabolism and development. In Bryant, D. A. (ed.), The Molecular Biology of Cyanobacteria. Springer, Dordrecht: 769–823.

    Chapter  Google Scholar 

  • Yema, L., E. Litchman & P. de Tezanos Pinto, 2016. The role of heterocytes in the physiology and ecology of bloom-forming harmful cyanobacteria. Harmful Algae 60: 131–138.

    Article  PubMed  CAS  Google Scholar 

  • Zevenboom, W., J. van der Does, K. Bruning & L. R. Mur, 1981. A non-heterocystous mutant of Aphanizomenon flosaquae, selected by competition in light-limited continuous culture. FEMS Microbiology Letters 10: 11–16.

    Article  Google Scholar 

  • Zhang, C.-C., S. Laurent, S. Sakr, L. Peng & S. Bédu, 2006. Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Molecular Microbiology 59: 367–375.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to researchers Ruben Lombardo, Martín Graziano, and Diego Frau for extending the statistics assistance. PTP acknowledges the funding from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina, PIP 1142010100236.

Author information

Authors and Affiliations

  1. 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, C1428EHA, Buenos Aires, Argentina

    Lilen Yema & Inés O’Farrell

  2. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, 49060, USA

    Colin T. Kremer

  3. Instituto de Botánica Darwinion, Labardén 200, Casilla de Correo 22, San Isidro, B1642HYD, Buenos Aires, Argentina

    Paula de Tezanos Pinto

Authors
  1. Lilen Yema
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Colin T. Kremer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Inés O’Farrell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paula de Tezanos Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lilen Yema.

Additional information

Handling editor: Judit Padisák

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yema, L., Kremer, C.T., O’Farrell, I. et al. Assessing patterns of morphological and physiological trait variations across heterocytous cyanobacteria at cellular and population levels. Hydrobiologia 823, 93–107 (2018). https://doi.org/10.1007/s10750-018-3698-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3698-5

Keywords

Search

Navigation