Skip to main content

Advertisement

SpringerLink
Log in

Morphological traits in nitrogen fixing heterocytous cyanobacteria: possible links between morphology and eco-physiology

  • PHYTOPLANKTON & SPATIAL GRADIENTS
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Heterocytous cyanobacteria are able to fix nitrogen (in heterocytes) and to produce dormant cells (akinetes). Heterocyte and akinete shape, size, and relative position have taxonomical relevance and possibly ecological value too. We collected—from literature and nature—and compared morphological data on vegetative cells, heterocytes, and akinetes across four genera taxonomically separated from Anabaena. In average, heterocyte size doubled that of vegetative cells—probably because of extra cell wall deposition. Heterocyte morphology was remarkably similar across genera, both in size and shape (spherical). The latter may decrease oxygen diffusion from adjoining vegetative cells. Akinetes were huge (one order of magnitude bigger) compared to vegetative cells, probably because of its massive genome replication, extra deposition of wall layers, allocation of storage and number of vegetative cells fused during akinete differentiation. Akinete shape was mostly cylindrical, or oval, but rarely spherical. In line with molecular data, we found morphological differences between Anabaena (non-aerotopated, soil or benthic) and Dolichospermum (aerotopated, planktonic), including vegetative cell size, and akinete size, shape, and relative position to the heterocyte. Differences may relate to adaptations to their contrasting environments (benthic versus planktic). Further research is needed to generalize our results to other heterocytous genera.

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

Similar content being viewed by others

References

  • Arnold, S. J., 1983. Morphology, performance and fitness. American Zoologist 23: 347–361.

    Article  Google Scholar 

  • Clark, R. L. & T. E. Jensen, 1969. Ultrastructure of akinete development in a blue green alga. Cylindrospermum sp. Cytologia 34: 439–448.

    Article  Google Scholar 

  • Cmiech, H. A., G. F. Leedale & C. S. Reynolds, 1984. Morphological and ultrastructural variability of planktonic Cyanophyceae in relation to seasonal periodicity. I. Gleotrichia echinulata: vegetative cells, polarity, heterocysts, akinetes. British Phycological. Journal 19: 259–275.

    Article  Google Scholar 

  • Fay, P., 1969. Cell differentiation and pigment composition in Anabaena cylindrica. Archives of Microbiology 67: 62–70.

    CAS  Google Scholar 

  • Flores, E., A. Herrero, C. P. Wolk & I. Maldener, 2006. Is the periplasm continuous in filamentous multicellular Cyanobacteria? Trends in Microbiology 14: 439–443.

    Article  CAS  PubMed  Google Scholar 

  • Gallon, J. R., 1992. Reconciling the incompatible: N2 fixation and oxygen. New Phytologist 122: 571–609.

    Article  CAS  Google Scholar 

  • Giddings, T. H. & L. A. Staehelin, 1981. Observation of microplasmodesmata in both heterocyst-forming and non-heterocyst forming filamentous cyanobacteria by freeze-fracture electron microscopy. Archives of Microbiology 129: 295–298.

    Article  Google Scholar 

  • Gugger, M., C. Lyra, P. Henriksen, A. Couté, J. F. Humbert & K. Sivonen, 2002. Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon. International Journal of Systematic and Evolutionary Microbiology 52: 1–14.

    Article  Google Scholar 

  • Hammer, Ø., D. A. T. Harper & P. D. Ryan, 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: p. 9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.

  • 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: 253.

  • Hodgson, J. G. E. A., 1999. Allocating C-S-R plant functional types: a soft approach to a hard problem. Oikos 85: 282–294.

    Article  Google Scholar 

  • Hoffman, L., J. Komárek & J. Kaštovský, 2005. System of cyanoprokaryotes (cyanobacteria)—state in 2004. Algological Studies 117: 95–115.

    Article  Google Scholar 

  • Herdman, M., 1987. Akinetes: structure and function. In Fay, P. & C. van Baalen (eds.), The Cyanobacteria. Elsevier, Amsterdam: 227–250.

    Google Scholar 

  • Herdman, M., 1988. Cellular differentiation: akinetes. Methods Enzymology 167: 222–232.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Iteman, I., R. Rippka, N. T. Marsac & M. Herdman, 2002. rDNA analyses of planktonic heterocystous cyanobacteria, including members of genera Anabaenopsis and Cyanospira. Microbiology 148: 481–496.

    Article  CAS  PubMed  Google Scholar 

  • Jaffe, D. A., 1992. The nitrogen cycle. In Butcher, S. S., R. J. Charlson, G. H. Orians & G. V. Wolfe (eds.), Global Biogeochemical Cycles. Academic Press, London: 265–284.

    Google Scholar 

  • Kaplan-Levy, R. N., O. Hadas, M. L. Summers, J. Rucker & A. Sukenik, 2010. Akinetes: dormant cells of Cyanobacteria. In Lubzens, E., et al. (eds.), Dormancy and Resistance in Harsh Environments, Topics in Current Genetics 21. Springer, Heidelberg: 5–27.

    Chapter  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 

  • Komárek, J., 1975. Blaualgen aus dem Naturschutzgebiet “Řežabinec“bei Ražice. Nova Hedwigia 26: 601–643.

    Google Scholar 

  • Komárek, J., 1996. Towards a combined approach for the taxonomy and species delimitation of picoplanktic cyanoprokaryotes. Algological Studies/Archiv für Hydrobiologie 83: 377–401.

    Google Scholar 

  • Komárek, J., 2013. Cyanoprokaryota 3. Teil/3rd Part: Heterocytous genera. In Büdel, B., G. Gärtner, L. Krienitz & M. Schagerl (eds.), Süwasserflora von Mitteleuropa/Freshwater flora of Central Europe 19/3. Springer Spektrum, Berlin, Heidelberg: 1130.

    Chapter  Google Scholar 

  • Komárek, J. & E. Zapomělová, 2007. Planktic morphospecies of the cyanobacterial genus Anabaena = subg. Dolichospermum – 1. part: coiled types. Fottea 7: 1–31.

    Article  Google Scholar 

  • Komárek, J. & E. Zapomělová, 2008. Planktic morphospecies of the cyanobacterial genus Anabaena = subg. Dolichospermum – 2. part: straight types. Fottea 8: 1–14.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kust A, E. Kozlíková–Zapomělová, J. Mareš1 K. Řeháko, 2015. A detailed morphological, phylogenetic and ecophysiological analysis of four benthic Anabaena (Nostocales, Cyanobacteria) strains confirms deep heterogeneity within the genus. Fottea, Olomouc 15: 113–122.

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Litchman, E., P. de Tezanos Pinto, C. Klausmeier, M. Thomas & K. Yoshiyama, 2010. Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653: 15–28.

    Article  CAS  Google Scholar 

  • Mullineaux, C. W., V. Mariscal, A. Nenninger, H. Khanum, A. Herrero, E. Flores & D. G. Adams, 2008. Mechanism of intracellular molecular Exchange in heterocyt-forming cyanobacteria. The EMBO Journal 27: 1299–1308.

    Article  PubMed Central  CAS  PubMed  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 

  • Padisák, J., L. 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 

  • Rajaniemi, P., P. Hrouzek, K. Kaštovská, R. Willame, A. Rantala, L. Hoffmann, J. Komárek & K. Sivonen, 2005a. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). International Journal of Systematic and Evolutionary Microbiology 55: 11–26.

    Article  CAS  PubMed  Google Scholar 

  • Rajaniemi, P., J. Komárek, R. Willame, P. Hrouzek, K. Kaštovská, L. Hoffmann & K. Sivonen, 2005b. Taxonomic consequences from the combined molecular and phenotype evaluation of selected Anabaena and Aphanizomenon strains. Archiv für Hydrobiologie/Algological Studied 117: 371–391.

    Google Scholar 

  • Reynolds, C. S., V. L. M. 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 

  • Salmaso, N. & J. Padisák, 2007. Morpho-functional groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578: 97–112.

    Article  Google Scholar 

  • Salmaso, N., L. Naselli-Flores & J. Padisák, 2014. Functional classifications and their application in phytoplankton ecology. Freshwater Biology 60: 603–619.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Simon, R. D., 1987. Inclusion bodies in the cyanobacteria: cyanophycin, polyphospate and poyhedral bodies. In Fay, P. & C. van Baalen (eds.), The Cyanobacteria: current Research. Elsevier/North Holland Biomedical Press, Amsterdam: 199–226.

    Google Scholar 

  • Sukenik, A., S. Stojkovic, N. Malinsky-Rushansky, Y. Viner-Motzini & J. Beardall, 2009. Fluorescence approaches reveal variations in cellular composition during formation of akinetes in the cyanobacterium Aphanizomenon ovalisporum. European Journal of Phycology 44: 309–317.

    Article  CAS  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 International Society for Microbial Ecology Journal 6: 670–679.

    Google Scholar 

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

    Article  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 Natural Academy of Science 103: 5442–5447.

    Article  CAS  Google Scholar 

  • Wacklin, P., L. Hoffmann & J. Komárek, 2009. Nomenclatural validation fo the genetically revised cyanobacterial genus Dolichospermum (Ralfs ex Bornet et Flahault) comb. nova. Fottea 9: 59–64.

    Article  Google Scholar 

  • Walsby, A. E., 2007. Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends in Microbiolgy 15: 340–348.

    Article  CAS  Google Scholar 

  • Wolk, C. P., A. Ernst & J. Elhai, 1994. Heterocyst metabolism and development. In Bryant, D. A. (ed.), Molecular Biology of Cyanobacteria. Advances in Photosynthesis and Respiration, Vol. 1. Springer, Dordrecht: 769–823.

    Chapter  Google Scholar 

  • Zapomělová, E., J. Jezberová, P. Hrouzek, D. Hisem, K. Řeháková & J. Komárková, 2009. Polyphasic characterization of three strains of Anabaena reniformis and Aphanizomenon aphanizomenoides (cyanobacteria) and their reclassification to Sphaerospermum gen. nov (incl. Anabaena kisseleviana). Journal of Phycology 45: 1363–1373.

    Article  Google Scholar 

  • Zapomělová, E., O. Skácelová, P. Pumann, R. Kopp & E. Janeček, 2012. Biogeographically interesting planktonic Nostocales (Cyanobacteria) in the Czech Republic and their polyphasic evaluation resulting in taxonomic revisions of Anabaena bergii Ostenfeld 1908 (Chrysosporum gen. nov.) and A. tenericaulis Nygaard 1949 (Dolichospermum tenericaule comb. nova). Hydrobiologia 698: 353–365.

    Article  Google Scholar 

  • Zapomělová, E., J. Mareš, A. Lukešová, O. Skácelová, K. Řeháková & A. Kust, 2013. Extensive polyphyly of non-gas-vacuolate Anabaena species (Nostocales, Cyanobacteria)—a challenge for modern cyanobacterial taxonomy. In: Book of abstracts, 19th Symposium of the International Society for Cyanophyte Research, Cleveland, Ohio, 51 pp.

Download references

Acknowledgements

We thank Lic. Ruben Lombardo for statistical advice. We are grateful to the funding agencies: (a) project of International Cooperation between the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Res.2549) Argentina and the Grant Agency of the Czech Republic (project No. 14-18067S) and (b) CONICET PIP 1142010100236 (Res. 1674). We specially want to thank the organizing committee of the 17th International Workshop of the International Association of Phytoplankton Taxonomy and Ecology and the Editors, for a great meeting. We are grateful to the reviewers for their criticism which markedly improved our manuscript.

Author information

Authors and Affiliations

  1. Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EHA, Buenos Aires Argentina IEGEBA (CONICET-UBA), Buenos Aires, Argentina

    Paula de Tezanos Pinto

  2. Biology Centre, AS CR, v.v.i, Institute of Hydrobiology, Na Sádkách 7, České Budějovice, Czech Republic

    Andreja Kust & Eliška Kozlíková-Zapomělová

  3. Faculty of Science, University of South Bohemia in České Budějovice, Branišovská 31, České Budějovice, Czech Republic

    Andreja Kust

  4. Instituto Nacional de Limnología (CONICET-UNL), Santa Fe, Argentina

    Melina Devercelli

Authors
  1. Paula de Tezanos Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andreja Kust
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Melina Devercelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eliška Kozlíková-Zapomělová
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paula de Tezanos Pinto.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Guest editors: Luigi Naselli-Flores & Judit Padisák / Biogeography and Spatial Patterns of Biodiversity of Freshwater Phytoplankton

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Tezanos Pinto, P., Kust, A., Devercelli, M. et al. Morphological traits in nitrogen fixing heterocytous cyanobacteria: possible links between morphology and eco-physiology. Hydrobiologia 764, 271–281 (2016). https://doi.org/10.1007/s10750-015-2516-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2516-6

Keywords

Search

Navigation