Regulation of gene expression in diverse cyanobacterial species by using theophylline-responsive riboswitches

Applied and Environmental Microbiology

Volumn 80, Issue 21, 2014, Pages 6704-6713

  Ma, Amy T ^a   Schmidt, Calvin M ^a,b   Golden, James W ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATMOSPHERIC CHEMISTRY; BACTERIA; CARBON DIOXIDE; GENE EXPRESSION; GENETIC ENGINEERING; PRODUCTION PLATFORMS; PROTEINS;

ATMOSPHERIC CARBON DIOXIDE; BIOLOGICAL PRODUCTION; BIOMASS ACCUMULATION; CYANOBACTERIAL SPECIES; GENETIC MANIPULATIONS; PHOTOSYNTHETIC BACTERIAS; SYNECHOCOCCUS ELONGATUS; YELLOW FLUORESCENT PROTEINS;

GENE EXPRESSION REGULATION;

BIOFUEL; BIOLOGICAL PRODUCTION; CYANOBACTERIUM; GENE EXPRESSION; GENETIC VARIATION; NITROGEN FIXATION; PHOTOSYNTHESIS; PROTEIN;

CYANOBACTERIA;

BACTERIAL PROTEIN; PHOTOPROTEIN; RIBOSWITCH; THEOPHYLLINE; YELLOW FLUORESCENT PROTEIN, BACTERIA;

CYANOBACTERIUM; DRUG EFFECTS; EVALUATION STUDY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIAL GENETICS; MOLECULAR BIOLOGY; PROCEDURES; REPORTER GENE; RIBOSWITCH;

BACTERIAL PROTEINS; CYANOBACTERIA; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GENETICS, MICROBIAL; LUMINESCENT PROTEINS; MOLECULAR BIOLOGY; RIBOSWITCH; THEOPHYLLINE;

EID: 84914159675     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01697-14     Document Type: Article

References (44)

1. Georgianna DR, Mayfield SP. 2012. Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488:329-335. http://dx.doi.org/10.1038/nature11479.
2. Gimpel JA, Specht EA, Georgianna DR, Mayfield SP. 2013. Advances in microalgae engineering and synthetic biology applications for biofuel production. Curr. Opin. Chem. Biol. 17:489-495. http://dx.doi.org/10.1016/j.cbpa.2013.03.038.
3. Berla BM, Saha R, Immethun CM, Maranas CD, Moon TS, Pakrasi HB. 2013. Synthetic biology of cyanobacteria: unique challenges and opportunities. Front. Microbiol. 4:246. http://dx.doi.org/10.3389/fmicb.2013.00246.
4. Ducat DC, Way JC, Silver PA. 2011. Engineering cyanobacteria to generate high-value products. Trends Biotechnol. 29:95-103. http://dx.doi.org/10.1016/j.tibtech.2010.12.003.
5. Rosgaard L, de Porcellinis AJ, Jacobsen JH, Frigaard NU, Sakuragi Y. 2012. Bioengineering of carbon fixation, biofuels, and biochemicals in cyanobacteria and plants. J. Biotechnol. 162:134-147. http://dx.doi.org/10.1016/j.jbiotec.2012.05.006.
6. Gupta V, Ratha SK, Sood A, Chaudhary V, Prasanna R. 2013. New insights into the biodiversity and applications of cyanobacteria (bluegreen algae)-prospects and challenges. Algal Res. 2:79-97. http://dx.doi.org/10.1016/j.algal.2013.01.006.
7. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, Calteau A, Cai F, Tandeau de Marsac N, Rippka R, Herdman M, Sivonen K, Coursin T, Laurent T, Goodwin L, Nolan M, Davenport KW, Han CS, Rubin EM, Eisen JA, Woyke T, Gugger M, Kerfeld CA. 2013. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. U. S. A. 110:1053-1058. http://dx.doi.org/10.1073/pnas.1217107110.
8. Ruffing AM. 2011. Engineered cyanobacteria: teaching an old bug new tricks. Bioeng. Bugs 2:136-149. http://dx.doi.org/10.4161/bbug.2.3.15285.
9. Wang B, Wang J, Zhang W, Meldrum DR. 2012. Application of synthetic biology in cyanobacteria and algae. Front. Microbiol. 3:344. http://dx.doi.org/10.3389/fmicb.2012.00344.
10. Huang HH, Camsund D, Lindblad P, Heidorn T. 2010. Design and characterization of molecular tools for a synthetic biology approach towards developing cyanobacterial biotechnology. Nucleic Acids Res. 38: 2577-2593. http://dx.doi.org/10.1093/nar/gkq164.
11. Huang HH, Lindblad P. 2013. Wide-dynamic-range promoters engineered for cyanobacteria. J. Biol. Eng. 7:10. http://dx.doi.org/10.1186/1754-1611-7-10.
12. Breaker RR. 2011. Prospects for riboswitch discovery and analysis. Mol. Cell 43:867-879. http://dx.doi.org/10.1016/j.molcel.2011.08.024.
13. Wachter A. 2010. Riboswitch-mediated control of gene expression in eukaryotes. RNA Biol. 7:67-76. http://dx.doi.org/10.4161/rna.7.1.10489.
14. Topp S, Reynoso CM, Seeliger JC, Goldlust IS, Desai SK, Murat D, Shen A, Puri AW, Komeili A, Bertozzi CR, Scott JR, Gallivan JP. 2010. Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl. Environ. Microbiol. 76:7881-7884. http://dx.doi.org/10.1128/AEM.01537-10.
15. Seeliger JC, Topp S, Sogi KM, Previti ML, Gallivan JP, Bertozzi CR. 2012. A riboswitch-based inducible gene expression system for mycobacteria. PLoS One 7(1):e29266. http://dx.doi.org/10.1371/journal.pone.0029266.
16. Reynoso CM, Miller MA, Bina JE, Gallivan JP, Weiss DS. 2012. Riboswitches for intracellular study of genes involved in Francisella pathogenesis. mBio 3(6):e00253-12. http://dx.doi.org/10.1128/mBio.00253-12.
17. Rudolph MM, Vockenhuber MP, Suess B. 2013. Synthetic riboswitches for the conditional control of gene expression in Streptomyces coelicolor. Microbiology 159:1416-1422. http://dx.doi.org/10.1099/mic.0.067322-0.
18. Nakahira Y, Ogawa A, Asano H, Oyama T, Tozawa Y. 2013. Theophylline-dependent riboswitch as a novel genetic tool for strict regulation of protein expression in cyanobacterium Synechococcus elongatus PCC 7942. Plant Cell Physiol. 54:1724-1735. http://dx.doi.org/10.1093/pcp/pct115.
19. Elledge SJ, Davis RW. 1989. Position and density effects on repression by stationary and mobile DNA-binding proteins. Genes Dev. 3:185-197. http://dx.doi.org/10.1101/gad.3.2.185.
20. Clerico EM, Ditty JL, Golden SS. 2007. Specialized techniques for sitedirected mutagenesis in cyanobacteria. Methods Mol. Biol. 362:155-171. http://dx.doi.org/10.1007/978-1-59745-257-1_11.
21. Monzingo AF, Ozburn A, Xia S, Meyer RJ, Robertus JD. 2007. The structure of the minimal relaxase domain of MobA at 2.1 A resolution. J. Mol. Biol. 366:165-178. http://dx.doi.org/10.1016/j.jmb.2006.11.031.
22. Taton A, Unglaub F, Wright NE, Zeng WY, Paz-Yepes J, Brahamsha B, Palenik B, Peterson TC, Haerizadeh F, Golden SS, Golden JW. 29 July 2014. Broad-host-range vector system for synthetic biology and biotechnology in cyanobacteria. Nucleic Acids Res. http://dx.doi.org/10.1093/nar/gku673.
23. Yoon H, Golden JW. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935-938. http://dx.doi.org/10.1126/science.282.5390.935.
24. Taton A, Lis E, Adin DM, Dong G, Cookson S, Kay SA, Golden SS, Golden JW. 2012. Gene transfer in Leptolyngbya sp. strain BL0902, a cyanobacterium suitable for production of biomass and bioproducts. PLoS One 7(1):e30901. http://dx.doi.org/10.1371/journal.pone.0030901.
25. Elhai J, Vepritskiy A, Muro-Pastor AM, Flores E, Wolk CP. 1997. Reduction of conjugal transfer efficiency by three restriction activities of Anabaena sp. strain PCC 7120. J. Bacteriol. 179:1998-2005.
26. Mutsuda M, Michel KP, Zhang X, Montgomery BL, Golden SS. 2003. Biochemical properties of CikA, an unusual phytochrome-like histidine protein kinase that resets the circadian clock in Synechococcus elongatus PCC 7942. J. Biol. Chem. 278:19102-19110. http://dx.doi.org/10.1074/jbc.M213255200.
27. Cai YP, Wolk CP. 1990. Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J. Bacteriol. 172:3138-3145.
28. Katoh K, Kuma K, Toh H, Miyata T. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33: 511-518. http://dx.doi.org/10.1093/nar/gki198.
29. Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56:564-577. http://dx.doi.org/10.1080/10635150701472164.
30. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704. http://dx.doi.org/10.1080/10635150390235520.
31. Peccia J, Haznedaroglu B, Gutierrez J, Zimmerman JB. 2013. Nitrogen supply is an important driver of sustainable microalgae biofuel production. Trends Biotechnol. 31:134-138. http://dx.doi.org/10.1016/j.tibtech.2013.01.010.
32. Ng WO, Zentella R, Wang Y, Taylor JS, Pakrasi HB. 2000. phrA, the major.sp. strain PCC 6803 codes for a cyclobutane-pyrimidine-dimerspecific DNA photolyase. Arch. Microbiol. 173:412-417. http://dx.doi.org/10.1007/s002030000164.
33. Griese M, Lange C, Soppa J. 2011. Ploidy in cyanobacteria. FEMS Microbiol. Lett. 323:124-131. http://dx.doi.org/10.1111/j.1574-6968.2011.02368.x.
34. Yang Y, Huang XZ, Wang L, Risoul V, Zhang CC, Chen WL. 2013. Phenotypic variation caused by variation in the relative copy number of pDU1-based plasmids expressing the GAF domain of Pkn41 or Pkn42 in Anabaena sp. PCC 7120. Res. Microbiol. 164:127-135. http://dx.doi.org/10.1016/j.resmic.2012.10.010.
35. Ried JL, Collmer A. 1987. An nptI-sacB-sacR cartridge for constructing directed, unmarked mutations in gram-negative bacteria by marker exchange-eviction mutagenesis. Gene 57:239-246. http://dx.doi.org/10.1016/0378-1119(87)90127-2.
36. Weigand JE, Suess B. 2009. Aptamers and riboswitches: perspectives in biotechnology. Appl. Microbiol. Biotechnol. 85:229-236. http://dx.doi.org/10.1007/s00253-009-2194-2.
37. Bocobza SE, Aharoni A. 2008. Switching the light on plant riboswitches. Trends Plant Sci. 13:526-533. http://dx.doi.org/10.1016/j.tplants.2008.07.004.
38. Verhounig A, Karcher D, Bock R. 2010. Inducible gene expression from the plastid genome by a synthetic riboswitch. Proc. Natl. Acad. Sci. U. S. A. 107:6204-6209. http://dx.doi.org/10.1073/pnas.0914423107.
39. Fowler CC, Li Y. 2014. Construction and application of riboswitch-based sensors that detect metabolites within bacterial cells. Methods Mol. Biol. 1103:177-197. http://dx.doi.org/10.1007/978-1-62703-730-3_14.
40. Wittmann A, Suess B. 2012. Engineered riboswitches: expanding researchers' toolbox with synthetic RNA regulators. FEBS Lett. 586:2076-2083. http://dx.doi.org/10.1016/j.febslet.2012.02.038.
41. Lee SK, Chou H, Ham TS, Lee TS, Keasling JD. 2008. Metabolic engineering of microorganisms for biofuels production: from bugs to synthetic biology to fuels. Curr. Opin. Biotechnol. 19:556-563. http://dx.doi.org/10.1016/j.copbio.2008.10.014.
42. Rasala BA, Muto M, Lee PA, Jager M, Cardoso RM, Behnke CA, Kirk P, Hokanson CA, Crea R, Mendez M, Mayfield SP. 2010. Production of therapeutic proteins in algae, analysis of expression of seven human proteins in the chloroplast of Chlamydomonas reinhardtii. Plant Biotechnol. J. 8:719-733. http://dx.doi.org/10.1111/j.1467-7652.2010.00503.x.
43. Kaiser BK, Carleton M, Hickman JW, Miller C, Lawson D, Budde M, Warrener P, Paredes A, Mullapudi S, Navarro P, Cross F, Roberts JM. 2013. Fatty aldehydes in cyanobacteria are a metabolically flexible precursor for a diversity of biofuel products. PLoS One 8(3):e58307. http://dx.doi.org/10.1371/journal.pone.0058307.
44. Oliver JW, Atsumi S. 2014. Metabolic design for cyanobacterial chemical synthesis. Photosynth. Res. 120:249-261. http://dx.doi.org/10.1007/s11120-014-9997-4.