Improving a Synechocystis-based photoautotrophic chassis through systematic genome mapping and validation of neutral sites

DNA Research

Volumn 22, Issue 6, 2015, Pages 425-437

  Pinto, Filipe ^a,b,c   Pacheco, Catarina C ^a,b   Oliveira, Paulo ^a,b   Montagud, Arnau ^d,f   Landels, Andrew ^e   Couto, Narciso ^e   Wright, Phillip C ^e   Urchueguía, Javier F ^d   Tamagnini, Paula ^a,b,c  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

^f INSERM U900   (France)

Author keywords

neutral sites; photoautotrophic chassis; Synechocystis; synthetic biology

Indexed keywords

CHROMOSOME; DNA TRANSCRIPTION; GENE MAPPING; GENETIC TRANSCRIPTION; INDEL MUTATION; SYNECHOCYSTIS; SYNTHETIC BIOLOGY; VALIDATION PROCESS; AUTOTROPHY; CHROMOSOMAL MAPPING; CYANOBACTERIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION; PROCEDURES;

GREEN FLUORESCENT PROTEIN;

AUTOTROPHIC PROCESSES; CHROMOSOME MAPPING; CYANOBACTERIA; GREEN FLUORESCENT PROTEINS; MUTATION; SYNECHOCYSTIS; SYNTHETIC BIOLOGY;

EID: 84950258160     PISSN: 13402838     EISSN: 17561663     Source Type: Journal    
DOI: 10.1093/dnares/dsv024     Document Type: Article

References (53)

1. Madigan, M.T., Martinko, J.M., Stahl, D.A. and Clark, D.P. 2010, Brock biology of microorganisms. Benjamin Cummings: San Francisco.
2. Harwood, C.R., Pohl, S., Smith, W. and Wipat, A. 2013, Bacillus subtilis: model Gram-positive synthetic biology chassis. In: Colin, H. and Anil, W. (eds), Methods in microbiology. Academic Press: Amsterdam, The Netherlands, pp. 87-117.
3. Li, M. and Borodina, I. 2014, Application of synthetic biology for production of chemicals in yeast Saccharomyces cerevisiae, FEMS Yeast Res., 15, 1-12.
4. Berla, B.M., Saha, R., Immethun, C.M., Maranas, C.D., Moon, T.S. and Pakrasi, H.B. 2013, Synthetic biology of cyanobacteria: unique challenges and opportunities, Front. Microbiol., 4, 246.
5. Whitton, B.A. and Potts, M. 2000, Introduction to the cyanobacteria. In: Whitton, B. and Potts, M. (eds), The ecology of cyanobacteria-their diversity in time and space. Kluwer Academic Publishers: Dordrecht, The Netherlands, pp. 1-11.
6. Montagud, A., Navarro, E., Fernandez de Cordoba, P., Urchueguia, J. and Patil, K. 2010, Reconstruction and analysis of genome-scale metabolic model of a photosynthetic bacterium, BMC Syst. Biol., 4, 156.
7. Kaneko, T., Sato, S., Kotani, H., et al. 1996, Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions, DNA Res., 3, 109-36.
8. Koksharova, O.A. and Wolk, C.P. 2002, Genetic tools for cyanobacteria, Appl. Microbiol. Biotechnol., 58, 123-37.
9. Heidorn, T., Camsund, D., Huang, H.-H., et al. 2011, Synthetic biology in cyanobacteria: engineering and analyzing novel functions. In: Chris, V. (ed.), Methods enzymol. Academic Press: New York, pp. 539-79.
10. Taton, A., Unglaub, F., Wright, N.E., et al. 2014, Broad-host-range vector system for synthetic biology and biotechnology in cyanobacteria, Nucleic Acids Res., 42, e136.
11. Williams, J.G.K. 1988, Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. In: Packer, L. and Glazer, A.N. (eds), Methods enzymol. Academic Press: New York, pp. 766-78.
12. Burnap, R.L., Qian, M., Shen, J.R., Inoue, Y. and Sherman, L.A. 1994, Role of disulfide linkage and putative intermolecular binding residues in the stability and binding of the extrinsic manganese-stabilizing protein to the photosystem II reaction center, Biochemistry US, 33, 13712-18.
13. Aoki, R., Goto, T. and Fujita, Y. 2011, A heme oxygenase isoform is essential for aerobic growth in the cyanobacterium Synechocystis sp. PCC 6803: modes of differential operation of two isoforms/enzymes to adapt to low oxygen environments in cyanobacteria, Plant Cell Physiol., 52, 1744-56.
14. Aoki, S., Kondo, T. and Ishiura, M. 1995, Circadian expression of the dnaK gene in the cyanobacterium Synechocystis sp. strain PCC 6803, J. Bacteriol., 177, 5606-11.
15. Ng, A.H., Berla, B.M. and Pakrasi, H.B. 2015, Fine-tuning of photoautotrophic protein production by combining promoters and neutral sites in the cyanobacterium Synechocystis sp. strain PCC 6803, Appl. Environ. Microbiol., 81, 6857-63.
16. Clerico, E.M., Ditty, J.L. and Golden, S.S. 2007, Specialized techniques for site-directed mutagenesis in cyanobacteria. In: Rosato, E. (ed.), Circadian rhythms. Humana Press: Totowa, pp. 155-71.
17. Trautmann, D., Voß, B., Wilde, A., Al-Babili, S. and Hess, W.R. 2012, Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803, DNA Res., 19, 435-48.
18. Kanesaki, Y., Shiwa, Y., Tajima, N., et al. 2012, Identification of substrainspecific mutations by massively parallel whole-genome resequencing of Synechocystis sp. PCC 6803, DNA Res., 19, 67-79.
19. Stanier, R.Y., Kunisawa, R., Mandel, M. and Cohenbaz, G. 1971, Purification and properties of unicellular blue-green algae (order Chroococcales), Bacteriol. Rev., 35, 171-205.
20. Sambrook, J. and Russell, D.W. 2001, Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press: New York.
21. Tamagnini, P., Troshina, O., Oxelfelt, F., Salema, R. and Lindblad, P. 1997, Hydrogenases in Nostoc sp. strain PCC 73102, a strain lacking a bidirectional enzyme, Appl. Environ. Microbiol., 63, 1801-7.
22. Leitão, E., Pereira, S., Bondoso, J., et al. 2006, Genes involved in the maturation of hydrogenase(s) in the nonheterocystous cyanobacterium Lyngbya majuscula CCAP 1446/4, Int. J. Hydrogen Energ., 31, 1469-77.
23. Ferreira, D., Pinto, F., Moradas-Ferreira, P., Mendes, M. and Tamagnini, P. 2009, Transcription profiles of hydrogenases related genes in the cyanobacterium Lyngbya majuscula CCAP 1446/4, BMC Microbiol., 9, 67.
24. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G. and 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.
25. Eriksson, J., Salih, G.F., Ghebramedhin, H. and Jansson, C. 2000, Deletion mutagenesis of the 5′ psbA2 region in Synechocystis 6803: identification of a putative cis element involved in photoregulation, Mol. Cell. Biol. Res. Commun., 3, 292-8.
26. Shibato, J.S., Agrawal, G.A., Kato, H.K., Asayama, M.A. and Shirai, M.S. 2002, The 5′-upstream cis-acting sequences of a cyanobacterial psbA gene: analysis of their roles in basal, light-dependent and circadian transcription, Mol. Genet. Genomics, 267, 684-94.
27. Pinto, F., Pacheco, C.C., Ferreira, D., Moradas-Ferreira, P. and Tamagnini, P. 2012, Selection of suitable reference genes for RT-qPCR analyses in cyanobacteria, PLoS One, 7, e34983.
28. Bustin, S.A., Benes, V., Garson, J.A., et al. 2009, The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments, Clin. Chem., 55, 611-22.
29. Bensadoun, A. and Weinstein, D. 1976, Assay of proteins in the presence of interfering materials, Anal. Biochem., 70, 241-50.
30. Reidegeld, K.A., Eisenacher, M., Kohl, M., et al. 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, 1129-37.
31. Elias, J.E. and Gygi, S.P. 2007, Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry, Nat. Methods, 4, 207-14.
32. Ow, S.Y., Salim, M., Noirel, J., Evans, C., Rehman, I. and Wright, P.C. 2009, iTRAQ underestimation in simple and complex mixtures: "the good, the bad and the ugly", J. Proteome Res., 8, 5347-55.
33. Pham, T.K., Roy, S., Noirel, J., Douglas, I., Wright, P.C. and Stafford, G.P. 2010, A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia, Proteomics, 10, 3130-41.
34. Matsunaga, T. and Takeyama, H. 1995, Genetic engineering in marine cyanobacteria, J. Appl. Phycol., 7, 77-84.
35. Vioque, A. 2007, Transformation of cyanobacteria. In: León, R., Galván, A. and Fernández, E. (eds), Volume 616, Transgenic Microalgae as Green Cell Factories, Adv. Exp. Med. Biol., Springer: New York, pp. 12-22.
36. De Gelder, L., Ponciano, J.M., Joyce, P. and Top, E.M. 2007, Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship, Microbiology, 153, 452-63.
37. Meyer, R. 2009, Replication and conjugative mobilization of broad host-range IncQ plasmids, Plasmid, 62, 57-70.
38. Berla, B.M. and Pakrasi, H.B. 2012, Up-regulation of plasmid-encoded genes during stationary phase in Synechocystis sp. PCC 6803, a cyanobacterium, Appl. Environ. Microbiol., 78, 5448-51.
39. Griese, M., Lange, C. and Soppa, J. 2011, Ploidy in cyanobacteria, FEMS Microbiol. Lett., 323, 124-31.
40. Sergeyenko, T.V. and Los, D.A. 2000, Identification of secreted proteins of the cyanobacterium Synechocystis sp. strain PCC 6803, FEMS Microbiol. Lett., 193, 213-6.
41. Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., et al. 2009, CDD: specific functional annotation with the Conserved Domain Database, Nucleic Acids Res., 37, D205-10.
42. Mitschke, J., Georg, J., Scholz, I., et al. 2011, An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803, Proc. Natl Acad. Sci. USA, 108, 2124-9.
43. Kopf, M., Klähn, S., Scholz, I., Matthiessen, J.K.F., Hess, W.R. and Voß, B. 2014, Comparative analysis of the primary transcriptome of Synechocystis sp. PCC 6803, DNA Res., 21, 527-39.
44. - uptake in Synechocystis sp. strain PCC 6803, J. Bacteriol., 182, 2591-6.
45. Huckauf, J., Nomura, C., Forchhammer, K. and Hagemann, M. 2000, Stress responses of Synechocystis sp. strain PCC 6803 mutants impaired in genes encoding putative alternative sigma factors, Microbiology, 146, 2877-89.
46. Zhou, H., Hu, H. and Lai, M. 2010, Non-coding RNAs and their epigenetic regulatory mechanisms, Biol. Cell, 102, 645-55.
47. Morris, K.V. 2012, Non-coding RNAs and the epigenetic regulation of gene expression: drivers of natural selection. Caister Academic Press: Norfolk, UK.
48. Git, A., Dvinge, H., Salmon-Divon, M., et al. 2010, Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression, RNA, 16, 991-1006.
49. Ishii, A. and Hihara, Y. 2008, An AbrB-like transcriptional regulator, Sll0822, is essential for the activation of nitrogen-regulated genes in Synechocystis sp. PCC 6803, Plant Physiol., 148, 660-70.
50. Oliveira, P. and Lindblad, P. 2008, An AbrB-like protein regulates the expression of the bidirectional hydrogenase in Synechocystis sp. strain PCC 6803, J. Bacteriol., 190, 1011-9.
51. Lopo, M., Montagud, A., Navarro, E., et al. 2012, Experimental and modeling analysis of Synechocystis sp. PCC 6803 growth, J. Mol. Microbiol. Biotechnol., 22, 71-82.
52. Prakash, J.S.S., Sinetova, M., Zorina, A., et al. 2009, DNA supercoiling regulates the stress-inducible expression of genes in the cyanobacterium Synechocystis, Mol. Biosyst., 5, 1904-12.
53. Fulda, S., Mikkat, S., Huang, F., et al. 2006, Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803, Proteomics, 6, 2733-45.