Developmental genetics and symbiotic potential of cyanobacteria



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Abstract

Many cyanobacteria can differentiate specialized cells – heterocysts that fix nitrogen aerobically, akinetes able to survive under unfavorable conditions, and hormogonia providing a means of dispersal. Of great importance for evolution of the biosphere was the ability of cyanobacteria to establish symbioses with eukaryotic organisms that was a prerequisite for the emergence of chloroplasts. This review describes the genes and regulatory systems that control differentiation of specialized cells and the ability of cyanobacteria to establish symbiotic associations with a variety of hosts.

About the authors

Ivan Ya Khudyakov

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: iykhudyakov@yandex.ru

References

  1. Adams D. G., 1997. Cyanobacteria. // Bacteria as multicellular organisms / Eds. J. A. Shapiro et al. Oxford University Press, New York. P. 109–148.
  2. Adams, D. G., Duggan P. S., 1999. Heterocyst and akinete differentiation in cyanobacteria // New Phytol. Vol. 144. P. 3–33.
  3. Adams D. G., Duggan P. S., 2008. Cyanobacteria-bryophyte symbioses // J. Exp. Bot. Vol. 59. P. 1047–1058.
  4. Anderson D. C., Campbell E. L., Meeks J. C., 2006. A soluble 3D LC/MS/MS proteome of the filamentous cyanobacterium Nostoc punctiforme // J. Proteome Res. Vol. 5. P. 3096–3104.
  5. Argueta C., Summers M. L., 2005. Characterization of a model system for the study of Nostoc punctiforme akinetes // Arch. Microbiol. Vol. 183. P. 338–346.
  6. Argueta C., Yuksek K., Patel R. et al., 2006. Identification of Nostoc punctiforme akinete-expressed genes using differential display // Mol. Microbiol. Vol. 61. P. 748–757.
  7. Black T. A., Wolk C. P., 1994. Analysis of a Het- mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing // J. Bacteriol. Vol. 176. P. 2282–2292.
  8. Borthakur P. B., Orozco C. C., Young-Robbins S. S. et al., 2005. Inactivation of patS and hetN causes lethal levels of heterocyst differentiation in the filamentous cyanobacterium Anabaena sp. PCC 7120 // Mol. Microbiol. Vol. 57. P. 111–123.
  9. Bothe H., Tripp H. J., Zehr J. P., 2010. Unicellular cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed // Arch. Microbiol. Vol. 192. P. 783–790.
  10. Buikema W. J., Haselkorn R., 2001. Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions // Proc. Natl. Acad. Sci. U. S. A. Vol. 98. P. 2729–2734.
  11. Callahan S. M., Buikema W. J., 2001. The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120 // Mol. Microbiol. Vol. 40. P. 941–950.
  12. Campbell E. L., Brahamsha B., Meeks J. C., 1998. Mutation of an alternative sigma factor in the cyanobacterium Nostoc punctiforme results in increased infection of its symbiotic plant partner, Anthoceros punctatus // J. Bacteriol. Vol. 180. P. 4938–4941.
  13. Campbell E. L., Summers M. L., Christman H. et al., 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. Vol. 189. P. 5247–5256.
  14. Carr N. G., 1988. Nitrogen reserves and dynamic reservoirs in cyanobacteria // Biochemistry of the Algae and Cyanobacteria / Eds. L. J. Rogers and J. R. Gallon, Clarendon Press, Oxford, United Kingdom, P. 13–39.
  15. Castenholz R. W., 2001. Phylum BX. Cyanobacteria // Bergey’s Manual of Systematic Bacteriology / Eds. D. R. Boone and R. W. Castenholz. New York, Springer, 2nd edn, Vol. 1. P. 473–487.
  16. Cohen M. F., Meeks J. C., 1997. A hormogonium regulating locus, hrmUA, of the cyanobacterium Nostoc punctiforme strain ATCC 29133 and its response to an extract of a symbiotic plant partner Anthoceros punctatus // Mol. Plant-Microbe Interact. Vol. 10. P. 280–289.
  17. Damerval T., Houmard J., Guglielmi G. et al., 1987. A developmentally regulated gvpABC operon is involved in the formation of gas vesicles in the cyanobacterium Calothrix 7601 // Plant Cell. Vol. 3. P. 191–201.
  18. Damerval T., Guglielmi G., Houmard J., Tandeau de Marsac N., 1991. Hormogonium differentiation in the cyanobacterium Calothrix: a photoregulated developmental process // Plant Cell Vol. 3. P. 191–201.
  19. Du Y., Cai Y., Hou S., Xu X., 2012. Identification of the HetR recognition sequence upstream of hetZ in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 194. P. 2297–2306.
  20. Duggan P. S., Gottardello P., Adams D. G., 2007. Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection // J. Bacteriol. Vol. 198. P. 4547–4551.
  21. Ehira S., Ohmori M., Sato N., 2003. Genome-wide expression analysis of the responses to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 // DNA Res. Vol. 10. P. 97–113.
  22. Ehira S., Ohmori M., 2006. NrrA, a nitrogenresponsive response regulator facilitates heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120//Mol. Microbiol. Vol. 59. P. 1692–1703.
  23. Fan Q., Huang G., Lechno-Yossef S. et al., 2005. Clustered genes required for synthesis and deposition of envelope glycolipids in Anabaena sp. strain PCC 7120 // Mol. Microbiol. Vol. 58. P. 227–243.
  24. Fernández-Piñas F., Leganés F., Wolk CP., 1994. A third genetic locus required for the formation of heterocysts in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 176. P. 5277–83.
  25. Flores E., Pernil R., Muro-Pastor A. M. et al., 2007. Septum-localized protein required for filament integrity and diazotrophy in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 189. P. 3884–3890.
  26. Fiedler G., Arnold M., Hannus S. et al., 1998. The DevBCA exporter is essential for envelope formation in heterocysts of the cyanobacterium Anabaena sp. strain PCC 7120 // Mol. Microbiol. Vol. 27. P. 1193–1202.
  27. Haselkorn R., 1978. Heterocysts // Annu. Rev. Plant Physiol. Vol. 29. P. 319–344.
  28. Haselkorn R. 2008. Cell-cell communication in filamentous cyanobacteria // Mol. Microbiol. Vol. 70. P. 783–785.
  29. Hebbar P. B., Curtis S. E., 2000. Characterization of devH, a gene encoding a putative DNA binding protein required for heterocyst function in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 182. P. 3572–3581.
  30. Herdman M., Rippka R., 1988. Cellular differentiation: hormogonia and baeocytes // Methods Enzymol. Vol. 167. P. 232–242.
  31. Herrero A., Muro-Pastor A. M., Valladares A., Flores E., 2004. Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria // FEMS Microbiol. Rev. Vol. 28. P. 469–487.
  32. Higa K. C., Callahan S. M., 2010. Ectopic expression of hetP can partially bypass the need for hetR in heterocyst differentiation by Anabaena sp. strain PCC 7120 // Mol. Microbiol. Vol. 77. P. 562–574.
  33. Higa K. C., Rajagopalan R., Risser D. D. et al., 2012. The RGSGR amino acid motif of the intercellular signalling protein, HetN, is required for patterning of heterocysts in Anabaena sp. strain PCC 7120 // Mol. Microbiol. Vol. 83. P. 682–693.
  34. Hoiczyk E., Baumeister W., 1998. The junctional pore complex, a prokaryotic secretion organelle, is the molecular motor underlying gliding motility in cyanobacteria // Curr. Biol. Vol. 8. P. 1161–1168.
  35. Huang X., Dong Y., Zhao J., 2004. HetR homodimer is a DNA-binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS // Proc. Natl. Acad. Sci. U. S. A. Vol. 101. P. 4848–4853.
  36. Huang G., Fan Q., Lechno-Yossef S. et al., 2005. Clustered genes required for the synthesis of heterocyst envelope polysaccharide in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 187. P. 1114–1123.
  37. Jang J., Wang L., Jeanjean R. et al., 2007. PrpJ, a PP2C-type protein phosphatase located on the plasma membrane, is involved in heterocyst maturation in the cyanobacterium Anabaena sp. PCC 7120 // Mol. Microbiol. Vol. 64. P. 347–358.
  38. Jensen T. E., Clark R. L., 1969. Cell wall and coat of the developing akinete of a Cylindrospermum species // J. Bacteriol. Vol. 97. P. 1494–1495.
  39. Johansson C., Bergman B., 1992. Early events during the establishment of the Gunnera / Nostoc symbiosis // Planta Vol. 188. P. 403–413.
  40. Khudyakov I. Y., Golden J. W., 2001. Identification and inactivation of three group 2 sigma factor genes in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 183. P. 6667–6675.
  41. Khudyakov I. Y., Golden J. W., 2004. Different functions of HetR, a master regulator of heterocyst differentiation in Anabaena sp. PCC 7120 can be separated by mutation // Proc. Natl. Acad. Sci. U. S. A. Vol. 101. P. 16040–16045.
  42. Khudyakov I., Wolk C. P., 1996. Evidence that the hanA gene coding for HU protein is essential for heterocyst differentiation in, and cyanophage A-4(L) sensitivity of, Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 178. P. 3572–3577.
  43. Khudyakov I., Wolk C. P. 1997. hetC, a gene coding for a protein similar to bacterial ABC protein exporters, is involved in early regulation of heterocyst differentiation in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 179. P. 6971–6978.
  44. Knight C. D., Adams D. G., 1996. A method for studying chemotaxis in nitrogen fixing cyanobacterium-plant symbioses // Physiol. Mol. Plant Pathol. Vol. 49. P. 73–77.
  45. Kuhn I., Peng L., Bedu S., Zhang C. C., 2000. Developmental regulation of the cell division protein FtsZ in Anabaena sp. strain PCC 7120, a cyanobacterium capable of terminal differentiation // J. Bacteriol. Vol. 182. P. 4640–4643.
  46. Lázaro S., Fernández-Piñas F., Fernández-Valiente E. et al., 2001. pbpB, a gene coding for a putative penicillin-binding protein, is required for aerobic nitrogen fixation in the cyanobacterium Anabaena sp. strain PCC7120 // J. Bacteriol. Vol. 183. P. 628–636.
  47. Leganés F, Blanco-Rivero A, Fernández-Piñas F. et al., 2005. Wide variation in the cyanobacterial complement of presumptive penicillin-binding proteins // Arch. Microbiol. Vol. 184. P. 234–248.
  48. Liang J., Scappino L., Haselkorn R., 1992. The patA gene product, which contains a region similar to CheY of Escherichia coli, controls heterocyst pattern formation in the cyanobacterium Anabaena 7120 // Proc. Natl. Acad. Sci. U. S. A. Vol. 89. P. 5655–5659.
  49. Madan A. P., Nierzwicki-Bauer S. A., 1993. In situ detection of transcripts for ribulose-1,5-bisphosphate carboxylase in cyanobacterial heterocysts // J. Bacteriol. Vol. 175. P. 7301–7306.
  50. Mariscal V., Flores E., 2010. Multicellularity in a heterocyst-forming cyanobacterium: pathways for intercellular communication // Adv. Exp. Med. Bio.l. Vol. 675. P. 123–135.
  51. Mariscal V., Herrero A., Flores E., 2007. Continuous periplasm in a filamentous, heterocyst-forming cyanobacterium // Mol. Microbiol. Vol. 65. P. 1139–1145.
  52. Mariscal V., Herrero A., Nenninger A. et al., 2011. Functional dissection of the three-domain SepJ protein joining the cells in cyanobacterial trichomes // Mol. Microbiol. Vol. 79. P. 1077–1088.
  53. Meeks J. C., 1998. Symbiosis between nitrogen-fixing cyanobacteria and plants // BioScience. Vol. 48. P. 266–276.
  54. Meeks J. C., Campbell E. L., Summers M. L., Wong F. C., 2002. Cellular differentiation in the cyanobacterium Nostoc punctiforme // Arch. Microbiol. Vol. 178. P. 395–403.
  55. Meeks J. C., Elhai J., 2002. Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states // Microbiol. Mol. Biol. Rev. Vol. 66. P. 94–121.
  56. Mella-Herrera R. A., Neunuebel M. R., Golden J. W., 2011. Anabaena sp. strain PCC 7120 conR contains a LytR-CpsA-Psr domain, is developmentally regulated, and is essential for diazotrophic growth and heterocyst morphogenesis // Microbiology Vol. 157. P. 617–626.
  57. Merino-Puerto V, Mariscal V, Schwarz H. et al., 2011. FraH is required for reorganization of intracellular membranes during heterocyst differentiation in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 193. P. 6815–6823.
  58. Merino-Puerto V., Schwarz H., Maldener I. et al., 2011. FraC / FraD-dependent intercellular molecular exchange in the filaments of a heterocyst-forming cyanobacterium, Anabaena sp // Mol. Microbiol. Vol. 82. P. 87–98.
  59. Moslavac S., Nicolaisen K., Mirus O. et al., 2007. A TolC-like protein is required for heterocyst development in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 189. P. 7887–7895.
  60. Muro-Pastor A. M., Hess W. R. 2012. Heterocyst differentiation: from single mutants to global approaches // Trends Microbiol. Vol. 20. Р. 548–557
  61. Nayar A. S., Yamaura H., Rajagopalan R. et al., 2007. FraG is necessary for filament integrity and heterocyst maturation in the cyanobacterium Anabaena sp. strain PCC 7120 // Microbiology. Vol. 153. P. 601–607.
  62. Olmedo-Verd E., Flores E., Herrero A., Muro-Pastor A. M., 2005. HetR-dependent and -independent expression of heterocyst-related genes in an Anabaena strain overproducing the NtcA transcription factor // J. Bacteriol. Vol. 187. P. 1985–1991.
  63. Picossi S., Valladares A., Flores E. et al., 2004. Nitrogen-regulated genes for the metabolism of cyanophycin, a bacterial nitrogen reserve polymer: expression and mutational analysis of two cyanophycin synthetase and cyanophycinase gene clusters in heterocyst-forming cyanobacterium Anabaena sp. PCC 7120 // J. Biol. Chem. Vol. 279. P. 11582–11592.
  64. Ramírez M. E., Hebbar P. B., Zhou R. et al., 2005. Anabaena sp. strain PCC 7120 gene devH is required for synthesis of the heterocyst glycolipid layer // J. Bacteriol. Vol. 187. P. 2326–2331.
  65. Ran L., Larsson J., Vigil-Stenman T., et al. 2010. Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium // PLoS One. Vol. 5. P. e11486.
  66. Raven J. A. 2002. Evolution of cyanobacterial symbioses // Cyanobacteria in symbiosis / Eds. A. N. Rai et al., Kluwer Academic Publishers, Dordrecht, The Netherlands. P. 329–346.
  67. Rippka R., Herdman M., 1992. Pasteur Culture Collection of Cyanobacterial Strains in Axenic Culture, Catalogue and Taxonomic Handbook // Catalog of strains, Institut Pasteur, Paris. P. 1–103.
  68. Risser D. D., Callahan S. M., 2008. HetF and PatA control levels of HetR in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 190. P. 7645–7654.
  69. Risser D. D., Wong F. C., Meeks J. C., 2012. Biased inheritance of the protein PatN frees vegetative cells to initiate patterned heterocyst differentiation // Proc. Natl. Acad. Sci. U. S. A. Vol. 109. P. 15342–15347.
  70. Risser R.D, Meeks J. C., 2012. Identification of a novel polysaccharide secretion system essential for gliding motility in Nostoc punctiforme // Abstr. XIV Intern. Symp. Phototr. Prokar., Porto, Portugal. P42.
  71. Robinson B. L., Miller J. H., 1970. Photomorphogenesis in the blue-green alga Nostoc commune 584 // Physiol. Plantarum. Vol. 23. P. 461–472.
  72. Sakr S., Jeanjean R., Zhang C.-C. et al., 2006. Inhibition of cell division suppresses heterocyst development in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 188. P. 1396–1404.
  73. Shi L., Li J. H., Cheng Y. et al., 2007. Two genes encoding protein kinases of the HstK family are involved in synthesis of the minor heterocyst-specific glycolipid in the cyanobacterium Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 189. P. 5075–5081.
  74. Simon R. D. 1971. Cyanophycin granules from the blue-green alga Anabaena cylindrica: A reserve material consisting of copolymers of aspartic acid and arginine // Proc. Natl. Acad. Sci. U. S. A. Vol. 68. P. 265–267.
  75. Sukenik A., Kaplan-Levy R. N., Welch J. M. et al., 2012. Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria) // ISME J. Vol. 6. P. 670–679.
  76. Tandeau de Marsac N., 1994. Differentiation of hormogonia and relationships with other biological processes // The molecular biology of cyanobacteria / Ed. D. A. Bryant, Kluwer. Academic Publishers, Boston. P. 825–842.
  77. Thiel T., Wolk C. P., 1983. Metabolic activities of spores of Nostoc spongiaeforme // J. Bacteriol. Vol. 156. P. 369–374.
  78. Thompson A. W., Foster R. A., Krupke A. et al., 2012. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga // Science Vol. 337. P. 1546–1550.
  79. Tripp H. J., Bench S. R., Turk K. A., 2010. Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium // Nature Vol. 464. P. 90–94.
  80. Valladares A., Herrero A., Pils D. et al., 2003. Cytochrome c oxidase genes required for nitrogenase activity and diazotrophic growth in Anabaena sp. PCC 7120 // Mol. Microbiol. Vol. 47. P. 1239–1249.
  81. Valladares A., Maldener I., Muro-Pastor A. M. et al., 2007. Heterocyst development and diazotrophic metabolism in terminal respiratory oxidase mutants of the cyanobacterium Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 189. P. 4425–4430.
  82. Wang Y., Xu X., 2005. Regulation by hetC of genes required for heterocyst differentiation and cell division in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 187. P. 8489–8493.
  83. Wilk L., Strauss M., Rudolf M. et al., 2011. Outer membrane continuity and septosome formation between vegetative cells in the filaments of Anabaena sp. PCC 7120 // Cell Microbiol. Vol. 13. P. 1744–1754.
  84. Wolk C. P., Ernst A., Elhai J., 1994. Heterocyst metabolism and development // The molecular biology of cyanobacteria / Ed. D. A. Bryant, Kluwer Academic Publishers, Boston. P. 769–823.
  85. Wong F. C. Y., Meeks J. C., 2002. Establishment of a functional symbiosis between the cyanobacterium Nostoc punctiforme and the bryophyte hornwort Anthoceros punctatus requires genes involved in nitrogen control and initiation of heterocyst differentiation // Microbiology Vol. 148. P. 315–323.
  86. Wood S. A., Jentzsch K., Rueckert A. et al., 2009. Hindcasting cyanobacterial communities in Lake Okaro with germination experiments and genetic analyses // FEMS Microbiol. Ecol. Vol. 67. P. 252–260.
  87. Wu X., Lee D. W., Mella R. A., Golden J. W., 2007. The Anabaena sp. strain PCC 7120 asr1734 gene encodes a negative regulator of heterocyst development // Mol. Microbiol. Vol. 64. P. 782–794.
  88. Xu X., Elhai J., Wolk C. P., 2008. Transcriptional and developmental responses by Anabaena to deprivation of fixed nitrogen // The Cyanobacteria: Molecular Biology, Genomics and Evolution / Eds. Herrero A,, Flores E., Caister Academic Press, Norfolk. P. 383–422.
  89. Xu X., Khudyakov I., Wolk C. P., 1997. Lipopolysaccharide dependence of cyanophage sensitivity and aerobic nitrogen fixation in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 179. P. 2884–2891
  90. Xu X., Wolk C. P., 2001. Role for hetC in the transition to a nondividing state during heterocyst differentiation in Anabaena sp. // J. Bacteriol. Vol. 183. P. 393–396.
  91. Yoon H-S, Golden J. W., 1998. Heterocyst pattern formation controlled by a diffusible peptide // Science. Vol. 282. P. 935–938.
  92. Zehr J. P., Bench S. R., Carter B. J. et al., 2008. Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II // Science. Vol. 322. P. 1110–1112.
  93. Zhang C. C., Laurent S., Sakr S. et al., 2006. Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals // Mol. Microbiol. Vol. 59. P. 367–375.
  94. Zhang L. C., Chen Y. F., Chen W. L., Zhang C. C., 2008. Existence of periplasmic barriers preventing green fluorescent protein diffusion from cell to cell in the cyanobacterium Anabaena sp. strain PCC 7120 // Mol. Microbiol. Vol. 70. P. 814–823.
  95. Zhang W., Du Y., Khudyakov I. et al., 2007. A gene cluster that regulates both heterocyst differentiation and pattern formation in Anabaena sp. strain PCC 7120 // Mol. Microbiol. Vol. 66. P. 1429–1443.
  96. Zhao M. X., Jiang Y. L., He Y. X. et al., 2010. Structural basis for the allosteric control of the global transcription factor NtcA by the nitrogen starvation signal 2-oxoglutarate // Proc. Natl. Acad. Sci. U. S. A. Vol. 107. P. 12487–12492
  97. Zheng W., Bergman B., Chen B. et al., 2009. Cellular responses in the cyanobacterial symbiont during its vertical transfer between plant generations in the Azolla microphylla symbiosis // New Phytol. Vol. 181. P. 53–61.
  98. Zhou R., Wolk C. P., 2002. Identification of an akinete marker gene in Anabaena variabilis // J. Bacteriol. Vol. 184. P. 2529–2532.
  99. Zhou R., Wolk C. P., 2003. A two-component system mediates developmental regulation of biosynthesis of a heterocyst polysaccharide // J. Biol. Chem. Vol. 278. P. 19939–19946.
  100. Zhu J., Jäger K., Black T. et al., 2001. HcwA, an autolysin, is required for heterocyst maturation in Anabaena sp. strain PCC 7120 // J. Bacteriol. Vol. 183. P. 6841–6851.

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