Extracellular Matrix (ECM)

  • Richard F. HelmEmail author
  • Malcolm Potts


The region of space at the periphery of cyanobacterial cells is the interface between the environment and intracellular processes. This metaspace may include a structure appressed to the outer wall and membrane, such as an extracellular polysaccharide (EPS), a structural and/or physiological discontinuity in the control of flow metabolites, as well as a temporal flux that accompanies stress or cell division. The functional framework within this region is designed to recognize environmental perturbations and relay physical and biochemical information to the cell interior, and perhaps to the cell community, for the appropriate physiological response. Communication between the environment and the cells is thus initiated within this extracellular milieu, which is therefore an important spatial domain in the cyanobacteria. The ECM of cyanobacterial cells is multifaceted. It is not only a complex and dynamic mixture of polysaccharides, proteins, cell remnants and lower molecular weight secondary metabolites, but a hyperspace that tunes seasonal as well as short-term stochastic modulations in environmental conditions. Such stresses result in changes in both the composition and organization of the matrix as cyanobacterial cells adjust to the environmental perturbations. This chapter provides a critical appraisal of the ecology and evolution of the cyanobacterial ECM compared with other prokaryotes. Emphasis is placed on how little is understood about this “occupied space” and several hypotheses and examples are presented in an effort to promote additional investigations of this oft-ignored interface.


Voronoi Tessellation Cyanobacterial Cell Homoserine Lactone Cyanobacterial Community Rhodopseudomonas Palustris 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Agger SA, Lopez-Gallego F, Hoye TR, Schmidt-Dannert C (2008) Identification of sesquiterpene synthases from Nostoc punctiforme PCC 73102 and Nostoc sp. strain PCC 7120. J Bacteriol 190:6084–6096PubMedCrossRefGoogle Scholar
  2. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2008) Molecular biology of the cell, 4th edn. Garland Science, New York, 1359 ppGoogle Scholar
  3. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S et al (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–1128PubMedCrossRefGoogle Scholar
  4. Balskus EP, Walsh CT (2009) An enzymatic cyclopentyl[b]indole formation involved in scytonemin biosynthesis. J Am Chem Soc 131:14648–14649PubMedCrossRefGoogle Scholar
  5. Balskus EP, Walsh CT (2010) The genetic and molecular basis for sunscreen biosynthesis in cyanobacteria. Science 329:1653–1656PubMedCrossRefGoogle Scholar
  6. Baran R, Bowen BP, Bouskill NJ, Brodie EL, Yannone SM, Northen TR (2010) Metabolite identification in Synechococcus sp. PCC 7002 using untargeted stable isotope assisted metabolite profiling. Anal Chem 82:9034–9042PubMedCrossRefGoogle Scholar
  7. Baran R, Bowen BP, Northen TR (2011) Untargeted metabolic footprinting reveals a surprising breadth of metabolite uptake and release by Synechococcus sp. PCC 7002. Mol Biosyst 7:3200–3206PubMedCrossRefGoogle Scholar
  8. Barberousse H, Ruiz G, Gloaguen V, Lombardo RJ, Djediat C, Mascarell G et al (2006) Capsular polysaccharides secreted by building facade colonisers: characterisation and adsorption to surfaces. Biofouling 22:361–370PubMedCrossRefGoogle Scholar
  9. Battistuzzi FU, Hedges SB (2009) A major clade of prokaryotes with ancient adaptations to life on land. Mol Biol Evol 26:335–343PubMedCrossRefGoogle Scholar
  10. Bennette NB, Eng JF, Dismukes GC (2011) An LC-MS-based chemical and analytical method for targeted metabolite quantification in the model cyanobacterium Synechococcus sp. PCC 7002. Anal Chem 83:3808–3816PubMedCrossRefGoogle Scholar
  11. Berman-Frank I, Rosenberg G, Levitan O, Haramaty L, Mari X (2007) Coupling between autocatalytic cell death and transparent exopolymeric particle production in the marine cyanobacterium Trichodesmium. Environ Microbiol 9:1415–1422PubMedCrossRefGoogle Scholar
  12. Bewley CA, Gustafson KR, Boyd MR, Covell DG, Bax A, Clore GM et al (1998) Solution structure of cyanovirin-N, a potent HIV-inactivating protein. Nat Struct Biol 5:571–578PubMedCrossRefGoogle Scholar
  13. Boedicker JQ, Vincent ME, Ismagilov RF (2009) Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew Chem Int Ed Engl 48:5908–5911PubMedCrossRefGoogle Scholar
  14. Bohm GA, Pfleiderer W, Boger P, Scherer S (1995) Structure of a novel oligosaccharide-mycosporine amino acid ultraviolet A/B sunscreen from the terrestrial cyanobacterium Nostoc commune. J Biol Chem 270:8536–8539PubMedCrossRefGoogle Scholar
  15. Boles BR, Singh PK (2008) Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci USA 105:12503–12508PubMedCrossRefGoogle Scholar
  16. Boles BR, Thoendel M, Singh PK (2004) Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci USA 101:16630–16635PubMedCrossRefGoogle Scholar
  17. Boles BR, Thoendel M, Singh PK (2005) Genetic variation in biofilms and the insurance effects of diversity. Microbiology 151:2816–2818PubMedCrossRefGoogle Scholar
  18. Botos I, O’Keefe BR, Shenoy SR, Cartner LK, Ratner DM, Seeberger PH et al (2002) Structures of the complexes of a potent anti-HIV protein cyanovirin-N and high mannose oligosaccharides. J Biol Chem 277:34336–34342PubMedCrossRefGoogle Scholar
  19. Boyd MR, Gustafson KR, McMahon JB, Shoemaker RH, Okeefe BR, Mori T et al (1997) Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development. Antimicrob Agents Chemother 41:1521–1530PubMedGoogle Scholar
  20. Brahamsha B (1996) An abundant cell-surface polypeptide is required for swimming by the nonflagellated marine cyanobacterium Synechococcus. Proc Natl Acad Sci USA 93:6504–6509PubMedCrossRefGoogle Scholar
  21. Braissant O, Decho AW, Przekop KM, Gallagher KL, Glunk C, Dupraz C et al (2009) Characteristics and turnover of exopolymeric substances in a hypersaline microbial mat. FEMS Microbiol Ecol 67:293–307PubMedCrossRefGoogle Scholar
  22. Case RJ, Labbate M, Kjelleberg S (2008) AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J 2:345–349PubMedCrossRefGoogle Scholar
  23. Cates ME, Marenduzzo D, Pagonabarraga I, Tailleur J (2010) Arrested phase separation in reproducing bacteria creates a generic route to pattern formation. Proc Natl Acad Sci USA 107:11715–11720Google Scholar
  24. Chen LZ, Wang GH, Hong S, Liu A, Li C, Liu YD (2009) UV-B-induced oxidative damage and protective role of exopolysaccharides in desert cyanobacterium Microcoleus vaginatus. J Integr Plant Biol 51:194–200PubMedCrossRefGoogle Scholar
  25. Costerton WJ (2004) A short history of the development of the biofilm concept. In: Ghannoum M, O’Toole GA (eds) Microbial biofilms. ASM Press, Washington, DC, pp 4–19Google Scholar
  26. 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 73:155–177PubMedCrossRefGoogle Scholar
  27. De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175CrossRefGoogle Scholar
  28. Decho AW, Visscher PT, Ferry J, Kawaguchi T, He L, Przekop KM et al (2009) Autoinducers extracted from microbial mats reveal a surprising diversity of N-acylhomoserine lactones (AHLs) and abundance changes that may relate to diel pH. Environ Microbiol 11:409–420PubMedCrossRefGoogle Scholar
  29. Dell’Anno A, Danovaro R (2005) Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science 309:2179–2179PubMedCrossRefGoogle Scholar
  30. Dickschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343–369PubMedCrossRefGoogle Scholar
  31. Dittrich M, Sibler S (2005) Cell surface groups of two picocyanobacteria strains studied by zeta potential investigations, potentiometric titration, and infrared spectroscopy. J Colloid Interface Sci 286:487–495PubMedCrossRefGoogle Scholar
  32. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449PubMedCrossRefGoogle Scholar
  33. Ehling-Schulz M, Schulz S, Wait R, Gorg A, Scherer S (2002) The UV-B stimulon of the terrestrial cyanobacterium Nostoc commune comprises early shock proteins and late acclimation proteins. Mol Microbiol 46:827–843PubMedCrossRefGoogle Scholar
  34. Eisenhut M, Huege J, Schwarz D, Bauwe H, Kopka J, Hagemann M (2008) Metabolome phenotyping of inorganic carbon limitation in cells of the wild type and photorespiratory mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol 148:2109–2120PubMedCrossRefGoogle Scholar
  35. Firn RD, Jones CG (2000) The evolution of secondary metabolism – a unifying model. Mol Microbiol 37:989–994PubMedCrossRefGoogle Scholar
  36. Firn RD, Jones CG (2009) A Darwinian view of metabolism: molecular properties determine fitness. J Exp Bot 60:719–726PubMedCrossRefGoogle Scholar
  37. Fischbach MA, Clardy J (2007) One pathway, many products. Nat Chem Biol 3:353–355PubMedCrossRefGoogle Scholar
  38. Fischer D, Geyer A, Loos E (2006) Occurrence of glucosylsucrose alpha-D-glucopyranosyl-(1->2)-alpha-D-glucopyranosyl-(1->2)-beta-D-fructofuranoside and glucosylated homologues in cyanobacteria – Structural properties, cellular contents and possible function as thermoprotectants. FEBS J 273:137–149PubMedCrossRefGoogle Scholar
  39. Flores E, Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50PubMedCrossRefGoogle Scholar
  40. Foster JS, Green SJ, Ahrendt SR, Golubic S, Reid RP, Hetherington KL et al (2009) Molecular and morphological characterization of cyanobacterial diversity in the stromatolites of Highborne Cay, Bahamas. ISME J 3:573–587PubMedCrossRefGoogle Scholar
  41. Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B et al (2006) Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp strain PCC 6803. Proteomics 6:2733–2745PubMedCrossRefGoogle Scholar
  42. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275PubMedGoogle Scholar
  43. Gantner S, Schmid M, Durr C, Schuhegger R, Steidle A, Hutzler P et al (2006) In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone-mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiol Ecol 56:188–194PubMedCrossRefGoogle Scholar
  44. Garcia-Pichel F, Pringault O (2001) Microbiology – cyanobacteria track water in desert soils. Nature 413:380–381PubMedCrossRefGoogle Scholar
  45. Garcia-Pichel F, Wojciechowski MF (2009) The evolution of a capacity to build supra-cellular ropes enabled filamentous cyanobacteria to colonize highly erodible substrates. PLoS One 4:e7801PubMedCrossRefGoogle Scholar
  46. Geitler L (1932) Cyanophyceae. Rabenhorst’s Krytogamen-Flora von Deutschland, Österreich und der Schweiz 14. Akademische Verlagsgesellschaft, Leipzig, 1196 ppGoogle Scholar
  47. Ghosh D, Roy K, Williamson KE, Srinivasiah S, Wommack KE, Radosevich M (2009) Acyl-homoserine lactones can induce virus production in lysogenic bacteria: an alternative paradigm for prophage induction. Appl Environ Microbiol 75:7142–7152PubMedCrossRefGoogle Scholar
  48. Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631PubMedCrossRefGoogle Scholar
  49. Gorbushina AA, Broughton WJ (2009) Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol 63:431–450PubMedCrossRefGoogle Scholar
  50. Green JL, Bohannan BJ, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043PubMedCrossRefGoogle Scholar
  51. Gronenborn AM (2009) Protein acrobatics in pairs – dimerization via domain swapping. Curr Opin Struct Biol 19:39–49PubMedCrossRefGoogle Scholar
  52. Gupta RS (2009) Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59:2510–2526PubMedCrossRefGoogle Scholar
  53. Gupta RS, Mathews DW (2010) Signature proteins for the major clades of cyanobacteria. BMC Evol Biol 10:24PubMedCrossRefGoogle Scholar
  54. Harmsen M, Lappann M, Knochel S, Molin S (2010) Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 76:2271–2279PubMedCrossRefGoogle Scholar
  55. Haselkorn R (2008) Cell-cell communication in filamentous cyano­bacteria. Mol Microbiol 70:783–785PubMedGoogle Scholar
  56. Havemann SA, Foster JS (2008) Comparative characterization of the microbial diversities of an artificial microbialite model and a natural stromatolite. Appl Environ Microbiol 74:7410–7421PubMedCrossRefGoogle Scholar
  57. Helm RF, Huang Z, Edwards D, Leeson H, Peery W, Potts M (2000) Structural characterization of the released polysaccharide of desiccation-tolerant Nostoc commune DRH-1. J Bacteriol 182:974–982PubMedCrossRefGoogle Scholar
  58. Hense BA, Kuttler C, Muller J, Rothballer M, Hartmann A, Kreft J-U (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat Rev Microbiol 5:230–239PubMedCrossRefGoogle Scholar
  59. Hill DR, Hladun SL, Scherer S, Potts M (1994a) Water-stress proteins of Nostoc commune (Cyanobacteria) are secreted with UV-A/B-absorbing pigments and associate with 1,4-beta-D-xylanohydrolase activity. J Biol Chem 269:7726–7734PubMedGoogle Scholar
  60. Hill DR, Peat A, Potts M (1994b) Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc commune (Cyanobacteria). Protoplasma 182:126–148CrossRefGoogle Scholar
  61. Hill DR, Keenan TW, 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 9:237–248CrossRefGoogle Scholar
  62. Hillesland KL, Stahl DA (2010) Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc Natl Acad Sci USA 107:2124–2129PubMedCrossRefGoogle Scholar
  63. Hoiczyk E, Baumeister W (1997) Oscillin, an extracellular, Ca2+-binding glycoprotein essential for the gliding motility of cyanobacteria. Mol Microbiol 26:699–708PubMedCrossRefGoogle Scholar
  64. Hoiczyk E, Hansel A (2000) Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J Bacteriol 182:1191–1199PubMedCrossRefGoogle Scholar
  65. Izaguirre G, Hwang CJ, Krasner SW, McGuire MJ (1982) Geosmin and 2-methylisoborneol from cyanobacteria in three water supply systems. Appl Environ Microbiol 43:708–714PubMedGoogle Scholar
  66. Jones AC, Gu L, Sorrels CM, Sherman DH, Gerwick WH (2009) New tricks from ancient algae: natural products biosynthesis in marine cyanobacteria. Curr Opin Chem Biol 13:216–223Google Scholar
  67. Jones AC, Monroe EA, Eisman EB, Gerwick L, Sherman DH, Gerwick WH (2010) The unique mechanistic transformations involved in the biosynthesis of modular natural products from marine cyanobacteria. Nat Prod Rep 27:1048–1065Google Scholar
  68. Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347PubMedCrossRefGoogle Scholar
  69. Karseno HK, Bamba T, Dwi S, Mahakhant A, Yoshikawa T et al (2009) Extracellular phycoerythrin-like protein released by freshwater cyanobacteria Oscillatoria and Scytonema sp. Biotechnol Lett 31:999–1003PubMedCrossRefGoogle Scholar
  70. Kehr JC, Zilliges Y, Springer A, Disney MD, Ratner DD, Bouchier C et al (2006) A mannan binding lectin is involved in cell-cell attachment in a toxic strain of Microcystis aeruginosa. Mol Microbiol 59:893–906PubMedCrossRefGoogle Scholar
  71. Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, Ward DM et al (2008) Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci USA 105:2504–2509PubMedCrossRefGoogle Scholar
  72. Krall L, Huege J, Catchpole G, Steinhauser D, Willmitzer L (2009) Assessment of sampling strategies for gas chromatography-mass spectrometry (GC-MS) based metabolomics of cyanobacteria. J Chromatogr B Anal Technol Biomed Life Sci 877:2952–2960CrossRefGoogle Scholar
  73. Kumar KV, Kumaran A (2005) Voronoi cell volume distribution and configuration entropy of hard-spheres. J Chem Phys 123:114501PubMedCrossRefGoogle Scholar
  74. Lake JA (2009) Evidence for an early prokaryotic endosymbiosis. Nature 460:967–971PubMedCrossRefGoogle Scholar
  75. Lappann M, Claus H, van Alen T, Harmsen M, Elias J, Molin S et al (2010) A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol Microbiol 75:1355–1371PubMedCrossRefGoogle Scholar
  76. Leao PN, Vasconcelos MT, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282Google Scholar
  77. Leao PN, Pereira AR, Liu WT, Ng J, Pevzner PA, Dorrestein PC, Konig GM, Vasconcelos VM, Gerwick WH (2010) Synergistic allelochemicals from a freshwater cyanobacterium. Proc Natl Acad Sci USA 107:11183–11188Google Scholar
  78. Lehner J, Zhang Y, Berendt S, Rasse TM, Forchhammer K, Maldener I (2011) The morphogene AmiC2 is pivotal for multicellular development in the cyanobacterium Nostoc punctiforme. Mol Microbiol 79:1655–1669Google Scholar
  79. Leikoski N, Fewer DP, Sivonen K (2009) Widespread occurrence and lateral transfer of the cyanobactin biosynthesis gene cluster in cyanobacteria. Appl Environ Microbiol 75:853–857PubMedCrossRefGoogle Scholar
  80. Leikoski N, Fewer DP, Jokela J, Wahlsten M, Rouhiainen L, Sivonen K (2010) Highly diverse cyanobactins in strains of the genus Anabaena. Appl Environ Microbiol 76:701–709PubMedCrossRefGoogle Scholar
  81. Liaimer A, Jenke-Kodama H, Ishida K, Hinrichs K, Stangeland J, Hertweck C, Dittmann E (2011) A polyketide interferes with cellular differentiation in the symbiotic cyanobacterium Nostoc punctiforme. Environ Microbiol Rep 3: 550–558Google Scholar
  82. Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101:11013–11018PubMedCrossRefGoogle Scholar
  83. Long A, McDaniel LD, Mobberley J, Paul JH (2008) Comparison of lysogeny (prophage induction) in heterotrophic bacterial and Synechococcus populations in the Gulf of Mexico and Mississippi River plume. ISME J 2:132–144PubMedCrossRefGoogle Scholar
  84. Lopez D, Kolter R (2010) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34:134–149PubMedCrossRefGoogle Scholar
  85. Lopez D, Vlamakis H, Kolter R (2009a) Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33:152–163PubMedCrossRefGoogle Scholar
  86. Lopez D, Vlamakis H, Losick R, Kolter R (2009b) Paracrine signaling in a bacterium. Genes Dev 23:1631–1638PubMedCrossRefGoogle Scholar
  87. Macedo MF, Miller AZ, Dionisio A, Saiz-Jimenez C (2009) Biodiversity of cyanobacteria and green algae on monuments in the Mediterranean Basin: an overview. Microbiology 155:3476–3490PubMedCrossRefGoogle Scholar
  88. Marenduzzo D, Finan K, Cook PR (2006) The depletion attraction: an underappreciated force driving cellular organization. J Cell Biol 175:681–686PubMedCrossRefGoogle Scholar
  89. Martinez RE, Pokrovsky OS, Schott J, Oelkers EH (2008) Surface charge and zeta-potential of metabolically active and dead cyanobacteria. J Colloid Interface Sci 323:317–325PubMedCrossRefGoogle Scholar
  90. Martinez RE, Gardes E, Pokrovsky OS, Schott J, Oelkers EH (2010) Do photosynthetic bacteria have a protective mechanism against carbonate precipitation at their surfaces? Geochim Cosmochim Acta 74:1329–1337CrossRefGoogle Scholar
  91. Matei E, Furey W, Gronenborn AM (2008) Solution and crystal structures of a sugar binding site mutant of cyanovirin-N: no evidence of domain swapping. Structure 16:1183–1194PubMedCrossRefGoogle Scholar
  92. Mateo P, Berrendero E, Perona E, Loza V, Whitton BA (2010) Phosphatase activities of cyanobacteria as indicators of nutrient status in a Pyrenees river. Hydrobiologia 652:255–268CrossRefGoogle Scholar
  93. McCarren J, Brahamsha B (2007) SwmB, a 1.12-megadalton protein that is required for nonflagellar swimming motility in Synechococcus. J Bacteriol 189:1158–1162PubMedCrossRefGoogle Scholar
  94. McCarren J, Brahamsha B (2009) Swimming motility mutants of marine Synechococcus affected in production and localization of the S-Layer protein SwmA. J Bacteriol 191:1111–1114PubMedCrossRefGoogle Scholar
  95. McCarren J, Heuser J, Roth R, Yamada N, Martone M, Brahamsha B (2005) Inactivation of swmA results in the loss of an outer cell layer in a swimming Synechococcus strain. J Bacteriol 187:224–230PubMedCrossRefGoogle Scholar
  96. Morsy FM, Kuzuha S, Takani Y, Sakamoto T (2008) Novel thermostable glycosidases in the extracellular matrix of the terrestrial cyanobacterium Nostoc commune. J Gen Appl Microbiol 54:243–252PubMedCrossRefGoogle Scholar
  97. Morvan H, Gloaguen V, Vebret L, Joset F, Hoffmann L (1997) Structure-function investigations on capsular polymers as a necessary step for new biotechnological applications: the case of the cyanobacterium Mastigocladus laminosus. Plant Physiol Biochem 35:671–683Google Scholar
  98. Nadell CD, Xavier JB, Foster KR (2009) The sociobiology of biofilms. FEMS Microbiol Rev 33:206–224PubMedCrossRefGoogle Scholar
  99. Nakao M, Okamoto S, Kohara M, Fujishiro T, Fujisawa T, Sato S et al (2010) CyanoBase: the cyanobacteria genome database update 2010. Nucleic Acids Res 38:D379–D381PubMedCrossRefGoogle Scholar
  100. Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the Bacterial luminescent system. J Bacteriol 104:313–322PubMedGoogle Scholar
  101. OED (2009) Oxford english dictionary. Oxford University Press, OxfordGoogle Scholar
  102. Paerl HW, Huisman J (2008) Climate. Blooms like it hot. Science 320:57–58PubMedCrossRefGoogle Scholar
  103. Paerl HW, Steppe TF, Buchan KC, Potts M (2003) Hypersaline cyanobacterial mats as indicators of elevated tropical hurricane activity and associated climate change. Ambio 32:87–90PubMedGoogle Scholar
  104. Peat A, Powell N, Potts M (1988) Ultrastructural analysis of the rehydration of desiccated Nostoc commune Hun (Cyanobacteria) with particular reference to the immunolabelling of NifH. Protoplasma 146:72–80CrossRefGoogle Scholar
  105. Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol Rev 33:917–941PubMedCrossRefGoogle Scholar
  106. Pontis HG, Vargas WA, Salerno GL (2007) Structural characterization of the members of a polymer series, compatible solutes in Anabaena cells exposed to salt stress. Plant Sci 172:29–35CrossRefGoogle Scholar
  107. Potts M (1980) Blue-green-algae (Cyanophyta) in marine coastal environments of the Sinai peninsula: distribution, zonation, stratification, and taxonomic diversity. Phycologia 19:60–73CrossRefGoogle Scholar
  108. Potts M (1997) Etymology of the genus name Nostoc (cyanobacteria). Int J Syst Bacteriol 47:584CrossRefGoogle Scholar
  109. Potts M, Sun H, Mockaitis K, Kennelly PJ, Reed D, Tonks NK (1993) A protein-tyrosine/serine phosphatase encoded by the genome of the cyanobacterium Nostoc commune UTEX 584. J Biol Chem 268:7632–7635Google Scholar
  110. Potts M (2000) Nostoc. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 465–504, 669 ppGoogle Scholar
  111. Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Vaitomaa J, Börner T (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci USA 101:568–573PubMedCrossRefGoogle Scholar
  112. Read N, Connell S, Adams DG (2007) Nanoscale visualization of a fibrillar array in the cell wall of filamentous cyanobacteria and its implications for gliding motility. J Bacteriol 189:7361–7366PubMedCrossRefGoogle Scholar
  113. Redfield RJ (2002) Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10:365–370PubMedCrossRefGoogle Scholar
  114. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61CrossRefGoogle Scholar
  115. Romero M, Diggle SP, Heeb S, Camara M, Otero A (2008) Quorum quenching activity in Anabaena sp. PCC 7120: identification of AiiC, a novel AHL-acylase. FEMS Microbiol Lett 280:73–80PubMedCrossRefGoogle Scholar
  116. Romero M, Muro-Pastor AM, Otero A (2011) Quorum sensing N-acylhomoserine lactone signals affect nitrogen fixation in the cyanobacterium Anabaena sp. PCC7120. FEMS Microbiol Lett 315:101–108Google Scholar
  117. Rycroft CH, Grest GS, Landry JW, Bazant MZ (2006) Analysis of granular flow in a pebble-bed nuclear reactor. Phys Rev E 74:16CrossRefGoogle Scholar
  118. Sanchez-Baracaldo P, Hayes PK, Blank CE (2005) Morphological and habitat evolution in the Cyanobacteria using a compartmentalization approach. Geobiology 3:145–165CrossRefGoogle Scholar
  119. Sato Y, Okuyama S, Hori K (2007) Primary structure and carbohydrate binding specificity of a potent anti-HIV lectin isolated from the filamentous cyanobacterium Oscillatoria agardhii. J Biol Chem 282:11021–11029PubMedCrossRefGoogle Scholar
  120. Scanlan DJ, Carr NG (1988) Extracellular proteins. In: Packer L, Glazer AN (eds) Methods in enzymology, vol 167. Academic, San Diego, pp 599–605Google Scholar
  121. Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, Hagemann M, Paulsen I, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73:249–299PubMedCrossRefGoogle Scholar
  122. Schaefer AL, Greenberg EP, Oliver CM, Oda Y, Huang JJ, Bittan-Banin G, Peres GM, Schmidt S, Juhaszova K, Sufrin JR et al (2008) A new class of homoserine lactone quorum-sensing signals. Nature 454:595–599PubMedCrossRefGoogle Scholar
  123. Schatz D, Keren Y, Vardi A, Sukenik A, Carmeli S, Börner T, Dittmann E, Kaplan A et al (2007) Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins. Environ Microbiol 9:965–970PubMedCrossRefGoogle Scholar
  124. Schaudinn C, Stoodley P, Kainović A, O’Keeffe T, Costerton B, Robinson D, Baum D, Ehrlich G, Webster P (2007) Bacterial biofilms, other structures seen as mainstream concepts. Microbe 2:231–237Google Scholar
  125. Scherer S, Potts M (1989) Novel water-stress protein from a desiccation-tolerant cyanobacterium – purification and partial characterization. J Biol Chem 264:12546–12553PubMedGoogle Scholar
  126. Schirrmeister BE, Antonelli A, Bagheri HC (2011) The origin of multicellularity in cyanobacteria. BMC Evol Biol 11:45Google Scholar
  127. Sergeyenko TV, Los DA (2000) Identification of secreted proteins of the cyanobacterium Synechocystis sp strain PCC 6803. FEMS Microbiol Lett 193:213–216PubMedCrossRefGoogle Scholar
  128. Shahzad-Ul-Hussan S, Cai ML, Bewley CA (2009) Unprecedented glycosidase activity at a lectin carbohydrate-binding site exemplified by the cyanobacterial lectin MVL. J Am Chem Soc 131:16500–16508PubMedCrossRefGoogle Scholar
  129. Sharif DI, Gallon J, Smith CJ, Dudley E (2008) Quorum sensing in cyanobacteria: N-octanoyl-homoserine lactone release and response, by the epilithic colonial cyanobacterium Gloeothece PCC6909. ISME J 2:1171–1182PubMedCrossRefGoogle Scholar
  130. Shaw E, Hill DR, Brittain N, Wright DJ, Tauber U, Marand H et al (2003) Unusual water flux in the extracellular polysaccharide of the cyanobacterium Nostoc commune. Appl Environ Microbiol 69:5679–5684PubMedCrossRefGoogle Scholar
  131. Shi T, Falkowski PG (2008) Genome evolution in cyanobacteria: the stable core and the variable shell. Proc Natl Acad Sci USA 105:2510–2515PubMedCrossRefGoogle Scholar
  132. Shin BJ, Oh J, Kang S, Chung YH, Park YM, Kim YH, Kim S, Bhak J, Choi JS (2008) Cyanobacterial hybrid kinase Sll0043 regulates phototaxis by suppressing pilin and twitching motility protein. J Microbiol 46:300–308PubMedCrossRefGoogle Scholar
  133. Shirkey B, Kovarcik DP, Wright DJ, Wilmoth G, Prickett TF, Helm RF et al (2000) Active Fe-containing superoxide dismutase and abundant sodF mRNA in Nostoc commune (cyanobacteria) after years of desiccation. J Bacteriol 182:189–197PubMedCrossRefGoogle Scholar
  134. Sivonen K, Leikoski N, Fewer DP, Jokela J (2010) Cyanobactins-ribosomal cyclic peptides produced by cyanobacteria. Appl Microbiol Biotechnol 86:1213–1225PubMedCrossRefGoogle Scholar
  135. Smarda J, Smajs D, Komrska J, Krzyzanek V (2002) S-layers on cell walls of cyanobacteria. Micron 33:257–277PubMedCrossRefGoogle Scholar
  136. Spence E, Dunlap WC, Shick JM, Long PF (2012) Redundant pathways of sunscreen biosynthesis in a cyanobacterium. Chembiochem 13:531–533Google Scholar
  137. Steinberger RE, Holden PA (2005) Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 71:5404–5410PubMedCrossRefGoogle Scholar
  138. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210PubMedCrossRefGoogle Scholar
  139. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209PubMedCrossRefGoogle Scholar
  140. Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW (2006) Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4:e234PubMedCrossRefGoogle Scholar
  141. Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M, Sarracino D et al (2009) The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’. Environ Microbiol 11:2935–2951PubMedCrossRefGoogle Scholar
  142. Swingley WD, Blankenship RE, Raymond J (2008) Integrating Markov clustering and molecular phylogenetics to reconstruct the cyanobacterial species tree from conserved protein families. Mol Biol Evol 25:643–654PubMedCrossRefGoogle Scholar
  143. Timp W, Mirsaidov U, Matsudaira P, Timp G (2009) Jamming prokaryotic cell-to-cell communications in a model biofilm. Lab Chip 9:925–934PubMedCrossRefGoogle Scholar
  144. Van Wagoner RM, Drummond AK, Wright JLC (2007) Biogenetic diversity of cyanobacterial metabolites. In: Laskin AI, Sariaslani S, Gadd GM (eds) Advances in applied microbiology. Elsevier, Amsterdam, pp 89–217Google Scholar
  145. Ward DM, Cohan FM, Bhaya D, Heidelberg JF, Kuhl M, Grossman A (2008) Genomics, environmental genomics and the issue of microbial species. Heredity 100:207–219PubMedCrossRefGoogle Scholar
  146. Wase NV, Wright PC (2008) Systems biology of cyanobacterial secondary metabolite production and its role in drug discovery. Expert Opin Drug Discov 3:903–929CrossRefGoogle Scholar
  147. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346PubMedCrossRefGoogle Scholar
  148. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487–1487PubMedCrossRefGoogle Scholar
  149. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404PubMedCrossRefGoogle Scholar
  150. Whitfield C, Naismith JH (2008) Periplasmic export machines for outer membrane assembly. Curr Opin Struct Biol 18:466–474PubMedCrossRefGoogle Scholar
  151. Whitton BA, Grainger SLJ, Hawley GRW, Simon JW (1991) Cell-bound and extracellular phosphatase activities of cyanobacterial isolates. Microb Ecol 21:85–98CrossRefGoogle Scholar
  152. Whitton BA, Al-Shehri AH, Ellwood NTW, Turner BL (2005) Ecological aspects of phosphatase activity in cyanobacteria, eukaryotic algae and bryophytes. In: Turner BL, Frossard E, Baldwin E (eds) Organic phosphorus in the environment. CABU Publishing, Wallingford/Cambridge, pp 205–241, 399 ppCrossRefGoogle Scholar
  153. Wieneke R, Klein S, Geyer A, Loos E (2007) Structural and functional characterization of galactooligosaccharides in Nostoc commune: beta-D-galactofuranosyl-(1->6)-[beta-D-galactofuranosyl-(1->6)](2)-beta-D-1,4-anhydrogalactitol and beta-(1->6)-galactofuranosylated homologues. Carbohydr Res 342:2757–2765PubMedCrossRefGoogle Scholar
  154. Wood SA, Mountfort D, Selwood AI, Holland PT, Puddick J, Cary SC (2008) Widespread distribution and identification of eight novel microcystins in Antarctic cyanobacterial mats. Appl Environ Microbiol 74:7243–7251PubMedCrossRefGoogle Scholar
  155. Wright DJ, Smith SC, Joardar V, Scherer S, Jervis J, Warren A et al (2005) UV irradiation and desiccation modulate the three-dimensional extracellular matrix of Nostoc commune (cyanobacteria). J Biol Chem 280:40271–40281PubMedCrossRefGoogle Scholar
  156. Wu J, Xi C (2009) Evaluation of different methods for extracting extracellular DNA from the biofilm matrix. Appl Environ Microbiol 75:5390–5395PubMedCrossRefGoogle Scholar
  157. Yamaguchi M, Ogawa T, Muramoto K, Kamio Y, Jimbo M, Kamiya H (1999) Isolation and characterization of a mannan-binding lectin from the freshwater cyanobacterium (blue-green algae) Microcystis viridis. Biochem Biophys Res Commun 265:703–708PubMedCrossRefGoogle Scholar
  158. Yamasaki Y, Shikata T, Nukata A, Ichiki S, Nagasoe S, Matsubara T et al (2009) Extracellular polysaccharide-protein complexes of a harmful alga mediate the allelopathic control it exerts within the phytoplankton community. ISME J 3:808–817PubMedCrossRefGoogle Scholar
  159. Yang F, Bewley CA, Louis JM, Gustafson KR, Boyd MR, Gronenborn AM et al (1999) Crystal structure of cyanovirin-N, a potent HIV-inactivating protein, shows unexpected domain swapping. J Mol Biol 288:403–412PubMedCrossRefGoogle Scholar
  160. Yeager CM, Kornosky JL, Morgan RE, Cain EC, Garcia-Pichel F, Housman DC et al (2007) Three distinct clades of cultured heterocystous cyanobacteria constitute the dominant N2-fixing members of biological soil crusts of the Colorado Plateau, USA. FEMS Microbiol Ecol 60:85–97PubMedCrossRefGoogle Scholar
  161. Yoon HS, Golden JW (1998) Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935–938PubMedCrossRefGoogle Scholar
  162. Yoshimura H, Okamoto S, Tsumuraya Y, Ohmori M (2007) Group 3 sigma factor gene, sigJ, a key regulator of desiccation tolerance, regulates the synthesis of extracellular polysaccharide in cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 14:13–24PubMedCrossRefGoogle Scholar
  163. Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16:1099–1108PubMedCrossRefGoogle Scholar
  164. Zilliges Y, Kehr J-C, Mikkat S, Bouchier C, Tandeau de Marsac N, Borner T et al (2008) An extracellular glycoprotein is implicated in cell-cell contacts in the toxic cyanobacterium Microcystis aeruginosa PCC 7806. J Bacteriol 190:2871–2879PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Department of Biochemistry, Life Sciences IVirginia TechBlacksburgUSA
  2. 2.Department of Biological and Environmental Sciences, College of Arts and SciencesQatar UniversityDohaQatar

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