Abstract
Cyanobacteria are an ancient and morphologically diverse group of photosynthetic prokaryotes, which were the first to evolve oxygenic photosynthesis. Cyanobacteria are widely distributed in diversed environments. In the case of members of the orders Nostocales and Stigonematales, their persistence and success were attributed to their ability to form specialized cells: heterocysts, capable of fixing atmospheric nitrogen and spore-like cells, the akinetes. This review focuses on akinetes of Nostocales, emphasizing environmental triggers and cellular responses involved in differentiation, maturation, dormancy, and germination of these resting cells. Morphological and structural changes, variation in akinete composition, and metabolism are summarized. Special attention is given to the genetic regulation of the differentiation process in an attempt to close gaps in our understanding of the dormancy phenomenon in cyanobacteria and to identify open questions for future research.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adams DG, Duggan PS (1999) Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144:3–33
Adhikary SP (1996) Ecology of freshwater and terrestrial cyanobacteria. J Sci Ind Res 55:753–762
Anantharaman V, Aravind L (2002) The PRC-barrel: a widespread, conserved domain shared by photosynthetic reaction center subunits and proteins of RNA metabolism. Genome Biol 3:research0061.0061–research0061.0069
Argueta C, Summers ML (2005) Characterization of a model system for the study of Nostoc punctiforme akinetes. Arch Microbiol 183:338–346
Argueta C, Yuksek K, Summers M (2004) Construction and use of GFP reporter vectors for analysis of cell-type-specific gene expression in Nostoc punctiforme. J Microbiol Methods 59:181–188
Argueta C, Yuksek K, Patel R, Summers ML (2006) Identification of Nostoc punctiforme akinete-expressed genes using differential display. Mol Microbiol 61:748–757
Baker PD, Bellifemine D (2000) Environmental influences on akinete germination of Anabaena circinalis and implications for management of cyanobacterial blooms. Hydrobiologia 427:65–73
Barbiero RP, Kann J (1994) The importance of benthic recruitment to the population development of Aphanizomenon flos-aquae and internal loading in a shallow lake. J Plankton Res 16:1581–1588
Barbiero RP, Welch EB (1992) Contribution of benthic blue-green algal recruitment to lake populations and phosphorous translocation. Freshwater Biol 27:249–260
Berleman JE, Bauer CE (2004) Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum. Microbiology 150:383–390
Bjorn GS, Braune W, Bjorn LO (1983) Photochromic pigments in akinetes and pigment characteristics of akinetes in comparison with vegetative cells of Anabaena variabilis. Physiol Plant 59:493–500
Braune W (1979) C-Phycocyanin: The main photoreceptor in the light-dependent germination process of Anabaena akinetes. Arch Microbiol 122:289–296
Braune W (1980) Structural aspects of akinete germination in the cyanobacterium Anabaena variabilis. Arch Microbiol 126:257–262
Braune W, Doehler G (1996) 15N-uptake, influenced by UV-B radiation, and pattern of amino-acid pools during akinete germination in Anabaena variabilis (Cyanobacteria). J Basic Microbiol 36:219–227
Braun-Howland EB, Nierzwicki-Bauer SA (1990) Occurrence of the 32-kDa QB-binding protein of photosystem II in vegetative cells, heterocysts and akinetes of Azolla caroliniana cyanobionts. Planta 180:361–371
Campbell EL, Hagen KD, Cohen MF, Summers ML, Meeks JC (1996) The devR gene product is characteristic of receivers of two-component regulatory systems and is essential for heterocyst development in the filamentous cyanobacterium Nostoc sp. strain ATCC 29133. J Bacteriol 178:2037–2043
Campbell EL, Summers ML, Christman H, Martin ME, Meeks JC (2007) Global gene expression patterns of Nostoc punctiforme in steady-state dinitrogen-grown heterocyst -containing cultures and at single time points during the differentiation of akinetes and hormogonia. J Bacteriol 189:5247–5256
Cardemil L, Wolk CP (1976) The polysaccharides from heterocyst and spore envelopes of a blue-green alga. Methylation analysis and structure of the backbones. J Biol Chem 251:2967–2975
Cardemil L, Wolk CP (1979) The polysaccharides from heterocyst and spore envelopes of a blue-green alga. Structure of the basic repeating unit. J Biol Chem 254:736–741
Cardemil L, Wolk CP (1981) Polysaccharides from the envelopes of heterocysts and spores from the blue-green algae Anabaena variabilis and Cylindrospermum licheniforme. J Phycol 17:234–240
Chater KF (2000) Developmental decisions during sporulation in the areal mycelium in Streptomyces. In: Brun YV, Shimkets LJ (eds) Prokaryotic Development. American Society for Microbiology, Washington, DC, pp 33–48
Chauvat F, Corre B, Herdman M, Joset-Espardellier F (1982) Energetic and metabolic requirements for the germination of akinetes of the cyanobacterium Nostoc PCC 7524. Arch Microbiol 133:44–49
Corliss J (2001) Protozoan cysts and spores. Encyclopedia of life sciences. Wileyd, Chichester
Cross T (1968) The thermophilic actinomycetes. J Appl Bacteriol 31:36–53
Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103
Cruze-Martin MA, Diaz A, Manzanal MB, Hardisson C (1989) Role of trehalose in the spores of Streptomyces. FEMS Microbiol Ecol 35:49–54
Dworkin M (1996) Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev 60:70–120
Errington J (2003) Regulation of endospore formation in Bacillus subtilis. Nat Rev Microbiol 1:117–125
Fay P (1969a) Metabolic activities of isolated spores of Anabaena cylindrica. J Exp Bot 20:100–109
Fay P (1969b) Cell differentiation and pigment composition in Anabaena cylindrica. Arch Mikrobiol 67:62–70
Fay P (1988) Viability of akinetes of the planktonic cyanobacterium Anabaena circinalis. Proc R Soc Lond B 234:283–301
Fay P, Lynn JA, Majer SC (1984) Akinete development in the planktonic blue-green alga Anabaena circinalis. Br Phycol J 19:163–174
Fisher RW, Wolk CP (1976) Substance stimulating the differentiation of spores of the blue-green alga Cylindrospermum licheniforme. Nature 259:394–395
Hadas O, Pinkas R, Delphine E, Vardi A, Kaplan A, Sukenik A (1999) Limnological and ecophysiological aspects of Aphanizomenon ovalisporum bloom in Lake Kinneret, Israel. J Plankton Res 21:1439–1453
Hense I, Beckmann A (2006) Towards a model of cyanobacteria life cycle – effects of growing and resting stages on bloom formation of N2-fixing species. Ecol Model 195:205–218
Herdman M (1987) Akinetes: structure and function. In: Fay P, van Baalen C (eds) The cyanobacteria. Elsevier, Amsterdam, pp 227–250
Herdman M (1988) Cellular differentiation: akinetes. Methods Enzymol 167:222–232
Hershkovitz N, Oren A, Cohen Y (1991) Accumulation of trehalose and sucrose in cyanobacteria exposed to matric water stress. Appl Environ Microbiol 57:645–648
Higo A, Katoh H, Ohmori K, Ikeuchi M, Ohmori M (2006) The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 152:979–987
Hill DR, Thomas EK, Helm RF, Potts M, Crowe LM, Crowe JH (1997) Extracellular polysaccharide of Nostoc commune (Cyanobacteria) inhibits fusion of membrane vesicles during desiccation. J Appl Phycol 9:237–248
Hohmann S et al (2010) Saccharomyces cerevisiae spore germination. In: Lubzens E, Cerda J, Clark M (eds) Dormancy and resistance in harsh environments. Springer, Heidelberg
Hori K, Ji O, Tanji Y, Unno H (2003) Formation, sedimentation and germination properties of Anabaena akinetes. Biochem Eng J 14:67–73
Huber AL (1985) Factors affecting the germination of akinetes of Nodularia spumigena (cyanobacteriaceae). Appl Environ Microbiol 49:73–78
Karlsson-Elfgren I, Brunberg A-K (2004) The importance of shallow sediments in the recruitment of Anabaena and Aphanizomenon (Cyanophyceae). J Phycol 40:831–836
Karlsson-Elfgren I, Rengefors K, Gustafsson S (2004) Factors regulating recruitment from the sediment to the water column in the bloom-forming cyanobacterium Gleotrichia echinulata. Freshwater Biol 49:265–273
Kaushik M, Kumar HD (1970) The effect of light on growth and development of two nitrogen fixing blue-green algae. Arch Microbiol 74:52–57
Kezhi B, Guoliang W, Cheng C (1985) Studies on the mechanism of light-dependent germination of akinetes of blue-green algae. Hydrobiologia 123:89–91
Kroos L (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet 41:13–39
Leganés F (1994) Genetic evidence that hepA gene is involved in the normal deposition of the envelope of both heterocysts and akinetes in Anabaena variabilis ATCC 29413. FEMS Microbiol Lett 123:63–67
Leganés F, Fernández-Piňas F, Wolk CP (1994) Two mutations that block heterocyst differentiation have different effects on akinete differentiation in Nostoc ellipsosporum. Mol Microbiol 12:679–684
Leganés F, Fernández-Piňas F, Wolk CP (1998) A transposition-induced mutant of Nostoc ellipsosporum implicates an arginine-biosynthetic gene in the formation of cyanophycin granules and of functional heterocysts and akinetes. Microbiol (Reading) 144:1799–1805
Li R, Watanabe M, Watanabe MM (1997) Akinete formation in planktonic Anabaena spp (Cyanobacteria) by treatment with low temperature. J Phycol 33:576–584
Livingstone D, Jaworski GHM (1980) The viability of akinetes of blue-green algae recovered from the sediments of Rostherne Mere. Br Phycol J 15:357–364
McBride MJ, Ensign JC (1987) Effects of intracellular trehalose content of Streptomyces griseus spores. J Bacteriol 169:4995–5001
Meeks JC, Campbell EL, Summers ML, Wong FCY (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178:395–403
Miller MM, Lang NJ (1968) The fine structure of akinete formation and germination in Cylindrospermum. Arch Microbiol 60:303–313
Moore D, O'Donohue M, Shaw G, Critchley C (2003) Potential triggers for akinete differentiation in an Australian strain of the cyanobacterium Cylindrospermopsis raciborskii (AWT 205/1). Hydrobiologia 506–509:175–180
Moore D, McGregor G, Shaw G (2004) Morphological changes during akinete germination in Cylindrospermopsis raciborskii (Nostocales, cyanobacteria). J Phycol 40:1098–1105
Moore D, O'Donohue M, Garnett C, Critchley C, Shaw G (2005) Factors affecting akinete differentiation in Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria). Freshwater Biol 50:345–352
Muro-Pastor AM, Valladares A, Flores E, Herrero A (2002) Mutual dependence of the expression of the cell differentiation regulatory protein HetR and the global nitrogen regulator NtcA during heterocyst development. Mol Microbiol 44:1377–1385
Nichols JM, Adams DG (1982) Akinetes. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell, Oxford, pp 387–412
Nichols JM, Adams DG, Carr NG (1980) Effect of canavanine and other amino acid analogues on akinete formation in the cyanobacterium Anabaena cylindrica. Arch Microbiol 127:67–75
Padisák J (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol 107:563–593
Padisák J (1998) Sudden and gradual responses of phytoplankton to global climate change: case studies from two large, shallow lakes (Balaton, Hungary, and the Neusiedlersee, Austria/Hungary). In: George D, Jones J, Puncochar P, Reynolds C, Sutcliffe D (eds) Management of lakes and reservoirs during global change. Kluwer, London, pp 111–125
Pandey RK, Talpasayi ERS (1981) Factors affecting germination of spores in a blue-green alga Nodularia spumigena. Acta Bot Ind 9:35–42
Pope LM, Wyss O (1970) Outer layers of the Azotobacter vinelandii cyst. J Bacteriol 102:234–239
Rai AK, Pandey GP (1981) Influence of environmental stress on the germination of Anabaena vaginicola akinetes. Ann Bot (London) 48:361–370
Rai AN, Rao VV, Singh HV (1985) The biology of cyanobacterial akinetes. J Plant Sci Res 1:1–20
Rao VV, Ghosh R, Singh HN (1987) Diazotrophic regulation of akinete development in the cyanobacterium Anabaena doliolum. New Phytol 106:161–168
Reddy PM (1983) Effects of temperature pre-treatment, desiccation and aging on the viability of spores of halophilic blue-green algae. Hydrobiol 106:235–240
Rengefors K, Gustafsson S, Ståhl-Delbanco A (2004) Factors regulating the recruitment of cyanobacterial and eukaryotic phytoplankton from littoral and profundal sediments. Aquat Microb Ecol 36:213–226
Reynolds CS (1972) Growth, gas vacuolation and buoyancy in a natural population of a planktonic blue-green alga. Freshwat Biol 2:87–106
Risser DD, Callahan SM (2008) HetF and PatA control levels of HetR in Anabaena sp. strain PCC 7120. J Bacteriol 190:7645–7654
Rother JA, Fay P (1977) Sporulation and the development of planktonic blue-green algae in two salopian meres. Proc R Soc Lond B 196:317–332
Rücker J, Tingwey E, Wiedner C, Anu C, Nixdorf B (2009) Impact of the inoculum size on the population of Nostocales cyanobacteria in temperate lakes. J Plankton Res 31:1151–1159
Sarma TA, Khattar JIS (1993) Akinete differentiation in phototrophic, photoheterotrophic and chemoheterotrophic conditions in Anabaena torulosa. Folia Microbiol 38:335–340
Setlow P (2000) Resistance of bacterial spores. In: Storez G, Hengge-Atonis R (eds) Bacterial stress responses. American Society for Microbiology, Washington, DC, pp 217–230
Sili C, Ena A, Materassi R, Vincenzini M (1994) Germination of desiccated aged akinetes of alkaliphilic cyanobacteria. Arch Microbiol 162:20–25
Simon RD (1977) Macromolecular composition of spores from the filamentous cyanobacterium Anabaena cylindrica. J Bacteriol 129:1154–1155
Simon RD (1987) Inclusion bodies in the cyanobacteria: cyanophycin, polyphosphate, and polyhedral bodies. In: Fay P, van Baalen C (eds) The Cyanobacteria: current research. Elsevier/North Holland Biomedical Press, Amsterdam, pp 199–226
Sinclair C, Whitton BA (1977) Influence of nitrogen source on morphology of Rivulariaceae (cyanophyta). J Phycol 13:335–340
Singh HN, Sunita K (1974) Biochemical study of spore germination in blue-green alga Anabaena doliolum. J Exp Bot 25:837–845
Skill SC, Smith RJ (1987) Synchronous akinete germination and heterocyst differentiation in Anabaena PCC 7937 and Nostoc PCC 6720. J Gen Microbiol 133:299–304
Socilifsky MD, Wyss O (1962) Resistance of the Azotobacter cyst. J Bacteriol 84:119–124
Ståhl-Delbanco A, Hansson LA (2002) Effects of bioturbation on recruitment of algal cells from the “seed bank” of lake sediments. Limnol Oceanogr 47:1836–1843
Stüken A, Rücker J, Endrulat T, Preussel K, Hemm M, Nixdorf B, Karsten U, Wiedner C (2006) Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45:696–703
Sukenik A, Hadas O, Stojkovic S, Malinsky-Rushansky N, Viner-Motzini Y, Beardall J (2009) Fluorescence approaches reveal variations in cellular composition during formation of akinetes in the cyanobacterium Aphanizomenon ovalisporum. Eur J Phycol 44:309–317
Sukenik A, Beardall J, Hadas O (2007) Photosynthetic characterization of developing and mature akinetes of Aphanizomenon ovalisporum (cyanoprokaryota). J Phycol 43:780–788
Summers ML, Wallis JG, Campbell EL, Meeks JC (1995) Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. J Bacteriol 177:6184–6194
Sutherland JM, Herdman M, Stewart WDP (1979) Akinetes of the cyanobacterium Nostoc PCC 7524: macromolecular composition, structure and control of differentiation. J Gen Microbiol 115:273–287
Sutherland JM, Reaston J, Stewart WDP, Herdman M (1985a) Akinetes of cyanobacterium Nostoc PCC 7524 macromolecular and biochemical changes during synchronous germination. J Gen Microbiol 131:2855–2864
Sutherland JM, Stewart WDP, Herdman M (1985b) Akinetes of the cyanobacterium Nostoc PCC 7524 morphological changes during synchronous germination. Arch Microbiol 142:269–274
Thiel T, Wolk CP (1983) Metabolic activities of isolated akinetes of the cyanobacterium Nostoc spongiaeforme. J Bacteriol 156:369–374
Thompson PA, Jameson I, Blackburn SI (2009) The influence of light quality on akinete formation and germination in the toxic cyanobacterium Anabaena circinalis. Harmful Algae 8:504–512
van den Hoek C, Mann DG, Jahns HM (1998) Algae: An introduction to phycology. Cambridge University Press, Cambridge
van Dok W, Hart BT (1996) Akinete differentiation in Anabaena circinalis (Cyanophyta). J Phycol 32:557–565
van Dok W, Hart BT (1997) Akinete germination in Anabaena circinalis (Cyanophyta). J Phycol 33:12–17
van Geel B (ed) (1986) Application of fungal and algal remains and other microfossils in palynological analyses. Wiley, Chichester, pp 497–505
van Geel B, Mur LR, Ralska-Jasiewiczowa M, Goslar T (1994) Fossil akinetes of Aphanizomenon and Anabaena as indicators for medieval phosphate-eutrophication of Lake Gosciaz (Central Poland). Rev Palaeobot Palynol 83:97–105
Wiedner C, Rücker J, Brüggemann R, Nixdorf B (2007) Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia 152:473–484
Wildermuth H (1970) Development and organization of the aerial mycelium in Streptomyces coelicolor. J Gen Microbiol 60:43–50
Wildman RB, Loescher JH, Winger CL (1975) Development and germination of akinetes of Aphanizomenon-flos-aquae. J Phycol 11:96–104
Wolk CP (1966) Evidence of a role of heterocysts in the sporulation of a blue-green alga. Am J Bot 53:260–262
Wolk CP, Simon RD (1969) Pigments and lipids of heterocysts. Planta 86:92–97
Wolk CP, Ernst A, Elhai J (1994) Heterocyst metabolism and development. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer, The Netherlands, pp 769–823
Wong FCY, Meeks JC (2001) The hetF gene product is essential to heterocyst differentiation and affects HetR function in the cyanobacterium Nostoc punctiforme. J Bacteriol 183:2654–2661
Wong FCY, Meeks JC (2002) Establishment of a functional symbiosis between the cyanobacterium Nostoc punctiforme and the bryophyte Anthoceros punctatus requires genes involved in nitrogen control and initiation of heterocyst differentiation. Microbiology 148:315–323
Wyman M, Fay P (1986) Interaction between light quality and nitrogen availability in the differentiation of akinetes in the planktonic cyanobacterium Gloeotrichia echinulata. Br Phycol J 21:147–154
Yamamoto Y (1975) Effect of desiccation on the germination of akinetes of Anabaena cylindrica. Plant Cell Physiol 16:749–752
Yamamoto Y (1976) Effect of some physical and chemical factors on the germination of akinetes of Anabaena cylindrica. J Gen App Microbiol 22:311–323
Zhang C-C, Laurent S, Sakr S, Peng L, Bédu S (2006) Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59:367–375
Zhao J, Wolk CP (2007) Developmental biology of heterocysts. In: Whitworth DE (ed) Myxobacteria: multicellularity and differentiation. ASM Press, Herndon, VA, pp 397–418
Zhou R, Wolk CP (2002) Identification of an akinete marker gene in Anabaena variabilis. J Bacteriol 184:2529–2532
Acknowledgment
Our work was supported by a EU-NEST program project No 12674 “sleeping beauty” (AS, OH), by BMBF/MOST program project No WT803/2316 (OH AS JR), and by US-NIH SCORE grant 5S06GM048680 (MLS). We thank Dr. R. Reinhardt and Dr. M. Kube from Max Planck Institute for Molecular Genetics, Berlin for their guidance and support with the molecular analysis of A. ovalisporum genome. We wish to thank two anonymous reviewers who contributed to the improvement of an earlier version by their constructive comments and suggestions.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Kaplan-Levy, R.N., Hadas, O., Summers, M.L., Rücker, J., Sukenik, A. (2010). Akinetes: Dormant Cells of Cyanobacteria. In: Lubzens, E., Cerda, J., Clark, M. (eds) Dormancy and Resistance in Harsh Environments. Topics in Current Genetics, vol 21. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12422-8_2
Download citation
DOI: https://doi.org/10.1007/978-3-642-12422-8_2
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-12421-1
Online ISBN: 978-3-642-12422-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)