Akinetes: Dormant cells of cyanobacteria

Topics in Current Genetics

Volumn 21, Issue , 2010, Pages 5-27

  Kaplan Levy, Ruth N ^a   Hadas, Ora ^a   Summers, Michael L ^b   Rücker, Jacqueline ^c   Sukenik, Assaf ^a  

^a ISRAEL OCEANOGRAPHIC AND LIMNOLOGICAL RESEARCH   (Israel)

^b CALIFORNIA STATE UNIVERSITY   (United States)

^c BRANDENBURG UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77955951694     PISSN: 16102096     EISSN: 16106970     Source Type: Book Series    
DOI: 10.1007/978-3-642-12422-8_2     Document Type: Article

References (113)

1. Adams DG, Duggan PS (1999) Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144:3-33
2. Adhikary SP (1996) Ecology of freshwater and terrestrial cyanobacteria. J Sci Ind Res 55:753-762
3. 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
4. Argueta C, Summers ML (2005) Characterization of a model system for the study of Nostoc punctiforme akinetes. Arch Microbiol 183:338-346
5. 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
6. Argueta C, Yuksek K, Patel R, Summers ML (2006) Identification of Nostoc punctiforme akineteexpressed genes using differential display. Mol Microbiol 61:748-757
7. Baker PD, Bellifemine D (2000) Environmental influences on akinete germination of Anabaena circinalis and implications for management of cyanobacterial blooms. Hydrobiologia 427: 65-73
8. 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
9. Barbiero RP, Welch EB (1992) Contribution of benthic blue-green algal recruitment to lake populations and phosphorous translocation. Freshwater Biol 27:249-260
10. Berleman JE, Bauer CE (2004) Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum. Microbiology 150:383-390
11. 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
12. Braune W (1979) C-Phycocyanin: The main photoreceptor in the light-dependent germination process of Anabaena akinetes. Arch Microbiol 122:289-296
13. Braune W (1980) Structural aspects of akinete germination in the cyanobacterium Anabaena variabilis. Arch Microbiol 126:257-262
14. 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
15. 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
16. 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
17. 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
18. Cardemil L, Wolk CP (1976) The polysaccharides from heterocyst and spore envelopes of a bluegreen alga. Methylation analysis and structure of the backbones. J Biol Chem 251:2967-2975
19. Cardemil L, Wolk CP (1979) The polysaccharides from heterocyst and spore envelopes of a bluegreen alga. Structure of the basic repeating unit. J Biol Chem 254:736-741
20. 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
21. 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
22. 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
23. Corliss J (2001) Protozoan cysts and spores. Encyclopedia of life sciences. Wileyd, Chichester
24. Cross T (1968) The thermophilic actinomycetes. J Appl Bacteriol 31:36-53
25. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73-103
26. Cruze-Martin MA, Diaz A, Manzanal MB, Hardisson C (1989) Role of trehalose in the spores of Streptomyces. FEMS Microbiol Ecol 35:49-54
27. Dworkin M (1996) Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev 60:70-120
28. Errington J (2003) Regulation of endospore formation in Bacillus subtilis. Nat Rev Microbiol 1:117-125
29. Fay P (1969a) Metabolic activities of isolated spores of Anabaena cylindrica. J Exp Bot 20:100-109
30. Fay P (1969b) Cell differentiation and pigment composition in Anabaena cylindrica. Arch Mikrobiol 67:62-70
31. Fay P (1988) Viability of akinetes of the planktonic cyanobacterium Anabaena circinalis. Proc R Soc Lond B 234:283-301
32. Fay P, Lynn JA, Majer SC (1984) Akinete development in the planktonic blue-green alga Anabaena circinalis. Br Phycol J 19:163-174
33. Fisher RW, Wolk CP (1976) Substance stimulating the differentiation of spores of the blue-green alga Cylindrospermum licheniforme. Nature 259:394-395
34. 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
35. 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
36. Herdman M (1987) Akinetes: structure and function. In: Fay P, van Baalen C (eds) The cyanobacteria. Elsevier, Amsterdam, pp 227-250
37. Herdman M (1988) Cellular differentiation: akinetes. Methods Enzymol 167:222-232
38. 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
39. 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
40. 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
41. 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
42. Hori K, Ji O, Tanji Y, Unno H (2003) Formation, sedimentation and germination properties of Anabaena akinetes. Biochem Eng J 14:67-73
43. Huber AL (1985) Factors affecting the germination of akinetes of Nodularia spumigena (cyanobacteriaceae). Appl Environ Microbiol 49:73-78
44. 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
45. 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
46. 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
47. 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
48. Kroos L (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet 41:13-39
49. 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
50. 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
51. 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
52. Li R, Watanabe M, Watanabe MM (1997) Akinete formation in planktonic Anabaena spp (Cyanobacteria) by treatment with low temperature. J Phycol 33:576-584
53. 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
54. McBride MJ, Ensign JC (1987) Effects of intracellular trehalose content of Streptomyces griseus spores. J Bacteriol 169:4995-5001
55. Meeks JC, Campbell EL, Summers ML, Wong FCY (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178:395-403
56. Miller MM, Lang NJ (1968) The fine structure of akinete formation and germination in Cylindrospermum. Arch Microbiol 60:303-313
57. 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
58. Moore D, McGregor G, Shaw G (2004) Morphological changes during akinete germination in Cylindrospermopsis raciborskii (Nostocales, cyanobacteria). J Phycol 40:1098-1105
59. 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
60. 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
61. Nichols JM, Adams DG (1982) Akinetes. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell, Oxford, pp 387-412
62. 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
63. 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
64. 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
65. Pandey RK, Talpasayi ERS (1981) Factors affecting germination of spores in a blue-green alga Nodularia spumigena. Acta Bot Ind 9:35-42
66. Pope LM, Wyss O (1970) Outer layers of the Azotobacter vinelandii cyst. J Bacteriol 102:234-239
67. Rai AK, Pandey GP (1981) Influence of environmental stress on the germination of Anabaena vaginicola akinetes. Ann Bot (London) 48:361-370
68. Rai AN, Rao VV, Singh HV (1985) The biology of cyanobacterial akinetes. J Plant Sci Res 1:1-20
69. Rao VV, Ghosh R, Singh HN (1987) Diazotrophic regulation of akinete development in the cyanobacterium Anabaena doliolum. New Phytol 106:161-168
70. 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
71. 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
72. Reynolds CS (1972) Growth, gas vacuolation and buoyancy in a natural population of a planktonic blue-green alga. Freshwat Biol 2:87-106
73. Risser DD, Callahan SM (2008) HetF and PatA control levels of HetR in Anabaena sp. strain PCC 7120. J Bacteriol 190:7645-7654
74. 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
75. R€ucker 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
76. Sarma TA, Khattar JIS (1993) Akinete differentiation in phototrophic, photoheterotrophic and chemoheterotrophic conditions in Anabaena torulosa. Folia Microbiol 38:335-340
77. 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
78. Sili C, Ena A, Materassi R, Vincenzini M (1994) Germination of desiccated aged akinetes of alkaliphilic cyanobacteria. Arch Microbiol 162:20-25
79. Simon RD (1977) Macromolecular composition of spores from the filamentous cyanobacterium Anabaena cylindrica. J Bacteriol 129:1154-1155
80. 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
81. Sinclair C, Whitton BA (1977) Influence of nitrogen source on morphology of Rivulariaceae (cyanophyta). J Phycol 13:335-340
82. Singh HN, Sunita K (1974) Biochemical study of spore germination in blue-green alga Anabaena doliolum. J Exp Bot 25:837-845
83. 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
84. Socilifsky MD, Wyss O (1962) Resistance of the Azotobacter cyst. J Bacteriol 84:119-124
85. 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
86. St€uken A, R€ucker 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
87. 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
88. Sukenik A, Beardall J, Hadas O (2007) Photosynthetic characterization of developing and mature akinetes of Aphanizomenon ovalisporum (cyanoprokaryota). J Phycol 43:780-788
89. 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
90. Sutherland JM, Herdman M, StewartWDP (1979) Akinetes of the cyanobacterium Nostoc PCC 7524: macromolecular composition, structure and control of differentiation. JGen Microbiol 115:273-287
91. Sutherland JM, Reaston J, Stewart WDP, HerdmanM(1985a) Akinetes of cyanobacterium Nostoc PCC 7524 macromolecular and biochemical changes during synchronous germination. J Gen Microbiol 131:2855-2864
92. Sutherland JM, Stewart WDP, Herdman M (1985b) Akinetes of the cyanobacterium Nostoc PCC 7524 morphological changes during synchronous germination. Arch Microbiol 142:269-274
93. Thiel T, Wolk CP (1983) Metabolic activities of isolated akinetes of the cyanobacterium Nostoc spongiaeforme. J Bacteriol 156:369-374
94. 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
95. van den Hoek C, Mann DG, Jahns HM (1998) Algae: An introduction to phycology. Cambridge University Press, Cambridge
96. van Dok W, Hart BT (1996) Akinete differentiation in Anabaena circinalis (Cyanophyta). J Phycol 32:557-565
97. van Dok W, Hart BT (1997) Akinete germination in Anabaena circinalis (Cyanophyta). J Phycol 33:12-17
98. van Geel B (ed) (1986) Application of fungal and algal remains and other microfossils in palynological analyses. Wiley, Chichester, 497-505
99. 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
100. Wiedner C, R€ucker J, Br€uggemann R, Nixdorf B (2007) Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia 152:473-484
101. Wildermuth H (1970) Development and organization of the aerial mycelium in Streptomyces coelicolor. J Gen Microbiol 60:43-50
102. Wildman RB, Loescher JH, Winger CL (1975) Development and germination of akinetes of Aphanizomenon-flos-aquae. J Phycol 11:96-104
103. Wolk CP (1966) Evidence of a role of heterocysts in the sporulation of a blue-green alga. Am J Bot 53:260-262
104. Wolk CP, Simon RD (1969) Pigments and lipids of heterocysts. Planta 86:92-97
105. 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
106. 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
107. 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
108. 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
109. Yamamoto Y (1975) Effect of desiccation on the germination of akinetes of Anabaena cylindrica. Plant Cell Physiol 16:749-752
110. 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
111. 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
112. Zhao J, Wolk CP (2007) Developmental biology of heterocysts. In: Whitworth DE (ed) Myxobacteria: multicellularity and differentiation. ASM Press, Herndon, VA, pp 397-418
113. Zhou R, Wolk CP (2002) Identification of an akinete marker gene in Anabaena variabilis. J Bacteriol 184:2529-2532