Small antisense RNA RblR positively regulates RuBisCo in synechocystis sp. PCC 6803

Frontiers in Microbiology

Volumn 8, Issue FEB, 2017, Pages

  Hu, Jinlu ^a   Li, Tianpei ^b,c   Xu, Wen ^d   Zhan, Jiao ^b   Chen, Hui ^b   He, Chenliu ^b   Wang, Qiang ^b  

^a NORTHWESTERN POLYTECHNICAL UNIVERSITY   (China)

^b INSTITUTE OF HYDROBIOLOGY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

RbcL; RblR; RuBisCo; SRNA; Synechocystis sp. PCC 6803

Indexed keywords

COMPLEMENTARY RNA; RIBULOSEBISPHOSPHATE CARBOXYLASE; TRANSCRIPTOME;

ARTICLE; BASE PAIRING; CARBON FIXATION; CONTROLLED STUDY; DNA LIBRARY; FLUORESCENCE ANALYSIS; GENE EXPRESSION; GROWTH CURVE; IMMUNOBLOTTING; MUTAGENESIS; NONHUMAN; NORTHERN BLOTTING; PHOTOSYNTHESIS; PROTEIN GEL BLOT ANALYSIS; RBCL GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA GENE; SEQUENCE ANALYSIS; SYNECHOCYSTIS SP. PCC 6803;

EID: 85014479684     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00231     Document Type: Article

References (63)

1. Argaman, L., Hershberg, R., Vogel, J., Bejerano, G., Wagner, E. G. H., Margalit, H., et al. (2001). Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol. 11, 941-950. doi: 10.1016/S0960-9822(01)00270-6.
2. Axmann, I. M., Kensche, P., Vogel, J., Kohl, S., Herzel, H., and Hess, W. R. (2005). Identification of cyanobacterial non-coding RNAs by comparative genome analysis. Genome Biol. 6:R73. doi: 10.1186/gb-2005-6-9-r73.
3. Backofen, R., and Hess, W. R. (2010). Computational prediction of sRNAs and their targets in bacteria. RNA Biol. 7, 33-42. doi: 10.4161/rna.7.1.10655.
4. 2-concentrating mechanisms in algae. Can. J. Bot. 76, 1052-1071. doi: 10.1139/b98-074.
5. Bassham, J. A., and Krause, G. H. (1969). Free energy changes and metabolic regulation in steady-state photosynthetic carbon reduction. Biochim. Biophys. Acta 189, 207-221. doi: 10.1016/0005-2728(69)90048-6.
6. Berg, J. M., Tymoczko, J. L., and Stryer, L. (2012). "The Calvin cycle and the pentose phosphate pathway," in Biochemistry, ed W. H. Freeman (New York, NY: W. H. Freeman and Company), 609-635.
7. Billis, K., Billini, M., Tripp, H. J., Kyrpides, N. C., and Mavromatis, K. (2014). Comparative transcriptomics between Synechococcus PCC 7942 and Synechocystis PCC 6803 provide insights into mechanisms of stress acclimation. PLoS ONE 9:e109738. doi: 10.1371/journal.pone.0109738.
8. 2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397-406. doi: 10.1007/BF00392238.
9. Coppins, R. L., Hall, K. B., and Groisman, E. A. (2007). The intricate world of riboswitches. Curr. Opin. Microbiol. 10, 176-181. doi: 10.1016/j.mib.2007.03.006.
10. Demmig-Adams, B., and Adams Iii, W. (1992). Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Biol. 43, 599-626. doi: 10.1146/annurev.pp.43.060192.003123.
11. Dühring, U., Axmann, I. M., Hess, W. R., and Wilde, A. (2006). An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc. Natl. Acad. Sci. U.S.A. 103, 7054-7058. doi: 10.1073/pnas.0600927103.
12. Ehretsmann, C. P., Carpousis, A. J., and Krisch, H. M. (1992). Specificity of Escherichia coli endoribonuclease RNase E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Gene Dev. 6, 149-159. doi: 10.1101/gad.6.1.149.
13. Eisenhut, M., Georg, J., Klähn, S., Sakurai, I., Mustila, H., Zhang, P., et al. (2012). The antisense RNA As1_flv4 in the cyanobacterium Synechocystis sp. PCC 6803 prevents premature expression of the flv4-2 operon upon shift in inorganic carbon supply. J. Biol. Chem. 287, 33153-33162. doi: 10.1074/jbc.M112.391755.
14. 2 assimilation in leaves of C3 species. Planta 149, 78-90. doi: 10.1007/BF00386231.
15. Feller, U., Anders, I., and Mae, T. (2008). Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J. Exp. Bot. 59, 1615-1624. doi: 10.1093/jxb/erm242.
16. Furbank, R. T., Chitty, J. A., Von Caemmerer, S., and Jenkins, C. (1996). Antisense RNA inhibition of rbcS gene expression reduces rubisco level and photosynthesis in the C4 plant Flaveria bidentis. Plant Physiol. 111, 725-734. doi: 10.1104/pp.111.3.725.
17. Georg, J., Dienst, D., Schürgers, N., Wallner, T., Kopp, D., Stazic, D., et al. (2014). The small regulatory RNA SyR1/PsrR1 controls photosynthetic functions in cyanobacteria. Plant Cell 26, 3661-3679. doi: 10.1105/tpc.114.129767.
18. Georg, J., and Hess, W. R. (2011). Cis-Antisense RNA, another level of gene regulation in bacteria. Microbiol. Mol. Biol. Rev. 75, 286-300. doi: 10.1128/MMBR.00032-10.
19. Georg, J., Voss, B., Scholz, I., Mitschke, J., Wilde, A., and Hess, W. R. (2009). Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Mol. Syst. Biol. 5:305. doi: 10.1038/msb.2009.63.
20. Gierga, G., Voss, B., and Hess, W. R. (2012). Non-coding RNAs in marine Synechococcus and their regulation under environmentally relevant stress conditions. ISME J. 6, 1544-1557. doi: 10.1038/ismej.2011.215.
21. Golden, S. S., Brusslan, J., and Haselkorn, R. (1987). Genetic engineering of the cyanobacterial chromosome. Methods Enzymol. 153, 215-231. doi: 10.1016/0076-6879(87)53055-5.
22. Gottesman, S., and Storz, G. (2011). Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb. Perspect. Biol. 3, 1-16. doi: 10.1101/cshperspect.a003798.
23. Hihara, Y., Kamei, A., Kanehisa, M., Kaplan, A., and Ikeuchi, M. (2001). DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13, 793-806. doi: 10.1105/tpc.13.4.793.
24. Hu, J., Deng, X., Shao, N., Wang, G., and Huang, K. (2014). Rapid construction and screening of artificial microRNA systems in Chlamydomonas reinhardtii. Plant J. 79, 1052-1064. doi: 10.1111/tpj.12606.
25. Huttenhofer, A., Schattner, P., and Polacek, N. (2005). Non-coding RNAs: hope or hype? Trends Genet. 21, 289-297. doi: 10.1016/j.tig.2005.03.007.
26. Hüttenhofer, A., and Vogel, J. (2006). Experimental approaches to identify non-coding RNAs. Nucleic Acids Res. 34, 635-646. doi: 10.1093/nar/gkj469.
27. Ionescu, D., Voss, B., Oren, A., Hess, W. R., and Muro-Pastor, A. M. (2010). Heterocyst-specific transcription of NsiR1, a non-coding RNA encoded in a tandem array of direct repeats in cyanobacteria. J. Mol. Biol. 398, 177-188. doi: 10.1016/j.jmb.2010.03.010.
28. Kaberdin, V. R., Miczak, A., Jakobsen, J. S., Lin-Chao, S., McDowall, K. J., and von Gabain, A. (1998). The endoribonucleolytic N-terminal half of Escherichia coli RNase E is evolutionarily conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly. Proc. Natl. Acad. Sci. U.S.A. 95, 11637-11642. doi: 10.1073/pnas.95.20.11637.
29. Kawano, M., Aravind, L., and Storz, G. (2007). An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol. Microbiol. 64, 738-754. doi: 10.1111/j.1365-2958.2007.05688.x.
30. Kopf, M., and Hess, W. R. (2015). Regulatory RNAs in photosynthetic cyanobacteria. FEMS Microbiol. Rev. 39, 301-315. doi: 10.1093/femsre/fuv017.
31. Kopf, M., Klähn, S., Scholz, I., Matthiessen, J. K., Hess, W. R., and Voss, B. (2014). Comparative analysis of the primary transcriptome of Synechocystis sp. PCC 6803. DNA Res. 21, 527-539. doi: 10.1093/dnares/dsu018.
32. Lee, E. J., and Groisman, E. A. (2010). An antisense RNA that governs the expression kinetics of a multifunctional virulence gene. Mol. Microbiol. 76, 1020-1033. doi: 10.1111/j.1365-2958.2010.07161.x.
33. Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760. doi: 10.1093/bioinformatics/btp324.
34. Li, L., Huang, D., Cheung, M. K., Nong, W., Huang, Q., and Kwan, H. S. (2013). BSRD: a repository for bacterial small regulatory RNA. Nucleic Acids Res. 41, D233-D238. doi: 10.1093/nar/gks1264.
35. Liu, J. M., Livny, J., Lawrence, M. S., Kimball, M. D., Waldor, M. K., and Camilli, A. (2009). Experimental discovery of sRNAs in Vibrio cholerae by direct cloning, 5S/tRNA depletion and parallel sequencing. Nucleic Acids Res. 37, e46-e46. doi: 10.1093/nar/gkp080.
36. Luo, S., Ishida, H., Makino, A., and Mae, T. (2002). Fe2+-catalyzed site-specific cleavage of the large subunit of ribulose 1, 5-bisphosphate carboxylase close to the active site. J. Biol. Chem. 277, 12382-12387. doi: 10.1074/jbc.M111072200.
37. Marcus, Y., Altman-Gueta, H., Wolff, Y., and Gurevitz, M. (2011). Rubisco mutagenesis provides new insight into limitations on photosynthesis and growth in Synechocystis PCC6803. J. Exp. Bot. 62, 4173-4182. doi: 10.1093/jxb/err116.
38. Mehta, P., Goyal, S., and Wingreen, N. S. (2008). A quantitative comparison of sRNA-based and protein-based gene regulation. Mol. Syst. Biol. 4:221. doi: 10.1038/msb.2008.58.
39. Mitschke, J., Georg, J., Scholz, I., Sharma, C. M., Dienst, D., Bantscheff, J., et al. (2011a). An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc. Natl. Acad. Sci. U.S.A. 108, 2124-2129. doi: 10.1073/pnas.1015154108.
40. Mitschke, J., Vioque, A., Haas, F., Hess, W. R., and Muro-Pastor, A. M. (2011b). Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc. Natl. Acad. Sci. U.S.A. 108, 20130-20135. doi: 10.1073/pnas.1112724108.
41. Opdyke, J. A., Fozo, E. M., Hemm, M. R., and Storz, G. (2011). RNase III participates in GadY-dependent cleavage of the gadX-gadW mRNA. J. Mol. Biol. 406, 29-43. doi: 10.1016/j.jmb.2010.12.009.
42. Park, S.-Y., Cromie, M. J., Lee, E.-J., and Groisman, E. A. (2010). A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 142, 737-748. doi: 10.1016/j.cell.2010.07.046.
43. Pfreundt, U., Kopf, M., Belkin, N., Berman-Frank, I., and Hess, W. R. (2014). The primary transcriptome of the marine diazotroph Trichodesmium erythraeum IMS101. Sci. Rep. 4:6187. doi: 10.1038/srep06187.
44. Phok, K., Moisan, A., Rinaldi, D., Brucato, N., Carpousis, A. J., Gaspin, C., et al. (2011). Identification of CRISPR and riboswitch related RNAs among novel noncoding RNAs of the euryarchaeon Pyrococcus abyssi. BMC Genomics 12:312. doi: 10.1186/1471-2164-12-312.
45. Raghavan, R., Sloan, D. B., and Ochman, H. (2012). Antisense transcription is pervasive but rarely conserved in enteric bacteria. MBio 3, e00156-12. doi: 10.1128/mBio.00156-12.
46. Ramesh, A., Wakeman, C. A., and Winkler, W. C. (2011). Insights into metalloregulation by M-box riboswitch RNAs via structural analysis of manganese-bound complexes. J. Mol. Biol. 407, 556-570. doi: 10.1016/j.jmb.2011.01.049.
47. Romby, P., Vandenesch, F., and Wagner, E. G. (2006). The role of RNAs in the regulation of virulence-gene expression. Curr. Opin. Microbiol. 9, 229-236. doi: 10.1016/j.mib.2006.02.005.
48. Sakurai, I., Stazic, D., Eisenhut, M., Vuorio, E., Steglich, C., Hess, W. R., et al. (2012). Positive regulation of psbA gene expression by cis-encoded antisense RNAs in Synechocystis sp. PCC 6803. Plant Physiol. 160, 1000-1010. doi: 10.1104/pp.112.
49. Schopf, J. W. (1993). Microfossils of the early archean apex chert: new evidence of the antiquity of life. Science 260, 640-646. doi: 10.1126/science.260.5108.640.
50. Sharma, C. M., Hoffmann, S., Darfeuille, F., Reignier, J., Findeiß, S., Sittka, A., et al. (2010). The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464, 250-255. doi: 10.1038/nature08756.
51. Shimoni, Y., Friedlander, G., Hetzroni, G., Niv, G., Altuvia, S., Biham, O., et al. (2007). Regulation of gene expression by small non-coding RNAs: a quantitative view. Mol. Syst. Biol. 3:138. doi: 10.1038/msb4100181.
52. Smith, A. M., Fuchs, R. T., Grundy, F. J., and Henkin, T. (2010). Riboswitch RNAs: regulation of gene expression by direct monitoring of a physiological signal. RNA Biol. 7, 104-110. doi: 10.4161/rna.7.1.10757.
53. Spreitzer, R. J., and Salvucci, M. E. (2002). Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu. Rev. Plant Biol. 53, 449-475. doi: 10.1146/annurev.arplant.53.100301.135233.
54. Stazic, D., Lindell, D., and Steglich, C. (2011). Antisense RNA protects mRNA from RNase E degradation by RNA-RNA duplex formation during phage infection. Nucleic Acids Res. 39, 4890-4899. doi: 10.1093/nar/gkr037.
55. Steglich, C., Futschik, M. E., Lindell, D., Voss, B., Chisholm, S. W., and Hess, W. R. (2008). The challenge of regulation in a minimal photoautotroph: non-coding RNAs in Prochlorococcus. PLoS Genet. 4:e1000173. doi: 10.1371/journal.pgen.1000173.
56. Storz, G. (2002). An expanding universe of noncoding RNAs. Science 296, 1260-1263. doi: 10.1126/science.1072249.
57. Storz, G., Opdyke, J. A., and Zhang, A. (2004). Controlling mRNA stability and translation with small, noncoding RNAs. Curr. Opin. Microbiol. 7, 140-144. doi: 10.1016/j.mib.2004.02.015.
58. Voigt, K., Sharma, C. M., Mitschke, J., Lambrecht, S. J., Voss, B., Hess, W. R., et al. (2014). Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity. ISME J. 8, 2056-2068. doi: 10.1038/ismej.2014.57.
59. Volpe, T. A., Kidner, C., Hall, I. M., Teng, G., Grewal, S. I., and Martienssen, R. A. (2002). Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833-1837. doi: 10.1126/science.1074973.
60. Voss, B., Georg, J., Schön, V., Ude, S., and Hess, W. R. (2009). Biocomputational prediction of non-coding RNAs in model cyanobacteria. BMC Genomics 10:123. doi: 10.1186/1471-2164-10-123.
61. Waldbauer, J. R., Rodrigue, S., Coleman, M. L., and Chisholm, S. W. (2012). Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle. PLoS ONE 7:e43432. doi: 10.1371/journal.pone.0043432.
62. Wen, Y., Feng, J., Scott, D. R., Marcus, E. A., and Sachs, G. (2011). A cis-encoded antisense amall RNA regulated by the HP0165-HP0166 two-component system controls expression of ureB in Helicobacter pylori. J. Bacteriol. 193, 40-51. doi: 10.1128/jb.00800-10.
63. Xu, W., Chen, H., He, C.-L., and Wang, Q. (2014). Deep sequencing-based identification of small regulatory RNAs in Synechocystis sp. PCC 6803. PLoS ONE 9:e92711. doi: 10.1371/journal.pone.0092711.