Skip to main content

Advertisement

SpringerLink
Log in

Post-translational Modifications of Serine/Threonine and Histidine Kinases and Their Roles in Signal Transductions in Synechocystis Sp. PCC 6803

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Cyanobacterium Synechocystis sp. PCC 6803, a popular model organism for researches in photosynthesis and biofuel production, contains plant-like photosynthetic machineries which significantly contribute to global carbon fixation. There are 12 eukaryotic-type Ser/Thr kinases (SpkA-L) and 49 His kinases (Hik1-49) of two-component systems in the genome of Synechocystis sp. PCC 6803. They are the key regulators in sensing and transmitting stimuli including light- and glucose-mediate signal transduction. Proteomic studies were able to identify all the kinases. The majority of kinases no matter whether they have a predicted transmembrane domain were identified in the membrane fractions. Six Ser/Thr kinases (SpkA-D, F and G) and ten His kinases (Hik4, 12, 14, 21, 26–27, 29, 36, 43, and 46) were identified to have one or more of the three types of post-translational modifications: phosphorylation, acetylation, and thiol oxidation. Interestingly, SpkG has the phosphorylatable threonine residue that was aligned with the phosphorylated threonine residue in the activation loop of human CDK7, demonstrating conserved phosphorylation between cyanobacterial and human kinases. Transcriptomics and proteomics revealed differential expression of the kinases in heterotrophic and photoheterotrophic compared with photoautotrophic conditions, indicating their roles in regulating the growth modes of cyanobacteria. In summary, this review focuses on the discussions on post-transcriptional modifications, transcriptomic, and proteomic studies of Ser/Thr and His kinases. This together with our published review in 2019 present a complete story of an overview of sequences, domain architectures, and biochemical and physiological functions of cyanobacterial kinases with adequate details in the context of high throughput systems. We also emphasize the importance of discovering upstream molecules and substrates to understand the exact functions of the kinases in vivo. As an attempt, a model is proposed in which Hik31, His33, Sll1334, and IcfG are hypothesized to be critical for switching between autotrophic and heterotrophic modes based on the results from the phenotypes of the gene knockout strains combined with their post-translational modifications, and gene expression profiles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. De Marais, D. J. (2000). Evolution. When did photosynthesis emerge on Earth? Science, 289(5485), 1703–1705.

    PubMed  Google Scholar 

  2. Rye, R., & Holland, H. D. (1998). Paleosols and the evolution of atmospheric oxygen: a critical review. American Journal of Science, 298(8), 621–672.

    CAS  PubMed  Google Scholar 

  3. Allen, J. F. (2005). A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Letters, 579(5), 963–968.

    CAS  PubMed  Google Scholar 

  4. Dismukes, G. C., Klimov, V. V., Baranov, S. V., Kozlov, Y. N., DasGupta, J., & Tyryshkin, A. (2001). The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 98(5), 2170–2175.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Paumann, M., Regelsberger, G., Obinger, C., & Peschek, G. A. (2005). The bioenergetic role of dioxygen and the terminal oxidase(s) in cyanobacteria. Biochimica et Biophysica Acta, 1707(2–3), 231–253.

    CAS  PubMed  Google Scholar 

  6. Kolber, Z. S., Van Dover, C. L., Niederman, R. A., & Falkowski, P. G. (2000). Bacterial photosynthesis in surface waters of the open ocean. Nature, 407(6801), 177–179.

    CAS  PubMed  Google Scholar 

  7. Mwaura, F., Koyo, A. O., & Zech, B. (2004). Cyanobacterial blooms and the presence of cyanotoxins in small high altitude tropical headwater reservoirs in Kenya. Journal of Water and Health, 2(1), 49–57.

    CAS  PubMed  Google Scholar 

  8. Lem, N. W., & Glick, B. R. (1985). Biotechnological uses of cyanobacteria. Biotechnology Advances, 3(2), 195–208.

    CAS  PubMed  Google Scholar 

  9. Mekonnen, A. E., Prasanna, R., & Kaushik, B. D. (2002). Cyanobacterial N2 fixation in presence of nitrogen fertilizers. Indian Journal of Experimental Biology, 40(7), 854–857.

    CAS  PubMed  Google Scholar 

  10. Irisarri, P., Gonnet, S., & Monza, J. (2001). Cyanobacteria in Uruguayan rice fields: diversity, nitrogen fixing ability and tolerance to herbicides and combined nitrogen. Journal of Biotechnology, 91(2–3), 95–103.

    CAS  PubMed  Google Scholar 

  11. Dutta, D., De, D., Chaudhuri, S., & Bhattacharya, S. K. (2005). Hydrogen production by cyanobacteria. Microbial Cell Factories, 4(1), 36.

    PubMed  PubMed Central  Google Scholar 

  12. Tsygankov, A. A., Fedorov, A. S., Kosourov, S. N., & Rao, K. K. (2002). Hydrogen production by cyanobacteria in an automated outdoor photobioreactor under aerobic conditions. Biotechnology and Bioengineering, 80(7), 777–783.

    CAS  PubMed  Google Scholar 

  13. Ghirardi, M. L., Posewitz, M. C., Maness, P. C., Dubini, A., Yu, J., & Seibert, M. (2007). Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annual Review of Plant Biology, 58(1), 71–91.

    CAS  PubMed  Google Scholar 

  14. Rupprecht, J., Hankamer, B., Mussgnug, J. H., Ananyev, G., Dismukes, C., & Kruse, O. (2006). Perspectives and advances of biological H2 production in microorganisms. Applied Microbiology and Biotechnology, 72(3), 442–449.

    CAS  PubMed  Google Scholar 

  15. Ducat, D. C., Sachdeva, G., & Silver, P. A. (2012). Rewiring hydrogenase-dependent redox circuits in cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America, 108(10), 3941–3946.

    Google Scholar 

  16. Deng, M. D., & Coleman, J. R. (1999). Ethanol synthesis by genetic engineering in cyanobacteria. Applied and Environmental Microbiology, 65(2), 523–528.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Lan, E. I., & Liao, J. C. (2011). Metabolic engineering of cyanobacteria for 1-butanol production from carbon dioxide. Metabolic Engineering, 13(4), 353–363.

    CAS  PubMed  Google Scholar 

  18. Ungerer, J., Tao, L., Davis, M., Ghirardi, M., Maness, P.-C., & Yu, J. (2012). Sustained photosynthetic conversion of CO2 to ethylene in recombinant cyanobacterium Synechocystis 6803. Energy & Environmental Science, 5(10), 8998–9006.

    CAS  Google Scholar 

  19. Guerrero, F., Carbonell, V., Cossu, M., Correddu, D., & Jones, P. R. (2012). Ethylene synthesis and regulated expression of recombinant protein in Synechocystis sp. PCC 6803. PLoS One, 7(11), e50470.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Eckert, C., Xu, W., Xiong, W., Lynch, S., Ungerer, J., Tao, L., Gill, R., Maness, P.-C., & Yu, J. (2014). Ethylene-forming enzyme and bioethylene production. Biotechnology for Biofuels, 7(33), 11.

    Google Scholar 

  21. Atsumi, S., Higashide, W., & Liao, J. C. (2009). Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nature Biotechnology, 27(12), 1177–1180.

    CAS  PubMed  Google Scholar 

  22. Liu, X., Sheng, J., & Curtiss 3rd, R. (2011). Fatty acid production in genetically modified cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America, 108(17), 6899–6904.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Lindberg, P., Park, S., & Melis, A. (2009). Engineering a platform for photosynthetic isoprene production in cyanobacteria, using Synechocystis as the model organism. Metabolic Engineering, 12(1), 70–79.

    PubMed  Google Scholar 

  24. Corbett, T. H., Valeriote, F. A., Demchik, L., Polin, L., Panchapor, C., Pugh, S., White, K., Knight, J., Jones, J., Jones, L., LoRusso, P., Foster, B., Wiegand, R. A., Lisow, L., Golakoti, T., Heltzel, C. E., Ogino, J., Patterson, G. M., & Moore, R. E. (1996). Preclinical anticancer activity of cryptophycin-8. Journal of Experimental Therapeutics & Oncology, 1(2), 95–108.

    CAS  Google Scholar 

  25. Tan, L. T. (2007). Bioactive natural products from marine cyanobacteria for drug discovery. Phytochemistry, 68(7), 954–979.

    CAS  PubMed  Google Scholar 

  26. Singh, S., Kate, B. N., & Banerjee, U. C. (2005). Bioactive compounds from cyanobacteria and microalgae: an overview. Critical Reviews in Biotechnology, 25(3), 73–95.

    CAS  PubMed  Google Scholar 

  27. Burja, A. M., Banaigs, B., Abou-Mansour, E., Grant Burgess, J., & Wright, P. C. (2001). Marine cyanobacteria--a prolific source of natural products. Tetrahedron, 57(46), 9347–9377.

    CAS  Google Scholar 

  28. Schirmer, A., Rude, M. A., Li, X., Popova, E., & del Cardayre, S. B. (2010). Microbial biosynthesis of alkanes. Science, 329(5991), 559–562.

    CAS  PubMed  Google Scholar 

  29. KlÃhn, S., Baumgartner, D., Pfreundt, U., Voigt, K., Schoen, V., Steglich, C., & Hess, W. R. (2014). Alkane biosynthesis genes in cyanobacteria and their transcriptional organization. Frontiers in Bioengineering and Biotechnology, 2.

  30. Stanier, R. Y. A., & Bazine, G. C. (1977). Phototrophic prokaryotes: the cyanobacteria. Annual Review of Microbiology, 31(1), 225–274.

    CAS  PubMed  Google Scholar 

  31. Kaneko, T., & Tabata, S. (1997). Complete genome structure of the unicellular cyanobacterium Synechocystis sp. PCC6803. Plant & Cell Physiology, 38(11), 1171–1176.

    CAS  Google Scholar 

  32. Vermaas, W. (1996). Molecular genetics of the cyanobacterium Synechocystis sp. PCC 6803: principles and possible biotechnology applications. Journal of Applied Phycology, 8(4), 263–273.

    CAS  Google Scholar 

  33. Mitrophanov, A. Y., & Groisman, E. A. (2008). Signal integration in bacterial two-component regulatory systems. Genes & Development, 22(19), 2601–2611.

    CAS  Google Scholar 

  34. Krell, T., Lacal, J., Busch, A., Silva-Jiménez, H., Guazzaroni, M.-E., & Ramos, J. L. (2010). Bacterial sensor kinases: diversity in the recognition of environmental signals. Annual Review of Microbiology, 64(1), 539–559.

    CAS  PubMed  Google Scholar 

  35. Szurmant, H., White, R. A., & Hoch, J. A. (2007). Sensor complexes regulating two-component signal transduction. Current Opinion in Structural Biology, 17(6), 706–715.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Bhate, M. P., Molnar, K. S., Goulian, M., & DeGrado, W. F. (2015). Signal transduction in histidine kinases: insights from new structures. Structure (London, England : 1993), 23(6), 981–994.

    CAS  Google Scholar 

  37. Kamei, A., Yuasa, T., Geng, X., & Ikeuchi, M. (2002). Biochemical examination of the potential eukaryotic-type protein kinase genes in the complete genome of the unicellular Cyanobacterium Synechocystis sp. PCC 6803. DNA Research, 9(3), 71–78.

    CAS  PubMed  Google Scholar 

  38. Xu, W., & Wang, Y. (2019). Sequences, domain architectures, and biological functions of the serine/threonine and histidine kinases in Synechocystis sp. PCC 6803. Applied Biochemistry and Biotechnology, 188(4), 1022–1065.

    CAS  PubMed  Google Scholar 

  39. Hart, G. W., & Ball, L. E. (2013). Post-translational modifications: a major focus for the future of proteomics. Molecular & Cellular Proteomics, 12(12), 3443.

    CAS  Google Scholar 

  40. Mo, R., Yang, M., Chen, Z., Cheng, Z., Yi, X., Li, C., He, C., Xiong, Q., Chen, H., Wang, Q., & Ge, F. (2015). Acetylome analysis reveals the involvement of lysine acetylation in photosynthesis and carbon metabolism in the model cyanobacterium Synechocystis sp. PCC 6803. Journal of Proteome Research, 14(2), 1275–1286.

    CAS  PubMed  Google Scholar 

  41. Olsen, J. V., & Mann, M. (2013). Status of large-scale analysis of post-translational modifications by mass spectrometry. Molecular & Cellular Proteomics, 12(12), 3444–3452.

    CAS  Google Scholar 

  42. Macek, B., & Mijakovic, I. (2011). Site-specific analysis of bacterial phosphoproteomes. PROTEOMICS, 11(15), 3002–3011.

    CAS  PubMed  Google Scholar 

  43. Spät P, Maček B, Forchhammer K: Phosphoproteome of the cyanobacterium Synechocystis sp. PCC 6803 and its dynamics during nitrogen starvation. Frontiers in Microbiology 2015, 6 :248.

  44. Mikkat, S., Fulda, S., & Hagemann, M. (2014). A 2D gel electrophoresis-based snapshot of the phosphoproteome in the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology, 160(2), 296–306.

    CAS  PubMed  Google Scholar 

  45. Lee, D.-G., Kwon, J., Eom, C.-Y., Kang, Y.-M., Roh, S. W., Lee, K.-B., & Choi, J.-S. (2015). Directed analysis of cyanobacterial membrane phosphoproteome using stained phosphoproteins and titanium-enriched phosphopeptides. Journal of Microbiology, 53(4), 279–287.

    CAS  Google Scholar 

  46. Angeleri, M., Muth-Pawlak, D., Aro, E.-M., & Battchikova, N. (2016). Study of O-phosphorylation sites in proteins involved in photosynthesis-related processes in Synechocystis sp. strain PCC 6803: application of the SRM approach. Journal of Proteome Research, 15(12), 4638–4652.

    CAS  PubMed  Google Scholar 

  47. Yang, M.-k., Z-x, Q., W-y, Z., Xiong, Q., Zhang, J., Li, T., Ge, F., & Zhao, J.-D. (2013). Global phosphoproteomic analysis reveals diverse functions of serine/threonine/tyrosine phosphorylation in the model cyanobacterium Synechococcus sp. strain PCC 7002. Journal of Proteome Research, 12(4), 1909–1923.

    CAS  PubMed  Google Scholar 

  48. Larochelle, S., Chen, J., Knights, R., Pandur, J., Morcillo, P., Erdjument-Bromage, H., Tempst, P., Suter, B., & Fisher, R. P. (2001). T-loop phosphorylation stabilizes the CDK7–cyclin H–MAT1 complex in vivo and regulates its CTD kinase activity. The EMBO Journal, 20(14), 3749–3759.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Lolli, G., Lowe, E. D., Brown, N. R., & Johnson, L. N. (2004). The crystal structure of human CDK7 and its protein recognition properties. Structure (London, England: 1993), 12(11), 2067–2079.

    CAS  Google Scholar 

  50. Xu, W., & Ji, J.-Y. (2011). Dysregulation of CDK8 and Cyclin C in tumorigenesis. Journal of Genetics and Genomics, 38(10), 439–452.

    CAS  PubMed  Google Scholar 

  51. Xu, W., Amire-Brahimi, B., Xie, X.-J., Huang, L., & Ji, J.-Y. (2014). All-atomic molecular dynamic studies of human CDK8: insight into the A-loop, point mutations and binding with its partner CycC. Computational Biology and Chemistry, 51, 1–11.

    PubMed  PubMed Central  Google Scholar 

  52. Zhang, J., Sprung, R., Pei, J., Tan, X., Kim, S., Zhu, H., Liu, C.-F., Grishin, N. V., & Zhao, Y. (2009). Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Molecular & Cellular Proteomics, 8(2), 215–225.

    CAS  Google Scholar 

  53. Buchanan, B. B., & Balmer, Y. (2005). Redox regulation: a broadening horizon. Annual Review of Plant Biology, 56(1), 187–220.

    CAS  PubMed  Google Scholar 

  54. Guo, J., Nguyen, A. Y., Dai, Z., Su, D., Gaffrey, M. J., Moore, R. J., Jacobs, J. M., Monroe, M. E., Smith, R. D., Koppenaal, D. W., Pakrasi, H. B., & Qian, W. J. (2014). Proteome-wide light/dark modulation of thiol oxidation in cyanobacteria revealed by quantitative site-specific redox proteomics. Molecular & Cellular Proteomics, 13(12), 3270–3285.

    CAS  Google Scholar 

  55. Kopf, M., Klähn, S., Scholz, I., Matthiessen, J. K. F., Hess, W. R., & Voß, B. (2014). Comparative analysis of the primary transcriptome of Synechocystis sp. PCC 6803. DNA Research, 21(5), 527–539.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Gao, L., Ge, H., Huang, X., Liu, K., Zhang, Y., Xu, W., & Wang, Y. (2015). Systematically ranking the tightness of membrane association for Peripheral Membrane Proteins (PMPs). Molecular & Cellular Proteomics, 14(2), 340–353.

    CAS  Google Scholar 

  57. Zhang, L.-F., Yang, H.-M., Cui, S.-X., Hu, J., Wang, J., Kuang, T.-Y., Norling, B., & Huang, F. (2009). Proteomic analysis of plasma membranes of cyanobacterium Synechocystis sp. strain PCC 6803 in response to high pH stress. Journal of Proteome Research, 8(6), 2892–2902.

    CAS  PubMed  Google Scholar 

  58. Plohnke, N., Seidel, T., Kahmann, U., Rögner, M., Schneider, D., & Rexroth, S. (2015). The proteome and lipidome of Synechocystis sp. PCC 6803 cells grown under light-activated heterotrophic conditions. Molecular & Cellular Proteomics, 14(3), 572–584.

    CAS  Google Scholar 

  59. Wegener, K. M., Singh, A. K., Jacobs, J. M., Elvitigala, T., Welsh, E. A., Keren, N., Gritsenko, M. A., Ghosh, B. K., Camp, D. G., Smith, R. D., et al. (2010). Global proteomics reveal an atypical strategy for carbon/nitrogen assimilation by a cyanobacterium under diverse environmental perturbations. Molecular & Cellular Proteomics, 9(12), 2678–2689.

    CAS  Google Scholar 

  60. Gao, L., Wang, J., Ge, H., Fang, L., Zhang, Y., Huang, X., & Wang, Y. (2015). Toward the complete proteome of Synechocystis sp. PCC 6803. Photosynthesis Research, 126(2), 203–219.

    CAS  PubMed  Google Scholar 

  61. Fang, L., Ge, H., Huang, X., Liu, Y., Lu, M., Wang, J., Chen, W., Xu, W., & Wang, Y. (2017). Trophic mode-dependent proteomic analysis reveals functional significance of light-independent chlorophyll synthesis in Synechocystis sp. PCC 6803. Molecular Plant, 10(1), 73–85.

    CAS  PubMed  Google Scholar 

  62. Pisareva, T., Kwon, J., Oh, J., Kim, S., Ge, C., Wieslander, Å., Choi, J.-S., & Norling, B. (2011). Model for membrane organization and protein sorting in the cyanobacterium Synechocystis sp. PCC 6803 inferred from proteomics and multivariate sequence analyses. Journal of Proteome Research, 10(8), 3617–3631.

    CAS  PubMed  Google Scholar 

  63. Jers, C., Soufi, B., Grangeasse, C., Deutscher, J., & Mijakovic, I. (2008). Phosphoproteomics in bacteria: towards a systemic understanding of bacterial phosphorylation networks. Expert Review of Proteomics, 5(4), 619–627.

    CAS  PubMed  Google Scholar 

  64. Yoshikawa, K., Hirasawa, T., Ogawa, K., Hidaka, Y., Nakajima, T., Furusawa, C., & Shimizu, H. (2013). Integrated transcriptomic and metabolomic analysis of the central metabolism of Synechocystis sp. PCC 6803 under different trophic conditions. Biotechnology Journal, 8(5), 571–580.

    CAS  PubMed  Google Scholar 

  65. Nagarajan, S., Srivastava, S., & Sherman, L. A. (2014). Essential role of the plasmid hik31 operon in regulating central metabolism in the dark in Synechocystis sp. PCC 6803. Molecular Microbiology, 91(1), 79–97.

    CAS  PubMed  Google Scholar 

  66. Lee, S., Ryu, J.-Y., Kim, S. Y., Jeon, J.-H., Song, J. Y., Cho, H.-T., Choi, S.-B., Choi, D., de Marsac, N. T., & Park, Y.-I. (2007). Transcriptional regulation of the respiratory genes in the cyanobacterium Synechocystis sp. PCC 6803 during the early response to glucose feeding. Plant Physiology, 145(3), 1018–1030.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Kurian, D., Jansèn, T., & Mäenpää, P. (2006). Proteomic analysis of heterotrophy in Synechocystis sp. PCC 6803. PROTEOMICS, 6(5), 1483–1494.

    CAS  PubMed  Google Scholar 

  68. Tabei, Y., Okada, K., & Tsuzuki, M. (2007). Sll1330 controls the expression of glycolytic genes in Synechocystis sp. PCC 6803. Biochemical and Biophysical Research Communications, 355(4), 1045–1050.

    CAS  PubMed  Google Scholar 

  69. Nakajima, T., Kajihata, S., Yoshikawa, K., Matsuda, F., Furusawa, C., Hirasawa, T., & Shimizu, H. (2014). Integrated metabolic flux and omics analysis of Synechocystis sp. PCC 6803 under mixotrophic and photoheterotrophic conditions. Plant & Cell Physiology, 55(9), 1605–1612.

    CAS  Google Scholar 

  70. Ughy, B., & Ajlani, G. (2004). Phycobilisome rod mutants in Synechocystis sp. strain PCC6803. Microbiology, 150(12), 4147–4156.

    CAS  PubMed  Google Scholar 

  71. Ajlani, G., Vernotte, C., DiMagno, L., & Haselkorn, R. (1995). Phycobilisome core mutants of Synechocystis PCC 6803. Biochimica et Biophysica Acta - Biomembranes, 1231(2), 189–196.

    Google Scholar 

  72. Liberton, M., Chrisler, W. B., Nicora, C. D., Moore, R. J., Smith, R. D., Koppenaal, D. W., Pakrasi, H. B., & Jacobs, J. M. (2017). Phycobilisome truncation causes widespread proteome changes in Synechocystis sp. PCC 6803. PLoS One, 12(3), e0173251.

    PubMed  PubMed Central  Google Scholar 

  73. Shi, L., Bischoff, K. M., & Kennelly, P. J. (1999). The icfG gene cluster of Synechocystis sp. strain PCC 6803 encodes an Rsb/Spo-like protein kinase, protein phosphatase, and two phosphoproteins. Journal of Bacteriology, 181(16), 4761–4767.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Kloft, N., & Forchhammer, K. (2005). Signal transduction protein PII phosphatase PphA is required for light-dependent control of nitrate utilization in Synechocystis sp. strain PCC 6803. Journal of Bacteriology, 187(19), 6683–6690.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Laurent, S., Jang, J., Janicki, A., Zhang, C.-C., & Bédu, S. (2008). Inactivation of spkD, encoding a Ser/Thr kinase, affects the pool of the TCA cycle metabolites in Synechocystis sp. strain PCC 6803. Microbiology, 154(7), 2161–2167.

    CAS  PubMed  Google Scholar 

  76. 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 Research, 14(5), 207–216.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The authors thank the support (NSF(2010)-PFUND-217 and LEQSF(2013-16)-RD-A-15) from the US National Science Foundation’s EPSCoR Program and Louisiana RCS Program to W.X..

Author information

Authors and Affiliations

  1. Department of Chemistry, University of Louisiana at Lafayette, Lafayette, LA, 70504, USA

    Wu Xu

  2. State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, No.1 West Beichen Rd, Beijing, 100101, China

    Yingchun Wang

Authors
  1. Wu Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yingchun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wu Xu or Yingchun Wang.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

Supplementary Fig. 1. An amino acid sequence alignment of SpkG of Synechocystis sp. PCC 6803 along with human CDK7 sequence in PDB (PDB ID: 1UA2). Activation loop (A-loop), DFG motif and the conserved threonine are labeled. Supplementary Fig. 2. a, A sequence alignment of SpkA of Synechococcus sp. PCC 7002 and Synechocystis sp. PCC 6803. Two phosphorylation sites are labeled; b, Domain architecture and phosphorylation sites of SpkA of Synechococcus sp. PCC 7002. Supplementary Fig. 3. a, A sequence alignment of A1682 of Synechococcus sp. PCC 7002 with SpkF of Synechocystis sp. PCC 6803. The phosphorylation sites are labeled in green for Synechocystis sp. PCC 6803 and in blue for Synechococcus sp. PCC 7002; b, Domain architecture and phosphorylation sites of A1682 of Synechococcus sp. PCC 7002. Supplementary Fig. 4. a, A sequence alignment of A2735 of Synechococcus sp. PCC 7002 with SpkC of Synechocystis sp. PCC 6803. The phosphorylation sites are labeled in green for Synechocystis sp. PCC 6803 and in blue for Synechococcus sp. PCC 7002; b, Domain architecture and phosphorylation sites of A2735 of Synechococcus sp. PCC 7002. Supplementary Fig. 5. Domain architectures and phosphorylation sites of A1727, A2611 and A1080 of Synechococcus sp. PCC 7002. Supplementary Fig. 6. a, A sequence alignment of A0689 of Synechococcus sp. PCC 7002 with Hik4 of Synechocystis sp. PCC 6803. The phosphorylation sites are labeled in blue for Synechococcus sp. PCC 7002; b, Domain architecture and phosphorylation sites of A0689 of Synechococcus sp. PCC 7002. Supplementary Fig. 7. a, A sequence alignment of A0049 of Synechococcus sp. PCC 7002 with Hik18 of Synechocystis sp. PCC 6803. The phosphorylation sites are labeled in blue for Synechococcus sp. PCC 7002; b, Domain architecture and phosphorylation sites of A0049 of Synechococcus sp. PCC 7002. Supplementary Fig. 8. A sequence alignment of A1639 of Synechococcus sp. PCC 7002 with Hik43 of Synechocystis sp. PCC 6803. The phosphorylation sites are labeled in green for Synechocystis sp. PCC 6803. Supplementary Fig. 9. a, A sequence alignment of A1639 of Synechococcus sp. PCC 7002 with Hik43 of Synechocystis sp. PCC 6803. The phosphorylation sites are labeled in blue for Synechococcus sp. PCC 7002; b, Domain architecture and phosphorylation sites of A1639 of Synechococcus sp. PCC 7002. Supplementary Fig. 10. Domain architectures and phosphorylation sites of A1641, A2365, A0865, A1354 and A2835 of Synechococcus sp. PCC 7002. Supplementary Fig. 11. A sequence alignment of protein kinase domains of Ser/Thr kinases of Synechococcus sp. PCC 7002 with human CDK7 sequence in PDB (PDB ID: 1UA2). Supplementary Fig. 12. Domain architecture, phosphorylation sites and acetylation sites of SpkA and SpkF of Synechocystis sp. PCC 6803. Supplementary Fig. 13. Domain architecture, phosphorylation sites and acetylation sites of Hik4, Hik26, Hik36 and Hik43 of Synechocystis sp. PCC 6803. Supplementary Fig. 14. Thiol oxidation of Hik26 of Synechocystis sp. PCC 6803. a, Domain architecture, acetylation site and oxidation and reduction site; b, Oxidation level of Hik26 at C261 under different growth conditions. Supplementary Fig. 15. a, The number of times of Synechocystis sp. PCC 6803 Ser/Thr kinases with and without predicted transmembrane domains of in membrane or soluble fractions; b, Presence of Spks in heterotrophic and photomixotrophic conditions. Supplementary Fig. 16. a, The number of times of Synechocystis sp. PCC 6803 histidine kinases with and without predicted transmembrane domains of in the membrane or soluble fractions; b, Presence of histidine kinases in the heterotrophic and photomixotrophic conditions. Supplementary Fig. 17. The ratios of kinase gene expression of Synechocystis sp. PCC 6803 under the different growth conditions. Supplementary Fig. 18. An amino acid sequence alignment of Hik31 (chromosomal gene product) and Hik47 (plasmid gene product) of Synechocystis sp. PCC 6803. Supplementary Fig. 19. A pie graph to show the distribution of photosynthesis and respiration related proteins in different groups. Number of proteins identified by mass spectrometry and proteins in cyanobase are indicated. Supplementary Fig. 20. Number of times of kinases identified by mass spectrometry from a total of 60 datasets from literature. a, Ser/Thr kinases; b, His kinases. Supplementary Fig. 21. Bacterial two-component systems. a, A typical His-Asp two-component system including a senor & histidine kinase and a response regulator; b, A His-Asp-His-Asp phosphorelay including a hybrid histidine, a linker often with a Hpt domain and a response regulator. Supplementary Fig. 22. The ratios of kinase protein levels of Synechocystis sp. PCC 6803 under different growth conditions. Average protein expression levels under different growth conditions are labeled with dot lines. Green dot line represents the ratio of photoheterotrophic/autotrophic conditions; Blue dot line represents the ratio of heterotrophic/autotrophic conditions; Red dot line represents the ratio of mixotrophic/autotrophic conditions. Some of the kinases differentially expressed under different growth conditions are labeled. Supplementary Fig. 23. The ratios of Ser/Thr kinase protein levels of Synechocystis sp. PCC 6803 for different truncated phycobilisoms. Average protein expression levels are labeled with dot lines. Blue dot line represents the ratio of the CB mutant/the wild type; Red dot line represents the ratio of the CK mutant/the wild type; Green dot line represents the ratio of the PAL mutant/the wild type. Supplementary Fig. 24. The ratios of histidine kinase protein levels of Synechocystis sp. PCC 6803 for different truncated phycobilisoms. Average protein expression levels are labeled with dot lines. Blue dot line represents the ratio of the CB mutant/the wild type; Red dot line represents the ratio of the CK mutant/the wild type; Green dot line represents the ratio of the PAL mutant/the wild type. The decreasing and increasing trends of the ratios of relative expression levels against the severeness of truncations are labeled with rectangles in pink and in blue respectively. (PDF 516 kb)

ESM 2

(XLSX 716 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, W., Wang, Y. Post-translational Modifications of Serine/Threonine and Histidine Kinases and Their Roles in Signal Transductions in Synechocystis Sp. PCC 6803. Appl Biochem Biotechnol 193, 687–716 (2021). https://doi.org/10.1007/s12010-020-03435-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-020-03435-2

Keywords

Search

Navigation