1887

Abstract

Cyanobacteria are photosynthetic prokaryotes that are promising ‘low-cost’ microbial cell factories due to their simple nutritional requirements and metabolic plasticity, and the availability of tools for their genetic manipulation. The unicellular non-nitrogen-fixing sp. PCC 6803 is the best studied cyanobacterial strain and its genome was the first to be sequenced. The vast amount of physiological and molecular data available, together with a relatively small genome, makes suitable for computational metabolic modelling and to be used as a photoautotrophic chassis in synthetic biology applications. To prepare it for the introduction of a synthetic hydrogen producing device, a sp. PCC 6803 deletion mutant lacking an active bidirectional hydrogenase (Δ) was produced and characterized at different levels: physiological, proteomic and transcriptional. The results showed that, under conditions favouring hydrogenase activity, 17 of the 210 identified proteins had significant differential fold changes in comparisons of the mutant with the wild-type. Most of these proteins are related to the redox and energy state of the cell. Transcriptional studies revealed that only six genes encoding those proteins exhibited significant differences in transcript levels. Moreover, the mutant exhibits similar growth behaviour compared with the wild-type, reflecting plasticity and metabolic adaptability. Overall, this study reveals that the Δ mutant is robust and can be used as a photoautotrophic chassis for the integration of synthetic constructs, i.e. molecular constructs assembled from well characterized biological and/or synthetic parts (e.g. promoters, regulators, coding regions, terminators) designed for a specific purpose.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.052282-0
2012-02-01
2019-09-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/2/448.html?itemId=/content/journal/micro/10.1099/mic.0.052282-0&mimeType=html&fmt=ahah

References

  1. Abed R. M. , Dobretsov S. , Sudesh K. . ( 2009; ). Applications of cyanobacteria in biotechnology. . J Appl Microbiol 106:, 1–12. [CrossRef] [PubMed]
    [Google Scholar]
  2. Agafonov D. E. , Kolb V. A. , Spirin A. S. . ( 2001; ). Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. . EMBO Rep 2:, 399–402.[PubMed] [CrossRef]
    [Google Scholar]
  3. Ananyev G. , Carrieri D. , Dismukes G. C. . ( 2008; ). Optimization of metabolic capacity and flux through environmental cues to maximize hydrogen production by the cyanobacterium “Arthrospira (Spirulina) maxima”. . Appl Environ Microbiol 74:, 6102–6113. [CrossRef] [PubMed]
    [Google Scholar]
  4. Angermayr S. A. , Hellingwerf K. J. , Lindblad P. , Teixeira de Mattos M. J. . ( 2009; ). Energy biotechnology with cyanobacteria. . Curr Opin Biotechnol 20:, 257–263. [CrossRef] [PubMed]
    [Google Scholar]
  5. Antal T. K. , Lindblad P. . ( 2005; ). Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. . J Appl Microbiol 98:, 114–120. [CrossRef] [PubMed]
    [Google Scholar]
  6. Antal T. K. , Oliveira P. , Lindblad P. . ( 2006; ). The bidirectional hydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. . Int J Hydrogen Energy 31:, 1439–1444. [CrossRef]
    [Google Scholar]
  7. Appel J. , Schulz R. . ( 1996; ). Sequence analysis of an operon of a NAD(P)-reducing nickel hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 gives additional evidence for direct coupling of the enzyme to NAD(P)H-dehydrogenase (complex I). . Biochim Biophys Acta 1298:, 141–147. [CrossRef] [PubMed]
    [Google Scholar]
  8. Appel J. , Schulz R. . ( 1998; ). Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising?. J Photochem Photobiol B 47:, 1–11. [CrossRef]
    [Google Scholar]
  9. Appel J. , Phunpruch S. , Schulz R. . ( 1999; ). Hydrogenase(s) in Synechocystis – tools for Photohydrogen Production?. In BioHydrogen, pp. 189–196. Edited by Zaborsky O. R. , Benemann J. R. , Matsunaga T. , Miyake J. , San Pietro A. . . US:: Springer;. [CrossRef]
    [Google Scholar]
  10. Appel J. , Phunpruch S. , Steinmüller K. , Schulz R. . ( 2000; ). The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. . Arch Microbiol 173:, 333–338. [CrossRef] [PubMed]
    [Google Scholar]
  11. Barrios-Llerena M. E. , Chong P. K. , Gan C. S. , Snijders A. P. L. , Reardon K. F. , Wright P. C. . ( 2006; ). Shotgun proteomics of cyanobacteria–applications of experimental and data-mining techniques. . Brief Funct Genomics Proteomics 5:, 121–132. [CrossRef] [PubMed]
    [Google Scholar]
  12. Bashor C. J. , Horwitz A. A. , Peisajovich S. G. , Lim W. A. . ( 2010; ). Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. . Annu Rev Biophys 39:, 515–537. [CrossRef] [PubMed]
    [Google Scholar]
  13. Bhaya D. , Vaulot D. , Amin P. , Takahashi A. W. , Grossman A. R. . ( 2000; ). Isolation of regulated genes of the cyanobacterium Synechocystis sp. strain PCC 6803 by differential display. . J Bacteriol 182:, 5692–5699. [CrossRef] [PubMed]
    [Google Scholar]
  14. Bothe H. , Schmitz O. , Yates M. G. , Newton W. E. . ( 2010a; ). Nitrogen fixation and hydrogen metabolism in cyanobacteria. . Microbiol Mol Biol Rev 74:, 529–551. [CrossRef] [PubMed]
    [Google Scholar]
  15. Bothe H. , Tripp H. J. , Zehr J. P. . ( 2010b; ). Unicellular cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed. . Arch Microbiol 192:, 783–790. [CrossRef] [PubMed]
    [Google Scholar]
  16. Brand S. N. , Tan X. , Widger W. R. . ( 1992; ). Cloning and sequencing of the petBD operon from the cyanobacterium Synechococcus sp. PCC 7002. . Plant Mol Biol 20:, 481–491. [CrossRef] [PubMed]
    [Google Scholar]
  17. Burja A. M. , Banaigs B. , Abou-Mansour E. , Burgess J. G. , Wright P. C. . ( 2001; ). Marine cyanobacteria – a prolific source of natural products. . Tetrahedron 57:, 9347–9377. [CrossRef]
    [Google Scholar]
  18. Carrieri D. , Wawrousek K. , Eckert C. , Yu J. , Maness P.-C. . ( 2011; ). The role of the bidirectional hydrogenase in cyanobacteria. . Bioresour Technol 102:, 8368–8377. [CrossRef] [PubMed]
    [Google Scholar]
  19. Chong P. K. , Gan C. S. , Pham T. K. , Wright P. C. . ( 2006; ). Isobaric tags for relative and absolute quantitation (iTRAQ) reproducibility: Implication of multiple injections. . J Proteome Res 5:, 1232–1240. [CrossRef] [PubMed]
    [Google Scholar]
  20. Cournac L. , Mus F. , Bernard L. , Guedeney G. , Vignais P. , Peltier G. . ( 2002; ). Limiting steps of hydrogen production in Chlamydomonas reinhardtii and Synechocystis PCC 6803 as analysed by light-induced gas exchange transients. . Int J Hydrogen Energy 27:, 1229–1237. [CrossRef]
    [Google Scholar]
  21. Cournac L. , Guedeney G. , Peltier G. , Vignais P. M. . ( 2004; ). Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex. . J Bacteriol 186:, 1737–1746. [CrossRef] [PubMed]
    [Google Scholar]
  22. Cramer W. A. , Martinez S. E. , Furbacher P. N. , Huang D. , Smith J. L. . ( 1994; ). The cytochrome b6f complex. . Curr Opin Struct Biol 4:, 536–544. [CrossRef]
    [Google Scholar]
  23. Dembitsky V. M. . ( 2006; ). Anticancer activity of natural and synthetic acetylenic lipids. . Lipids 41:, 883–924. [CrossRef] [PubMed]
    [Google Scholar]
  24. Devillers J. , Doré J. C. , Guyot M. , Poroikov V. , Gloriozova T. , Lagunin A. , Filimonov D. . ( 2007; ). Prediction of biological activity profiles of cyanobacterial secondary metabolites. . SAR QSAR Environ Res 18:, 629–643. [CrossRef] [PubMed]
    [Google Scholar]
  25. Dubrac S. , Touati D. . ( 2000; ). Fur positive regulation of iron superoxide dismutase in Escherichia coli: functional analysis of the sodB promoter. . J Bacteriol 182:, 3802–3808. [CrossRef] [PubMed]
    [Google Scholar]
  26. Elias J. E. , Gygi S. P. . ( 2007; ). Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. . Nat Methods 4:, 207–214. [CrossRef] [PubMed]
    [Google Scholar]
  27. Endy D. . ( 2005; ). Foundations for engineering biology. . Nature 438:, 449–453. [CrossRef] [PubMed]
    [Google Scholar]
  28. Fernández de Henestrosa A. R. , Ogi T. , Aoyagi S. , Chafin D. , Hayes J. J. , Ohmori H. , Woodgate R. . ( 2000; ). Identification of additional genes belonging to the LexA regulon in Escherichia coli . . Mol Microbiol 35:, 1560–1572. [CrossRef] [PubMed]
    [Google Scholar]
  29. Ferreira D. , Pinto F. , Moradas-Ferreira P. , Mendes M. V. , Tamagnini P. . ( 2009; ). Transcription profiles of hydrogenases related genes in the cyanobacterium Lyngbya majuscula CCAP 1446/4. . BMC Microbiol 9:, 67.[PubMed] [CrossRef]
    [Google Scholar]
  30. Gan C. S. , Reardon K. F. , Wright P. C. . ( 2005; ). Comparison of protein and peptide prefractionation methods for the shotgun proteomic analysis of Synechocystis sp. PCC 6803. . Proteomics 5:, 2468–2478. [CrossRef] [PubMed]
    [Google Scholar]
  31. Gan C. S. , Chong P. K. , Pham T. K. , Wright P. C. . ( 2007; ). Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). . J Proteome Res 6:, 821–827. [CrossRef] [PubMed]
    [Google Scholar]
  32. Gómez-García M. R. , Losada M. , Serrano A. . ( 2003; ). Concurrent transcriptional activation of ppa and ppx genes by phosphate deprivation in the cyanobacterium Synechocystis sp. strain PCC 6803. . Biochem Biophys Res Commun 302:, 601–609. [CrossRef] [PubMed]
    [Google Scholar]
  33. Gutekunst K. , Phunpruch S. , Schwarz C. , Schuchardt S. , Schulz-Friedrich R. , Appel J. . ( 2005; ). LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. . Mol Microbiol 58:, 810–823. [CrossRef] [PubMed]
    [Google Scholar]
  34. Gutthann F. , Egert M. , Marques A. , Appel J. . ( 2007; ). Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803. . Biochim Biophys Acta 1767:, 161–169. [CrossRef] [PubMed]
    [Google Scholar]
  35. Hall H. K. , Foster J. W. . ( 1996; ). The role of Fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. . J Bacteriol 178:, 5683–5691.[PubMed]
    [Google Scholar]
  36. Hihara Y. , Muramatsu M. , Nakamura K. , Sonoike K. . ( 2004; ). A cyanobacterial gene encoding an ortholog of Pirin is induced under stress conditions. . FEBS Lett 574:, 101–105. [CrossRef] [PubMed]
    [Google Scholar]
  37. Johnson M. , Zaretskaya I. , Raytselis Y. , Merezhuk Y. , McGinnis S. , Madden T. L. . ( 2008; ). NCBI BLAST: a better web interface. . Nucleic Acids Res 36: (Web Server issue), W5–W9. [CrossRef] [PubMed]
    [Google Scholar]
  38. Kaneko T. , Sato S. , Kotani H. , Tanaka A. , Asamizu E. , Nakamura Y. , Miyajima N. , Hirosawa M. , Sugiura M. . & other authors ( 1996; ). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. . DNA Res 3:, 109–136. [CrossRef] [PubMed]
    [Google Scholar]
  39. Kaneko T. , Nakamura Y. , Sasamoto S. , Watanabe A. , Kohara M. , Matsumoto M. , Shimpo S. , Yamada M. , Tabata S. . ( 2003; ). Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803. . DNA Res 10:, 221–228. [CrossRef] [PubMed]
    [Google Scholar]
  40. Kanematsu S. , Sato S. . ( 2008; ). Cloning of Fe-superoxide dismutase gene from the diazotroph Azotobacter vinelandii and the stimulation of its expression under anaerobic conditions in Escherichia coli . . Bull Minamikyushu Univ 38A:, 7–18.
    [Google Scholar]
  41. Kawakami K. , Iwai M. , Ikeuchi M. , Kamiya N. , Shen J.-R. . ( 2007; ). Location of PsbY in oxygen-evolving photosystem II revealed by mutagenesis and X-ray crystallography. . FEBS Lett 581:, 4983–4987. [CrossRef] [PubMed]
    [Google Scholar]
  42. Keasling J. D. . ( 2008; ). Synthetic biology for synthetic chemistry. . ACS Chem Biol 3:, 64–76. [CrossRef] [PubMed]
    [Google Scholar]
  43. Khalil A. S. , Collins J. J. . ( 2010; ). Synthetic biology: applications come of age. . Nat Rev Genet 11:, 367–379. [CrossRef] [PubMed]
    [Google Scholar]
  44. Kim J.-H. , Suh K. H. . ( 2005; ). Light-dependent expression of superoxide dismutase from cyanobacterium Synechocystis sp. strain PCC 6803. . Arch Microbiol 183:, 218–223. [CrossRef] [PubMed]
    [Google Scholar]
  45. Kiss É. , Kós P. B. , Vass I. . ( 2009; ). Transcriptional regulation of the bidirectional hydrogenase in the cyanobacterium Synechocystis 6803. . J Biotechnol 142:, 31–37. [CrossRef] [PubMed]
    [Google Scholar]
  46. Kobayashi M. , Ishizuka T. , Katayama M. , Kanehisa M. , Bhattacharyya-Pakrasi M. , Pakrasi H. B. , Ikeuchi M. . ( 2004; ). Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp. PCC 6803. . Plant Cell Physiol 45:, 290–299. [CrossRef] [PubMed]
    [Google Scholar]
  47. Koksharova O. A. , Wolk C. P. . ( 2002; ). Genetic tools for cyanobacteria. . Appl Microbiol Biotechnol 58:, 123–137. [CrossRef] [PubMed]
    [Google Scholar]
  48. Kornberg A. . ( 1962; ). On the metabolic significance of phosphorolytic and pyrophosphorolytic reactions. . In Horizons in Biochemistry: Albert Szent-Györgyi Dedicatory Volume, pp. 251–264. Edited by Kasha M. , Pullman B. . . New York:: Academic Press, Inc;.
    [Google Scholar]
  49. Krenn B. E. , Strotmann H. , Van Walraven H. S. , Scholts M. J. C. , Kraayenhof R. . ( 1997; ). The ATP synthase γ subunit provides the primary site of activation of the chloroplast enzyme: experiments with a chloroplast-like Synechocystis 6803 mutant. . Biochem J 323:, 841–845.[PubMed]
    [Google Scholar]
  50. Kruip J. , Nixon P. J. , Osiewacz H. D. , Rögner M. . ( 1994; ). Nucleotide sequence of the petB gene encoding cytochrome b 6 from the mesophilic cyanobacterium Synechocystis PCC 6803: implications for evolution and function. . Biochim Biophys Acta 1188:, 443–446. [CrossRef] [PubMed]
    [Google Scholar]
  51. Kunert A. , Vinnemeier J. , Erdmann N. , Hagemann M. . ( 2003; ). Repression by Fur is not the main mechanism controlling the iron-inducible isiAB operon in the cyanobacterium Synechocystis sp. PCC 6803. . FEMS Microbiol Lett 227:, 255–262. [CrossRef] [PubMed]
    [Google Scholar]
  52. Leitão E. , Pereira S. , Bondoso J. , Ferreira D. , Pinto F. , Moradas-Ferreira P. , Tamagnini P. . ( 2006; ). Genes involved in the maturation of hydrogenase(s) in the nonheterocystous cyanobacterium Lyngbya majuscula CCAP 1446/4. . Int J Hydrogen Energy 31:, 1469–1477. [CrossRef]
    [Google Scholar]
  53. Li H. , Singh A. K. , McIntyre L. M. , Sherman L. A. . ( 2004; ). Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. . J Bacteriol 186:, 3331–3345. [CrossRef] [PubMed]
    [Google Scholar]
  54. Li S. , Xu M. , Su Z. . ( 2010; ). Computational analysis of LexA regulons in Cyanobacteria. . BMC Genomics 11:, 527. [CrossRef] [PubMed]
    [Google Scholar]
  55. Lindahl M. , Florencio F. J. . ( 2003; ). Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. . Proc Natl Acad Sci U S A 100:, 16107–16112. [CrossRef] [PubMed]
    [Google Scholar]
  56. Little J. W. , Mount D. W. . ( 1982; ). The SOS regulatory system of Escherichia coli . . Cell 29:, 11–22. [CrossRef] [PubMed]
    [Google Scholar]
  57. Ludwig M. , Schulz-Friedrich R. , Appel J. . ( 2006; ). Occurrence of hydrogenases in cyanobacteria and anoxygenic photosynthetic bacteria: implications for the phylogenetic origin of cyanobacterial and algal hydrogenases. . J Mol Evol 63:, 758–768. [CrossRef] [PubMed]
    [Google Scholar]
  58. Masukawa H. , Mochimaru M. , Sakurai H. . ( 2002; ). Disruption of the uptake hydrogenase gene, but not of the bidirectional hydrogenase gene, leads to enhanced photobiological hydrogen production by the nitrogen-fixing cyanobacterium Anabaena sp. PCC 7120. . Appl Microbiol Biotechnol 58:, 618–624. [CrossRef] [PubMed]
    [Google Scholar]
  59. McIntosh C. L. , Germer F. , Schulz R. , Appel J. , Jones A. K. . ( 2011; ). The [NiFe]-hydrogenase of the cyanobacterium Synechocystis sp. PCC 6803 works bidirectionally with a bias to H2 production. . J Am Chem Soc 133:, 11308–11319. [CrossRef] [PubMed]
    [Google Scholar]
  60. McNeely K. , Xu Y. , Bennette N. , Bryant D. A. , Dismukes G. C. . ( 2010; ). Redirecting reductant flux into hydrogen production via metabolic engineering of fermentative carbon metabolism in a cyanobacterium. . Appl Environ Microbiol 76:, 5032–5038. [CrossRef] [PubMed]
    [Google Scholar]
  61. Moisander P. H. , Beinart R. A. , Hewson I. , White A. E. , Johnson K. S. , Carlson C. A. , Montoya J. P. , Zehr J. P. . ( 2010; ). Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. . Science 327:, 1512–1514. [CrossRef] [PubMed]
    [Google Scholar]
  62. Motohashi K. , Kondoh A. , Stumpp M. T. , Hisabori T. . ( 2001; ). Comprehensive survey of proteins targeted by chloroplast thioredoxin. . Proc Natl Acad Sci U S A 98:, 11224–11229. [CrossRef] [PubMed]
    [Google Scholar]
  63. Nakamura Y. , Kaneko T. , Tabata S. . ( 2000; ). CyanoBase, the genome database for Synechocystis sp. strain PCC6803: status for the year 2000. . Nucleic Acids Res 28:, 72. [CrossRef] [PubMed]
    [Google Scholar]
  64. Navarro F. , Martín-Figueroa E. , Florencio F. J. . ( 2000; ). Electron transport controls transcription of the thioredoxin gene (trxA) in the cyanobacterium Synechocystis sp. PCC 6803. . Plant Mol Biol 43:, 23–32. [CrossRef] [PubMed]
    [Google Scholar]
  65. Nefedova L. N. , Mel'nik V. A. , Babykin M. M. . ( 2003; ). Mutants of cyanobacterium Synechocystis sp. PCC 6803 with insertional inactivation of the sodB gene encoding Fe-superoxide dismutase. . Russ J Genet 39:, 386–389. [CrossRef]
    [Google Scholar]
  66. Noirel J. , Sanguinetti G. , Wright P. C. . ( 2008; ). Identifying differentially expressed subnetworks with MMG. . Bioinformatics 24:, 2792–2793. [CrossRef] [PubMed]
    [Google Scholar]
  67. Noirel J. , Ow S. Y. , Sanguinetti G. , Wright P. C. . ( 2009; ). Systems biology meets synthetic biology: a case study of the metabolic effects of synthetic rewiring. . Mol Biosyst 5:, 1214–1223. [CrossRef] [PubMed]
    [Google Scholar]
  68. Noirel J. , Evans C. , Salim M. , Mukherjee J. , Ow S. Y. , Pandhal J. , Pham T. K. , Biggs C. A. , Wright P. C. . ( 2011; ). Methods in quantitative proteomics: setting iTRAQ on the right track. . Curr Proteomics 8:, 17–30. [CrossRef]
    [Google Scholar]
  69. Nunoshiba T. , Obata F. , Boss A. C. , Oikawa S. , Mori T. , Kawanishi S. , Yamamoto K. . ( 1999; ). Role of iron and superoxide for generation of hydroxyl radical, oxidative DNA lesions, and mutagenesis in Escherichia coli . . J Biol Chem 274:, 34832–34837. [CrossRef] [PubMed]
    [Google Scholar]
  70. Oliveira P. . ( 2008; ). Regulation of the Cyanobacterial Bidirectional Hydrogenase, pp. 63. Uppsala:: Acta Universitatis Upsaliensis;.
    [Google Scholar]
  71. Oliveira P. , Lindblad P. . ( 2005; ). LexA, a transcription regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. . FEMS Microbiol Lett 251:, 59–66. [CrossRef] [PubMed]
    [Google Scholar]
  72. Oliveira P. , Lindblad P. . ( 2008; ). An AbrB-Like protein regulates the expression of the bidirectional hydrogenase in Synechocystis sp. strain PCC 6803. . J Bacteriol 190:, 1011–1019. [CrossRef] [PubMed]
    [Google Scholar]
  73. Oliveira P. , Lindblad P. . ( 2009; ). Transcriptional regulation of the cyanobacterial bidirectional Hox-hydrogenase. . Dalton Trans (45), 9990–9996. [CrossRef] [PubMed]
    [Google Scholar]
  74. Osanai T. , Kanesaki Y. , Nakano T. , Takahashi H. , Asayama M. , Shirai M. , Kanehisa M. , Suzuki I. , Murata N. , Tanaka K. . ( 2005; ). Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 σ factor sigE. . J Biol Chem 280:, 30653–30659. [CrossRef] [PubMed]
    [Google Scholar]
  75. Ow S. Y. , Wright P. C. . ( 2009; ). Current trends in high throughput proteomics in cyanobacteria. . FEBS Lett 583:, 1744–1752. [CrossRef] [PubMed]
    [Google Scholar]
  76. Ow S. Y. , Salim M. , Noirel J. , Evans C. , Rehman I. , Wright P. C. . ( 2009; ). iTRAQ underestimation in simple and complex mixtures: “the good, the bad and the ugly”. . J Proteome Res 8:, 5347–5355. [CrossRef] [PubMed]
    [Google Scholar]
  77. Padan E. , Bibi E. , Ito M. , Krulwich T. A. . ( 2005; ). Alkaline pH homeostasis in bacteria: new insights. . Biochim Biophys Acta 1717:, 67–88. [CrossRef] [PubMed]
    [Google Scholar]
  78. Patterson-Fortin L. M. , Colvin K. R. , Owttrim G. W. . ( 2006; ). A LexA-related protein regulates redox-sensitive expression of the cyanobacterial RNA helicase, crhR . . Nucleic Acids Res 34:, 3446–3454. [CrossRef] [PubMed]
    [Google Scholar]
  79. Pérez-Pérez M. E. , Martín-Figueroa E. , Florencio F. J. . ( 2009; ). Photosynthetic regulation of the cyanobacterium Synechocystis sp. PCC 6803 thioredoxin system and functional analysis of TrxB (Trx x) and TrxQ (Trx y) thioredoxins. . Mol Plant 2:, 270–283. [CrossRef] [PubMed]
    [Google Scholar]
  80. Pham T. K. , Roy S. , Noirel J. , Douglas I. , Wright P. C. , Stafford G. P. . ( 2010; ). A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia . . Proteomics 10:, 3130–3141. [CrossRef] [PubMed]
    [Google Scholar]
  81. Pósfai G. , Plunkett G. III , Fehér T. , Frisch D. , Keil G. M. , Umenhoffer K. , Kolisnychenko V. , Stahl B. , Sharma S. S. . & other authors ( 2006; ). Emergent properties of reduced-genome Escherichia coli . . Science 312:, 1044–1046. [CrossRef] [PubMed]
    [Google Scholar]
  82. Reidegeld K. A. , Eisenacher M. , Kohl M. , Chamrad D. , Körting G. , Blüggel M. , Meyer H. E. , Stephan C. . ( 2008; ). An easy-to-use Decoy Database Builder software tool, implementing different decoy strategies for false discovery rate calculation in automated MS/MS protein identifications. . Proteomics 8:, 1129–1137. [CrossRef] [PubMed]
    [Google Scholar]
  83. Sakthivel K. , Watanabe T. , Nakamoto H. . ( 2009; ). A small heat-shock protein confers stress tolerance and stabilizes thylakoid membrane proteins in cyanobacteria under oxidative stress. . Arch Microbiol 191:, 319–328. [CrossRef] [PubMed]
    [Google Scholar]
  84. Sambrook J. , Russell D. W. . ( 2001; ). Molecular Cloning: a Laboratory Manual. New York, USA:: Cold Spring Harbor Laboratory Press;.
    [Google Scholar]
  85. Sanguinetti G. , Noirel J. , Wright P. C. . ( 2008; ). MMG: a probabilistic tool to identify submodules of metabolic pathways. . Bioinformatics 24:, 1078–1084. [CrossRef] [PubMed]
    [Google Scholar]
  86. Sato S. , Shimoda Y. , Muraki A. , Kohara M. , Nakamura Y. , Tabata S. . ( 2007; ). A large-scale protein–protein interaction analysis in Synechocystis sp. PCC6803. . DNA Res 14:, 207–216. [CrossRef] [PubMed]
    [Google Scholar]
  87. Schäfer A. , Tauch A. , Jäger W. , Kalinowski J. , Thierbach G. , Pühler A. . ( 1994; ). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum . . Gene 145:, 69–73. [CrossRef] [PubMed]
    [Google Scholar]
  88. Schmitt W. A. Jr , Stephanopoulos G. . ( 2003; ). Prediction of transcriptional profiles of Synechocystis PCC6803 by dynamic autoregressive modeling of DNA microarray data. . Biotechnol Bioeng 84:, 855–863. [CrossRef] [PubMed]
    [Google Scholar]
  89. Schmitz O. , Bothe H. . ( 1996; ). The diaphorase subunit HoxU of the bidirectional hydrogenase as electron transferring protein in cyanobacterial respiration?. Naturwissenschaften 83:, 525–527. [CrossRef] [PubMed]
    [Google Scholar]
  90. Schütz K. , Happe T. , Troshina O. , Lindblad P. , Leitão E. , Oliveira P. , Tamagnini P. . ( 2004; ). Cyanobacterial H2 production – a comparative analysis. . Planta 218:, 350–359. [CrossRef] [PubMed]
    [Google Scholar]
  91. Sharma S. S. , Blattner F. R. , Harcum S. W. . ( 2007a; ). Recombinant protein production in an Escherichia coli reduced genome strain. . Metab Eng 9:, 133–141. [CrossRef] [PubMed]
    [Google Scholar]
  92. Sharma S. S. , Campbell J. W. , Frisch D. , Blattner F. R. , Harcum S. W. . ( 2007b; ). Expression of two recombinant chloramphenicol acetyltransferase variants in highly reduced genome Escherichia coli strains. . Biotechnol Bioeng 98:, 1056–1070. [CrossRef] [PubMed]
    [Google Scholar]
  93. Shcolnick S. , Summerfield T. C. , Reytman L. , Sherman L. A. , Keren N. . ( 2009; ). The mechanism of iron homeostasis in the unicellular cyanobacterium Synechocystis sp. PCC 6803 and its relationship to oxidative stress. . Plant Physiol 150:, 2045–2056. [CrossRef] [PubMed]
    [Google Scholar]
  94. Sherman D. M. , Troyan T. A. , Sherman L. A. . ( 1994; ). Localization of membrane proteins in the cyanobacterium Synechococcus sp. PCC7942 (radial asymmetry in the photosynthetic complexes). . Plant Physiol 106:, 251–262.[PubMed]
    [Google Scholar]
  95. Sjöholm J. , Oliveira P. , Lindblad P. . ( 2007; ). Transcription and regulation of the bidirectional hydrogenase in the cyanobacterium Nostoc sp. strain PCC 7120. . Appl Environ Microbiol 73:, 5435–5446. [CrossRef] [PubMed]
    [Google Scholar]
  96. Stal L. J. , Moezelaar R. . ( 1997; ). Fermentation in cyanobacteria. . FEMS Microbiol Rev 21:, 179–211. [CrossRef]
    [Google Scholar]
  97. Stanier R. Y. , Kunisawa R. , Mandel M. , Cohen-Bazire G. . ( 1971; ). Purification and properties of unicellular blue-green algae (order Chroococcales). . Bacteriol Rev 35:, 171–205.[PubMed]
    [Google Scholar]
  98. Stroebel D. , Choquet Y. , Popot J.-L. , Picot D. . ( 2003; ). An atypical haem in the cytochrome b6f complex. . Nature 426:, 413–418. [CrossRef] [PubMed]
    [Google Scholar]
  99. Summerfield T. C. , Sherman L. A. . ( 2008; ). Global transcriptional response of the alkali-tolerant cyanobacterium Synechocystis sp. strain PCC 6803 to a pH 10 environment. . Appl Environ Microbiol 74:, 5276–5284. [CrossRef] [PubMed]
    [Google Scholar]
  100. Summerfield T. C. , Nagarajan S. , Sherman L. A. . ( 2011; ). Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses. . Microbiology 157:, 301–312. [CrossRef] [PubMed]
    [Google Scholar]
  101. Suzuki I. , Simon W. J. , Slabas A. R. . ( 2006; ). The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics. . J Exp Bot 57:, 1573–1578. [CrossRef] [PubMed]
    [Google Scholar]
  102. Tamagnini P. , Troshina O. , Oxelfelt F. , Salema R. , Lindblad P. . ( 1997; ). Hydrogenases in Nostoc sp. strain PCC 73102, a strain lacking a bidirectional enzyme. . Appl Environ Microbiol 63:, 1801–1807.[PubMed]
    [Google Scholar]
  103. Tamagnini P. , Costa J. L. , Almeida L. , Oliveira M. J. , Salema R. , Lindblad P. . ( 2000; ). Diversity of cyanobacterial hydrogenases, a molecular approach. . Curr Microbiol 40:, 356–361. [CrossRef] [PubMed]
    [Google Scholar]
  104. Tamagnini P. , Axelsson R. , Lindberg P. , Oxelfelt F. , Wünschiers R. , Lindblad P. . ( 2002; ). Hydrogenases and hydrogen metabolism of cyanobacteria. . Microbiol Mol Biol Rev 66:, 1–20. [CrossRef] [PubMed]
    [Google Scholar]
  105. Tamagnini P. , Leitão E. , Oliveira P. , Ferreira D. , Pinto F. , Harris D. J. , Heidorn T. , Lindblad P. . ( 2007; ). Cyanobacterial hydrogenases: diversity, regulation and applications. . FEMS Microbiol Rev 31:, 692–720. [CrossRef] [PubMed]
    [Google Scholar]
  106. Thajuddin N. , Subramanian G. . ( 2005; ). Cyanobacterial biodiversity and potential applications in biotechnology. . Curr Sci 89:, 47–57.
    [Google Scholar]
  107. Troshina O. , Serebryakova L. , Sheremetieva M. , Lindblad P. . ( 2002; ). Production of H2 by the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermentation. . Int J Hydrogen Energy 27:, 1283–1289. [CrossRef]
    [Google Scholar]
  108. Ushimaru T. , Nishiyama Y. , Hayashi H. , Murata N. . ( 2002; ). No coordinated transcriptional regulation of the sod-kat antioxidative system in Synechocystis sp. PCC 6803. . J Plant Physiol 159:, 805–807. [CrossRef]
    [Google Scholar]
  109. van der Oost J. , Bulthuis B. A. , Feitz S. , Krab K. , Kraayenhof R. . ( 1989; ). Fermentation metabolism of the unicellular cyanobacterium Cyanothece PCC 7822. . Arch Microbiol 152:, 415–419. [CrossRef]
    [Google Scholar]
  110. Vila-Sanjurjo A. , Schuwirth B.-S. , Hau C. W. , Cate J. H. D. . ( 2004; ). Structural basis for the control of translation initiation during stress. . Nat Struct Mol Biol 11:, 1054–1059. [CrossRef] [PubMed]
    [Google Scholar]
  111. Vinnemeier J. , Kunert A. , Hagemann M. . ( 1998; ). Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. . FEMS Microbiol Lett 169:, 323–330. [CrossRef] [PubMed]
    [Google Scholar]
  112. Williams J. G. K. . ( 1988; ). Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. . Methods Enzymol 167:, 766–778. [CrossRef]
    [Google Scholar]
  113. Xu W. D. , McFadden B. A. . ( 1997; ). Sequence analysis of plasmid pCC5.2 from cyanobacterium Synechocystis PCC 6803 that replicates by a rolling circle mechanism. . Plasmid 37:, 95–104. [CrossRef] [PubMed]
    [Google Scholar]
  114. Yadav V. G. , Stephanopoulos G. . ( 2010; ). Reevaluating synthesis by biology. . Curr Opin Microbiol 13:, 371–376. [CrossRef] [PubMed]
    [Google Scholar]
  115. Yang X. Y. , McFadden B. A. . ( 1993; ). A small plasmid, pCA2.4, from the cyanobacterium Synechocystis sp. strain PCC 6803 encodes a Rep protein and replicates by a rolling circle mechanism. . J Bacteriol 175:, 3981–3991.[PubMed]
    [Google Scholar]
  116. Yang X. Y. , McFadden B. A. . ( 1994; ). The complete DNA sequence and replication analysis of the plasmid pCB2.4 from the cyanobacterium Synechocystis PCC 6803. . Plasmid 31:, 131–137. [CrossRef] [PubMed]
    [Google Scholar]
  117. Zhang Z. , Pendse N. D. , Phillips K. N. , Cotner J. B. , Khodursky A. . ( 2008; ). Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. . BMC Genomics 9:, 344. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.052282-0
Loading
/content/journal/micro/10.1099/mic.0.052282-0
Loading

Data & Media loading...

Supplementary material 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error