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Ultrastructural Plasticity of Cyanobacteria in Natural Symbioses with Plants

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Ultrastructural Plasticity of Cyanobacteria

Abstract

This chapter is dedicated to investigation of ultrastructural plasticity cyanobacteria in natural symbioses with liverwort Blasia pusilla and several species of cycad plants. According to the result presented therein, morphological and structural features of cyanobacteria in symbioses with higher plants suggest that these microorganisms possess previously unstudied or unknown physiological traits which appear within symbiosis. The evidence obtained in studies of Nostoc in natural symbioses as well as in model associations with higher plants together with the data on formation of L-form-like cells in other species reviewed in the book outlined a new field of symbiology dealing with the occurrence of L-transformation of cyanobiont in symbioses. Furthermore, diverse functional specificity of the CWDF within cyanobiont populations was determined. Special attention is paid to the novel phenomenon of the mass deposition in cytoplasm and transport to vesicles formed by cytoplasmic membrane of exopolysaccharides of symbiotic cyanobacteria featuring defective cell wall. Results presented in this chapter suggest that specialized cells including vegetative forms and heterocysts in populations of cyanobacteria adapted to the conditions of life in symbiosis with plants presumably have modified mechanisms of the synthesis and export of these compounds.

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References

  • Abdelahad N, Bazzichelli G, Ventola F (1984) An electron microscopic investigation on granules observed in the sheath of Nostoc commune. Arch Hydrobiol Suppl 67(2):205–211

    Google Scholar 

  • Adams DG, Duggan PS (2008) Cyanobacteria–bryophyte symbioses. J Exp Bot 59(5):1047–1058. doi:10.1093/jxb/ern005

    PubMed  CAS  Google Scholar 

  • Adams DG, Duggan PS (2012) Signalling in cyanobacteria–plant pymbioses. In: Perotto S, Baluška F (eds.) Signaling and communication in plant symbiosis, signaling and communication in plants 11. Springer, Berlin, Heidelberg. doi:10.1007/978-3-642-32781-0_5

  • Ahern CP, Staff IA (1994) Symbiosis in cycads: the origin and development of coralloid roots in Macrozamia communis (Cycadaceae). Am J Bot 18:1559–1570

    Google Scholar 

  • Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1994) Molecular biology of the cell. Garland, New York

    Google Scholar 

  • Baron-Epel O, Gharyal PK, Schindler M (1988) Pectins as mediators of wall porosity in soybean cells. Planta 175(3):389–395. doi:10.1007/BF00396345

    CAS  Google Scholar 

  • Baulina OI (2008) Population cytology and its role in research of life activity of prokaryotes. Mosc Uni Bio Sci Bull 63(1):32–39. doi:10.1007/s11966-008-1006-8

    Google Scholar 

  • Baulina OI, Gorelova OA, Lobakova ES (2009) The exopolysaccharides of the symbiotic cyanobacteria: the possibilities of the modification of their synthesis and export (in Russian). Byulleten Moskovskogo obshchestva ispytatelei prirody Otdel biologicheskii 114(2 Supplement 1 Physiology and genetics of microorganisms in natural and experimental systems):3–6

    Google Scholar 

  • Baulina OI, Gorelova OA, Lobakova ES (2011) Exopolysaccharide production by cell wall deficient forms of symbiotic cyanobacteria. In: Abstracts of the 4th congress of European microbiologists FEMS 2011, Geneva, Switzerland, 26–30 June 2011

    Google Scholar 

  • Baulina OI, Gorelova OA, Lobakova ES, Gusev MV, Korzhenevskaya TG (2000a) Cyanobacteria with a reduced cell wall in natural and model plant symbioses. In: Weber HC, Imhof S, Zeuske D (eds.) Programs, abstracts and papers of the third International congress on symbiosis, Philipps University of Marburg, Germany, 13–19 Aug 2000

    Google Scholar 

  • Baulina OI, Lobakova ES (2002) Ultrastructure of the reduced cell wall forms of cyanobionts of cycad plants (in Russian). In: Abstracts of the 2nd international conference on plant anatomy and morphology, St.- Petersburg, 14–18 Oct 2002

    Google Scholar 

  • Baulina OI, Lobakova ES (2003a) Atypical cell forms overproducing extracellular substances in populations of cycad cyanobionts. Microbiology (Transl) 72(6):701–712. doi:10.1023/B:MICI.0000008373.16642.e7

    CAS  Google Scholar 

  • Baulina OI, Lobakova ES (2003b) Heterocysts with reduced cell walls in populations of cycad cyanobionts. Microbiology (Transl) 72(6):713–722. doi:10.1023/B:MICI.0000008374.76257.d5

    CAS  Google Scholar 

  • Baulina OI, Lobakova ES (2003c) The symbiotic cyanobacteria—over-producers of extracellular substances. In: Abstracts of the 11th international congress on molecular plant-microbe interactions molecular plant-microbe interactions: new bridges between past and future, St.-Petersburg, Russia, 18–26 July 2003

    Google Scholar 

  • Baulina OI, Lobakova ES (2005) Ultrastructural features of intracellular synthesis of acidic polysaccharides by symbiotic cyanobacteria with reduced cell wall (in Russian). In: Proceedings of the All-Russia symposium with international participation autotrophic microorganisms, Moscow State University, 21–24 Dec 2005

    Google Scholar 

  • Baulina OI, Titel K, Gorelova OA, Malai OV, Ehwald R (2008) Permeability of cyanobacterial mucous surface structures for macromolecules. Microbiology (Transl) 77(2):198–205. doi:10.1134/S0026261708020136

    CAS  Google Scholar 

  • Baulina OI, Titel K, Malay OV, Gorelova OA (2000b) The study of permeability of the mucous surface structures of cyanobacteria for neutral hydrophilic macromolecules (in Russian). In: Abstracts of the conference problems of ecology and physiology of microorganisms, Lomonosov Moscow State University, Moscow, 21 Dec 1999

    Google Scholar 

  • Bergman B, Ran L, Adams DG (2008) Cyanobacterial-plant symbioses: signaling and development In: Herrero A, Flores E (eds.) The cyanobacteria. Molecular biology, genomics and evolution. Caister Academic Press, Norfolk

    Google Scholar 

  • Boulnois GJ, Jann K (1989) Bacterial polysaccharide capsule synthesis, export and evolution of structural diversity. Mol Microbiol 3(12):1819–1823. doi:10.1111/j.1365-2958.1989.tb00168.x

    PubMed  CAS  Google Scholar 

  • Braun E, Bachofen R (2004) Homoserine-lactones and microcystin in cyanobacterial assemblages in Swiss lakes. Hydrobiologia 522(1):271–280. doi:10.1023/B:HYDR.0000029968.70297.c3

    CAS  Google Scholar 

  • Costa JL, Lindblad P (2002) Cyanobacteria in symbiosis with cycads. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Costa JL, Romero EM, Lindblad P (2004) Sequence based data supports a single Nostoc strain in individual coralloid roots of cycads. FEMS Microbiol Ecol 49(3):481–487. doi:10.1016/j.femsec.2004.05.001

    PubMed  CAS  Google Scholar 

  • Costerton JW, Cheng K, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Ann Rev Microbiol 41(1):435–464

    CAS  Google Scholar 

  • Cuthbertson L, Kos V, Whitfield C (2010) ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev 74(3):341–362. doi:10.1128/MMBR.00009-10

    PubMed  CAS  Google Scholar 

  • Cuthbertson L, Mainprize IL, Naismith JH, Whitfield C (2009) Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in gram-negative bacteria. Microbiol Mol Biol Rev 73(1):155–177. doi:10.1128/MMBR.00024-08

    PubMed  CAS  Google Scholar 

  • Danilova MF, Barmicheva EM (1980) Root cap. (in Russian) In: Danilova MF, Kozubov GM (eds) Atlas of plant tissue ultrastructure. Karelia, Petrozavodsk

    Google Scholar 

  • Davey ME, O'Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64(4):847-867. doi:10.1128/MMBR.64.4.847-867.2000

    PubMed  CAS  Google Scholar 

  • Demuth DR, Lamont RJ (eds) (2006) Bacterial cell-to-cell communication: role in virulence and pathogenesis. Cambridge University Press, Cambridge

    Google Scholar 

  • Dittmann E, Glauβer Y, Hisberguer M, Tandeau de Marsac N, Börner T (2002) Microcystin—a cyanobacterial toxin with intercellular signalling function? In: Abstracts of the EURESCO conference Bacterial neural networks (intracellular signalling), Obernai, France, 7–12 June 2002

    Google Scholar 

  • Drews G (1973) Fine structure and chemical composition of the cell envelopes. In: Carr NG, Whitton BA (eds) The biology of blue-green algae. Blackwell, Oxford

    Google Scholar 

  • Duckett JG, Prasad A, Davies DA, Walker S (1977) A cytological analysis of the Nostoc-bryophyte relationship. New Phytol 79:349–362

    Google Scholar 

  • Dudman WF (1977) The role of surface polysaccharides in natural environments. In: Sutherland IW (ed) Surface carbohydrates of the prokaryotic cell. Academic Press, New York

    Google Scholar 

  • Dunn JH, Wolk CP (1970) Composition of the cellular envelopes of Anabaena cylindrica. J Bacteriol 103(1):153–158

    PubMed  CAS  Google Scholar 

  • Fedorenko TA, Lobakova ES, Baulina OI (2003) Features of the photosynthetic electron transport chain of cyanobionts of the cycads’ Ceratozamia mexicana and Encephalartos altensteinii apogeotropic roots (in Russian). In: Abstracts of the 5th congress of the Russian society of plant physiologists and the international conference plant physiology—the basis of phytobiotechnology, Penza, Russia, 15–21 Sept 2003

    Google Scholar 

  • Fjerdingstad E, Fjerdingstad E, Fjerdingstad EJ (1979) Evidence for the presence of collagen in the sheaths of a blue-green alga. An electron-microscopical and histochemical study of Scytonema myochrous status petalonemoides. Algological Studies/Archiv für Hydrobiologie. Suppl Vol 24:307–323

    Google Scholar 

  • Forni C, Haegi A, Del Gallo M (1998) Polysaccharide composition of the mucilage of Azolla algal packets. Symbiosis 24:303–314

    CAS  Google Scholar 

  • Geyer G (1973) Ultrahistochemie (in German). VEB Gustav Fischer Verlag, Jena

    Google Scholar 

  • Golden SS (2003) Think like a bacterium. EMBO Rep 4(1):15–17. doi:10.1038/sj.embor.embor702

    PubMed  CAS  Google Scholar 

  • Gorelova OA (2001) Surface ultrastructure of the heteromorphic cells of Nostoc muscorum CALU 304 in a mixed culture with the Rauwolfia callus tissue. Microbiology (Transl) 70(3):285–294. doi:10.1023/A:1010447109864

    CAS  Google Scholar 

  • Gorelova OA (2006) Communication of cyanobacteria with plant partners during association formation. Microbiology (Transl) 75(4):465–469. doi:10.1134/S0026261706040163

    CAS  Google Scholar 

  • Gorelova OA, Baulina OI (2009) Ultrastructure of cyanobacterium Nostoc sp. f. Blasia cell forms in persisting populations. Microbiology (Transl) 78(5):609–617. doi:10.1134/S0026261709050130

    CAS  Google Scholar 

  • Gorelova OA, Baulina OI, Shchelmanova AG, Korzhenevskaya TG, Gusev MV (1996) Heteromorphism of the cyanobacterium Nostoc sp., a microsymbiont of the Blasia pusilla moss. Microbiology (Transl) 65(6):719–726

    Google Scholar 

  • Gorelova OA, Korzhenevskaya TG, Gusev MV (1995) Formation and oriented propagation of cyanobacterial hormogonia in model systems with higher plant tissues. Mosc Uni Bio Sci Bull Vestnik Moskovskogo Universiteta Biologiya 50:17–25

    Google Scholar 

  • Gorelova OA, Shchelmanova AG, Baulina OI, Korzhenevskaya TG (1992) Ultrastructure of the symbiotic cyanobacteria Nostoc sp. populations (in Russian). In: Abstracts of the 14th conference on electron microscopy (biology, medicine), Chernogolovka, Russia, 1–5 June 1992

    Google Scholar 

  • Grilli Caiola M (1974) A light and electron microscopic study of the blue-green algae living either in the coralloid roots of «Macrozamia communis» or isolated in culture. Plant Biosystem 108(3–4):161–173. doi:10.1080/11263507409426358

    Google Scholar 

  • Grilli Caiola M (1975a) A light and electron microscopic study of blue-green algae growing in the coralloid-roots of Encephalartos altensteinii and in culture. Phycologia 14(1):25–33. doi:10.2216/i0031-8884-14-1-25.1

    Google Scholar 

  • Grilli Caiola M (1975b) Structural and ultrastructural aspects of blue-green algae growing in the coralloid roots of Dioon edule and in culture. Phycos 14:29–34

    Google Scholar 

  • Grilli Caiola M (1980) On the phycobionts of the cycad coralloid roots. New Phytol 85(4):537–544. doi:10.1111/j.1469-8137.1980.tb00769.x

    Google Scholar 

  • Grobbelaar N, Joubert L, Chang D, Coetzee J (1988) In situ EM studies of the endophytes of cycad (Encephalartos spp.) coralloid roots. In: Bothe H, de Bruijn FJ, Newton WE (eds) Nitrogen fixation: hundred years after. Gustav Fischer, Stuttgart

    Google Scholar 

  • Gusev MV, Baulina OI, Gorelova OA, Lobakova ES, Korzhenevskaya TG (2002) Artificial cyanobacterium-plant symbioses. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer Academic Publishers Dordrecht, The Netherlands

    Google Scholar 

  • Hellingwerf KJ (2004) A network of net-workers: report of the Euresco conference on ‘bacterial neural networks’ held at San Feliu (Spain) from 8 to 14 May 2004. Mol Microbiol 54(1):2–13. doi:10.1111/j.1365-2958.2004.04321.x

    PubMed  CAS  Google Scholar 

  • Hill DR, Peat A, Potts M (1994) Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc commune (Cyanobacteria). Protoplasma 182(3):126–148. doi:10.1007/BF01403474

    CAS  Google Scholar 

  • Hoare DS, Ingram LO, Thurston EL, Walkup R (1971) Dark heterotrophic growth of an endophytic blue-green alga. Arch Microbiol 78(4):310–321. doi:10.1007/BF00412271

    CAS  Google Scholar 

  • Hoiczyk E (1998) Structural and biochemical analysis of the sheath of Phormidium uncinatum. J Bacteriol 180(15):3923–3932

    PubMed  CAS  Google Scholar 

  • Hoiczyk E, Baumeister W (1995) Envelope structure of four gliding filamentous cyanobacteria. J Bacteriol 177(9):2387–2395

    PubMed  CAS  Google Scholar 

  • Hoiczyk E, Baumeister W (1998) The junctional pore complex, a prokaryotic secretion organelle, is the molecular motor underlying gliding motility in cyanobacteria. Curr Biol 8(21):1161–1168. doi:10.1016/S0960-9822(07)00487-3

    PubMed  CAS  Google Scholar 

  • Hoiczyk E, Hansel A (2000) Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J Bacteriol 182(5):1191–1199. doi:10.1128/JB.182.5.1191-1199.2000

    PubMed  CAS  Google Scholar 

  • Huang F, Hedman E, Funk C, Kieselbach T, Schröder WP, Norling B (2004) Isolation of outer membrane of Synechocystis sp. PCC 6803 and its proteomic characterization. Mol Cell Proteomics 3(6):586–595. doi:10.1074/mcp.M300137-MCP200

    PubMed  CAS  Google Scholar 

  • Huang F, Parmryd I, Nilsson F, Persson AL, Pakrasi HB, Andersson B, Norling B (2002) Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins. Mol Cell Proteomics 1(12):956–966. doi:10.1074/mcp.M200043-MCP200

    PubMed  CAS  Google Scholar 

  • Jagendorf AT, Michaels A (1990) Rough thylakoids: translation on photosynthetic membranes. Plant Sci 71(2):137–145. doi:10.1016/0168-9452(90)90001-5

    CAS  Google Scholar 

  • Johansson C (1994) Establishment of the Gunnera-Nostoc symbiosis. Stockholm University, Dissertation

    Google Scholar 

  • Johansson C, Bergman B (1992) Early events during the establishment of the Gunnera/Nostoc symbiosis. Planta 188(3):403–413

    Google Scholar 

  • Joubert L, Grobbelaar N, Coetzee J (1989) In situ studies of the ultrastructure of the cyanobacteria in the coralloid roots of Encephalartos arenarius, E. transvenosus and E. woodii (Cycadales). Phycologia 28(2):197–205. doi:10.2216/i0031-8884-28-2-197.1

    Google Scholar 

  • Jürgens UJ, Weckesser J (1985) The fine structure and chemical composition of the cell wall and sheath layers of cyanobacteria. Ann Inst Pasteur/Microbiol 136A:41–44

    Google Scholar 

  • Kanekiyo K, Lee JB, Hayashi K, Takenaka H, Hayakawa Y, Endo S, Hayashi T (2005) Isolation of an antiviral polysaccharide, nostoflan, from a terrestrial cyanobacterium, Nostoc flagelliforme. J Nat Prod 68(7):1037–1041. doi:10.1021/np050056c

    PubMed  CAS  Google Scholar 

  • Kaplan HB, Plamann L (1996) A Myxococcus xanthus cell density-sensing system required for multicellular development. FEMS Microbiol Lett 139(2–3):89–95. doi:10.1111/j.1574-6968.1996.tb08185.x

    PubMed  CAS  Google Scholar 

  • Kaprelyants AS, Antonyuk LP (2006) The conference “microbial communication”. Microbiology (Transl) 75(4):371–373. doi:10.1134/S0026261706040011

    CAS  Google Scholar 

  • Kehr JC, Zilliges Y, Springer A, Disney MD, Ratner DD, Bouchier C, Seeberger PH, De Marsac NT, Dittmann E (2006) A mannan binding lectin is involved in cell–cell attachment in a toxic strain of Microcystis aeruginosa. Mol Microbiol 59(3):893–906. doi:10.1111/j.1365-2958.2005.05001.x

    PubMed  CAS  Google Scholar 

  • Kellenberger E, Ryter A, Sechaud J (1958) Electron microscope study of DNA-containing plasms. J Biophys Biochem Cytol 4(6):671–678. doi:10.1083/jcb.4.6.671

    PubMed  CAS  Google Scholar 

  • Khmel IA (2006) Quorum-sensing regulation of gene expression: fundamental and applied aspects and the role in bacterial communication. Microbiology (Transl) 75(4):390–397. doi:10.1134/S0026261706040047

    CAS  Google Scholar 

  • Kimura G, Nakano T (1990) Reconstitution of the Blasia-Nostoc symbiotic association under axenic conditions. Nova Hedwigia 50:191–200

    Google Scholar 

  • Koksharova O, Schubert M, Shestakov S, Cerff R (1998) Genetic and biochemical evidence for distinct key functions of two highly divergent GAPDH genes in catabolic and anabolic carbon flow of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 36(1):183–194. doi:10.1023/A:1005925732743

    PubMed  CAS  Google Scholar 

  • Korolev NP (1984) Results of science and technology. Ser. Common problems of physico-chemical biology (in Russian), vol 1. The functions of lectins in the cell. VINITI

    Google Scholar 

  • Korzhenevskaya TG, Baulina OI, Gorelova OA, Lobacova ES, Butenko RG, Gusev MV (1993) Artificial syncyanoses: the potential for modeling and analysis of natural symbioses. Symbiosis 15(1–2):77–103

    Google Scholar 

  • Kröncke KD, Boulnois G, Roberts I, Bitter-Suermann D, Golecki JR, Jann B, Jann K (1990a) Expression of the Escherichia coli K5 capsular antigen: immunoelectron microscopic and biochemical studies with recombinant E. coli. J Bacteriol 172(2):1085–1091

    PubMed  Google Scholar 

  • Kröncke KD, Golecki JR, Jann K (1990b) Further electron microscopic studies on the expression of Escherichia coli group II capsules. J Bacteriol 172(6):3469–3472

    PubMed  Google Scholar 

  • Lamont HC (1969) Sacrificial cell death and trichome breakage in an oscillatoriacean blue-green alga: the role of murein. Arch Microbiol 69(3):237–259. doi:10.1007/BF00408976

    Google Scholar 

  • Lang NJ, Fay P (1971) The heterocysts of blue-green algae. II. Details of ultrastructure. Proc Royal Soc Lond Ser B Bio Sci 178:193–203

    Google Scholar 

  • Leak LV (1967) Fine structure of the mucilaginous sheath of Anabaena sp. J Ultrastruct Res 21(1):61–74. doi:10.1016/S0022-5320(67)80006-6

    PubMed  CAS  Google Scholar 

  • Liberton M, Austin JR II, Berg RH, Pakrasi HB (2011) Unique thylakoid membrane architecture of a unicellular N2-fixing cyanobacterium revealed by electron tomography. Plant Physiol 155(4):1656–1666. doi:10.1104/pp.110.165332

    PubMed  CAS  Google Scholar 

  • Liberton M, Howard Berg R, Heuser J, Roth R, Pakrasi HB (2006) Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Protoplasma 227(2):129–138. doi:10.1007/s00709-006-0145-7

    Google Scholar 

  • Lindblad P, Bergman B, Hofsten AV, Hallbom L, Nylund JE (1985) The cyanobacterium-Zamia symbiosis: an ultrastructural study. New Phytologist 101:707–716

    Google Scholar 

  • Lobakova E, Dubravina G, Zagoskina N (2004) Formation of phenolic compounds in apogeotropic roots of cycad plants. Russ J Plant Physiol 51(4):486–493

    CAS  Google Scholar 

  • Lobakova ES (2004) The associative microorganisms of plant symbioses, Doctoral dissertation. Moscow State University, Moscow

    Google Scholar 

  • Lobakova ES, Baulina OI (2001) The morphology and ultrastructure of symbiotic cyanobacteria in apogeotropic roots of cycad plants in the dormant period (in Russian). In: Abstracts of the All-Russian conference agricultural microbiology in XIX–XXI centuries, St.-Petersburg, Russia, 14–19 June 2001

    Google Scholar 

  • Luft JH (1971) Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat Rec 171(3):347–368. doi:10.1002/ar.1091710302

    PubMed  CAS  Google Scholar 

  • Margheri MC, Allotta G (1993) Homoacetic fermentation in the cyanobacterium Nostoc sp. strain Cc from Cycas circinalis. FEMS Microbiol Lett 111(2–3):213–217

    CAS  Google Scholar 

  • Meeks JC (1998) Symbiosis between nitrogen-fixing cyanobacteria and plants. Bioscience 48(4):266–276

    Google Scholar 

  • Meeks JC, Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66(1):94–121. doi:10.1128/MMBR.66.1.94-121.2002

    PubMed  CAS  Google Scholar 

  • Merzlyak M, Razi Naqvi K (2000) On recording the true absorption spectrum and the scattering spectrum of a turbid sample: application to cell suspensions of the cyanobacterium Anabaena variabilis. J Photochem Photobiol B Biol 58(2–3):123–129. doi:org/10.1016/S1011-1344(00)00114-7

    CAS  Google Scholar 

  • Moezelaar R, Stal L (1997) A comparison of fermentation in the cyanobacterium Microcystis PCC7806 grown under a light/dark cycle and continuous light. Eur J Phycol 32(4):373–378. doi:10.1080/09670269710001737309

    Google Scholar 

  • Mullineaux CW (2008) Biogenesis and dynamics of thylakoid membranes and the photosynthetic apparatus. In: Herrero A, Flores E (eds.) The cyanobacteria. Molecular biology, genomics and evolution. Caister Academic Press, Norfolk

    Google Scholar 

  • Nathanielsz CP, Staff IA (1975) A mode of entry of blue-green algae into the apogeotropic roots of Macrozamia communis. Am J Bot 62:232–235

    Google Scholar 

  • Nobles DR, Romanovicz DK, Brown Jr RM (2001) Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase? Plant Physiol 127(2):529–542. doi:10.1104/pp.010557

    PubMed  CAS  Google Scholar 

  • Obukowicz M, Schaller M, Kennedy GS (1981) Ultrastructure and phenolic histochemistry of the Cycas revoluta-Anabaena symbiosis. New Phytologist 87:751–759

    Google Scholar 

  • Oleskin AV, Botvinko IV, Tsavkelova EA (2000) Colonial organization and intercellular communication in microorganisms. Microbiology (Transl) 69(3):249–265. doi:10.1007/BF02756730

    CAS  Google Scholar 

  • Painter TJ (1995) Biofertilizers: exceptional calcium binding affinity of a sheath proteoglycan from the blue-green soil alga Nostoc calcicola. Carbohydr Polym 26(3):231–233

    CAS  Google Scholar 

  • Parker DL, Schram BR, Plude JL, Moore RE (1996) Effect of metal cations on the viscosity of a pectin-like capsular polysaccharide from the cyanobacterium Microcystis flos-aquae C3–40. Appl Environ Microbiol 62(4):1208–1213

    PubMed  CAS  Google Scholar 

  • Pavelka MS Jr, Hayes SF, Silver RP (1994) Characterization of KpsT, the ATP-binding component of the ABC-transporter involved with the export of capsular polysialic acid in Escherichia coli K1. J Biol Chem 269(31):20149–20158

    PubMed  CAS  Google Scholar 

  • Pavlova IB (1999) Patterns of bacterial population development in the environment (electron microscopy study). Doctoral dissertation, All-Russian Scientific Research Institute of Veterinary Sanitation, Hygiene and Ecology of the Russian Academy of Agricultural Sciences, Moscow

    Google Scholar 

  • Raff M (1998) Cell suicide for beginners. Nature 396(6707):119

    PubMed  CAS  Google Scholar 

  • Rai AN, Söderbäck E, Bergman B (2000) Tansley review no. 116 cyanobacterium–plant symbioses. New Phytologist 147(3):449–481. doi:10.1046/j.1469-8137.2000.00720.x

  • Rai AN (ed) (1990) Handbook of symbiotic cyanobacteria. CRC Press, Boca Raton, Florida

    Google Scholar 

  • Rai AN, Bergman B, Rasmussen U (eds.) (2002) Cyanobacteria in symbiosis. Kluwer Academic Publishers, Dordrecht, the Netherlands

    Google Scholar 

  • Reddy KJ, Soper BW, Tang J, Bradley RL (1996) Phenotypic variation in exopolysaccharide production in the marine, aerobic nitrogen-fixing unicellular cyanobacterium Cyanothece sp. World J Microbiol Biotechnol 12:311–318. doi:10.1007/BF00340206

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17(1):208–212

    PubMed  CAS  Google Scholar 

  • Romanova YM, Smirnova TA, Andreev AL, Il’ina TS, Didenko LV, Gintsburg AL (2006) Formation of biofilms as an example of the social behavior of bacteria. Microbiology (Transl) 75(4):481–485. doi:10.1134/S0026261706040199

    CAS  Google Scholar 

  • Sarcina M, Adams DG, Mullineaux CW (2000) Cell-cell communication in anabaena cylindrica In: Abstracts of 10th international sympjsium on phototrophic prokaryotes, Barcelona, Spain, 26–31 Aug 2000

    Google Scholar 

  • Schatz D, Keren Y, Vardi A, Sukenik A, Carmeli S, Börner T, Dittmann E, Kaplan A (2007) Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins. Environ Microbiol 9(4):965–970. doi:10.1111/j.1462-2920.2006.01218.x

    PubMed  CAS  Google Scholar 

  • Shah V, Ray A, Garg N, Madamwar D (2000) Characterization of the extracellular polysaccharide produced by a marine cyanobacterium, Cyanothece sp. ATCC 51142, and its exploitation toward metal removal from solutions. Curr Microbiol 40(4):274–278. doi:10.1007/s002849910054

    PubMed  CAS  Google Scholar 

  • Sharif DI, Gallon J, Smith CJ (2008) Quorum sensing in cyanobacteria: N-octanoyl-homoserine lactone release and response, by the epilithic colonial cyanobacterium Gloeothece PCC6909. ISME J 2(12):1171–1182. doi:10.1038/ismej.2008.68

    PubMed  CAS  Google Scholar 

  • Shibaev VN (1982) The biosynthesis of the carbon chains of polymers constituting the bacterial cell surface (in in Russian). Uspekhi biologicheskoy khimii 23:61–101

    Google Scholar 

  • Söderbäck E, Lindblad P, Bergman B (1990) Developmental patterns related to nitrogen fixation in the Nostoc-Gunnera magellanica Lam. symbiosis. Planta 182(3):355–362. doi:10.1007/BF02411385

    Google Scholar 

  • Steenbergen SM, Vimr ER (2008) Biosynthesis of the Escherichia coli K1 group 2 polysialic acid capsule occurs within a protected cytoplasmic compartment. Mol Microbiol 68(5):1252–1267. doi:10.1111/j.1365-2958.2008.06231.x

    PubMed  CAS  Google Scholar 

  • Surette MG (2002) Interaction and communication in mixed microbial communities In: Abstracts of the EURESCO conference bacterial neural networks (intracellular signalling), Obernai, France, 7–12 June 2002

    Google Scholar 

  • Sutherland IW (2002) Biofilms—formation, structure and interactions! In: Abstracts of the EURESCO conference Bacterial neural networks (intracellular signalling), Obernai, France, 7–12 June 2002

    Google Scholar 

  • Towata EM (1985) Morphometric and cytochemical ultrastructural analyses of the Gunnera kaalensis/Nostoc symbiosis. Bot Gazette 146(3):293–301

    Google Scholar 

  • van de Meene AML, Hohmann-Marriott MF, Vermaas WFJ, Roberson RW (2006) The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 184(5):259–270. doi:10.1007/s00203-005-0027-y

    Google Scholar 

  • Vicente-García V, Ríos-Leal E, Calderón-Domínguez G, Cañizares-Villanueva RO, Olvera-Ramírez R (2004) Detection, isolation, and characterization of exopolysaccharide produced by a strain of Phormidium 94a isolated from an arid zone of Mexico. Biotechnol Bioeng 85(3):306–310. doi:10.1002/bit.10912

    PubMed  Google Scholar 

  • Vimr ER, Steenbergen SM (2009) Early molecular-recognition events in the synthesis and export of group 2 capsular polysaccharides. Microbiology 155(1):9–15. doi:10.1099/mic.0.023564-0

    PubMed  CAS  Google Scholar 

  • Vysotskii VV, Bakulina NA, Vaisman IS, Efimova OG, Kotlyarov GA (1984) The structural principles of microbial populations as polymorphic multicellular systems (in Russian). In: Abstracts of the All-Union conference on the cytology of microorganisms, Institute of biochemistry and physiology of microorganisms, Pushchino, Russia, 21–23 Nov 1984

    Google Scholar 

  • Waisman IS (1984) Prerequisites for a comprehensive assessment of the physiological state of bacteria and their populations (in Russian). Zhurnal Mikrobiologii, Epidemiologii i Immunobiologii 4:3–8

    Google Scholar 

  • Wang WS, Tischer RG (1973) Study of the extracellular polysaccharides produced by a blue-green alga, Anabaena flos-aquae A-37. Arch Microbiol 91(1):77–81. doi:10.1007/BF00409540

    CAS  Google Scholar 

  • Weckesser J, Hofmann K, Jürgens UWEJ, Whitton BA, Raffelsberger B (1988) Isolation and chemical analysis of the sheaths of the filamentous cyanobacteria Calothrix parietina and C. scopulorum. J Gen Microbiol 134(3):629–634. doi:10.1099/00221287-134-3-629

    CAS  Google Scholar 

  • Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25(4):365–404. doi:10.1111/j.1574-6976.2001.tb00583.x

    PubMed  CAS  Google Scholar 

  • Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39–68. doi:10.1146/annurev.biochem.75.103004.142545

    PubMed  CAS  Google Scholar 

  • Williams P (2007) Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153(12):3923–3938. doi:10.1099/mic.0.2007/012856-0

    PubMed  CAS  Google Scholar 

  • Woehlecke H (1996) The dynamics of the ultrafilter properties of plant cell walls. Dissertation. Humboldt University, Berlin

    Google Scholar 

  • Woehlecke H, Ehwald R (1995) Characterization of size-permeation limits of cell walls and porous separation materials by high-performance size-exclusion chromatography. J Chromatogr A 708(2):263–271. doi:10.1016/0021-9673(95)00407-E

    CAS  Google Scholar 

  • Yarmolinsky MB (1995) Programmed cell death in bacterial populations. Science (Washington) 267(5199):836–837

    CAS  Google Scholar 

  • Zabalueva KT, Shatilov VR, Filippovicn II (1993) Characterization of ribosome-containing rod-like structures isolated from Phormidium laminosum photosynthetic membranes. Photosynthetica 29(3):463–467

    CAS  Google Scholar 

  • Zheng WW, Song TY, Bao XD, Bergman B, Rasmussen U (2002) High cyanobacterial diversity in coralloid roots of cycads revealed by PCR fingerprinting. FEMS Microbiol Ecol 40:215–222

    PubMed  CAS  Google Scholar 

  • Zilliges Y, Kehr JC, Mikkat S, Bouchier C, De Marsac NT, Börner T, Dittmann E (2008) An extracellular glycoprotein is implicated in cell–cell contacts in the toxic cyanobacterium Microcystis aeruginosa PCC 7806. J Bacteriol 190(8):2871–2879. doi:10.1128/JB.01867-07

    PubMed  CAS  Google Scholar 

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Baulina, O.I. (2012). Ultrastructural Plasticity of Cyanobacteria in Natural Symbioses with Plants. In: Ultrastructural Plasticity of Cyanobacteria. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32781-0_5

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