1887

Abstract

Ethylene is a gaseous signal sensed by plants and bacteria. Heterologous expression of the ethylene-forming enzyme (EFE) from Pseudomonas syringae in cyanobacteria leads to the production of ethylene under photoautotrophic conditions. The recent characterization of an ethylene-responsive signalling pathway affecting phototaxis in the cyanobacterium Synechocystis sp. PCC 6803 implied that biotechnologically relevant ethylene synthesis may induce regulatory processes that are not related to changes in metabolism. Here, we provide data that indicate that endogenously produced ethylene accelerates the movement of cells towards light. Microarray analysis demonstrates that ethylene mainly deactivates transcription from the csiR1/lsiR promoter, which is under the control of the two-component system consisting of the ethylene- and UV-A-sensing histidine kinase UirS and the DNA-binding response regulator UirR. Surprisingly, ethylene production triggers a very specific transcriptional response and only a few other smaller transcriptional changes are detected in the microarray analysis.

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2017-11-01
2019-10-22
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References

  1. Savakis P, Hellingwerf KJ. Engineering cyanobacteria for direct biofuel production from CO2. Curr Opin Biotechnol 2015;33:8–14 [CrossRef][PubMed]
    [Google Scholar]
  2. Eckert C, Xu W, Xiong W, Lynch S, Ungerer J et al. Ethylene-forming enzyme and bioethylene production. Biotechnol Biofuels 2014;7:33 [CrossRef][PubMed]
    [Google Scholar]
  3. Ungerer J, Tao L, Davis M, Ghirardi M, Maness P-C et al. Sustained photosynthetic conversion of CO2 to ethylene in recombinant cyanobacterium Synechocystis 6803. Energy Environ Sci 2012;5:8998 [CrossRef]
    [Google Scholar]
  4. Zavřel T, Knoop H, Steuer R, Jones PR, Červený J et al. A quantitative evaluation of ethylene production in the recombinant cyanobacterium Synechocystis sp. PCC 6803 harboring the ethylene-forming enzyme by membrane inlet mass spectrometry. Bioresour Technol 2016;202:142–151 [CrossRef][PubMed]
    [Google Scholar]
  5. Veetil VP, Angermayr SA, Hellingwerf KJ. Ethylene production with engineered Synechocystis sp. PCC 6803 strains. Microb Cell Fact 2017;16:34 [CrossRef][PubMed]
    [Google Scholar]
  6. Guerrero F, Carbonell V, Cossu M, Correddu D, Jones PR. Ethylene synthesis and regulated expression of recombinant protein in Synechocystis sp. PCC 6803. PLoS One 2012;7:e50470 [CrossRef][PubMed]
    [Google Scholar]
  7. Mo H, Xie X, Zhu T, Lu X. Effects of global transcription factor NtcA on photosynthetic production of ethylene in recombinant Synechocystis sp. PCC 6803. Biotechnol Biofuels 2017;10:145 [CrossRef][PubMed]
    [Google Scholar]
  8. McManus MT. The Plant Hormone Ethylenevol. 44 UK: Wiley-Blackwell; 2012; pp.1–416
    [Google Scholar]
  9. Huang T-C, Chow T-J. Ethylene production by blue-green algae. Bot Bull Acad Sin 1984;25:81–86
    [Google Scholar]
  10. Le Henry M, Charton M, Alignan M, Maury P, Luniov A et al. Ethylene stimulates growth and affects fatty acid content of Synechocystis sp. PCC 6803. Algal Res 2017;26:234–239 [CrossRef]
    [Google Scholar]
  11. Mount SM, Chang C. Evidence for a plastid origin of plant ethylene receptor genes. Plant Physiol 2002;130:10–14 [CrossRef][PubMed]
    [Google Scholar]
  12. Wang W, Esch JJ, Shiu SH, Agula H, Binder BM et al. Identification of important regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor of Arabidopsis. Plant Cell 2006;18:3429–3442 [CrossRef][PubMed]
    [Google Scholar]
  13. Lacey RF, Binder BM. Ethylene regulates the physiology of the cyanobacterium Synechocystis sp. PCC 6803 via an ethylene receptor. Plant Physiol 2016;171:2798–2809 [CrossRef][PubMed]
    [Google Scholar]
  14. Song JY, Cho HS, Cho JI, Jeon JS, Lagarias JC et al. Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 2011;108:10780–10785 [CrossRef][PubMed]
    [Google Scholar]
  15. Ramakrishnan P, Tabor JJ. Repurposing Synechocystis PCC6803 UirS-UirR as a UV-violet/green photoreversible transcriptional regulatory tool in E. coli. ACS Synth Biol 2016;5:733–740 [CrossRef][PubMed]
    [Google Scholar]
  16. Jakob A, Schuergers N, Wilde A. Phototaxis assays of Synechocystis sp. PCC 6803 at macroscopic and microscopic scales. Bio Protoc 2017;7: [CrossRef]
    [Google Scholar]
  17. Zinchenko VV, Piven V, Melnik VA, Shestakov SV. Vectors for the complementation analysis of cyanobacterial mutants. Russ J Genet 1999;35:228–232
    [Google Scholar]
  18. Black TA, Cai Y, Wolk CP. Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol Microbiol 1993;9:77–84 [CrossRef][PubMed]
    [Google Scholar]
  19. Trautmann D, Voss B, Wilde A, Al-Babili S, Hess WR. Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803. DNA Res 2012;19:435–448 [CrossRef][PubMed]
    [Google Scholar]
  20. Pinto FL, Thapper A, Sontheim W, Lindblad P. Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria. BMC Mol Biol 2009;10:79 [CrossRef][PubMed]
    [Google Scholar]
  21. Georg J, Dienst D, Schürgers N, Wallner T, Kopp D et al. The small regulatory RNA SyR1/PsrR1 controls photosynthetic functions in cyanobacteria. Plant Cell 2014;26:3661–3679 [CrossRef][PubMed]
    [Google Scholar]
  22. Georg J, Voss B, Scholz I, Mitschke J, Wilde A et al. Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Mol Syst Biol 2009;5:305 [CrossRef][PubMed]
    [Google Scholar]
  23. Kopf M, Klähn S, Scholz I, Matthiessen JK, Hess WR et al. Comparative analysis of the primary transcriptome of Synechocystis sp. PCC 6803. DNA Res 2014;21:527–539 [CrossRef][PubMed]
    [Google Scholar]
  24. Kopf M, Hess WR. Regulatory RNAs in photosynthetic cyanobacteria. FEMS Microbiol Rev 2015;39:301–315 [CrossRef][PubMed]
    [Google Scholar]
  25. Davis KM, Isberg RR. Defining heterogeneity within bacterial populations via single cell approaches. Bioessays 2016;38:782–790 [CrossRef][PubMed]
    [Google Scholar]
  26. Klähn S, Schaal C, Georg J, Baumgartner D, Knippen G et al. The sRNA NsiR4 is involved in nitrogen assimilation control in cyanobacteria by targeting glutamine synthetase inactivating factor IF7. Proc Natl Acad Sci USA 2015;112:E6243E6252 [CrossRef][PubMed]
    [Google Scholar]
  27. Kim H-E, Shitashiro M, Kuroda A, Takiguchi N, Kato J. Ethylene chemotaxis in Pseudomonas aeruginosa and other Pseudomonas species. Microbes Environ 2007;22:186–189 [CrossRef]
    [Google Scholar]
  28. Ohkawa H, Hashimoto N, Furukawa S, Kadono T, Kawano T. Forced symbiosis between Synechocystis spp. PCC 6803 and apo-symbiotic Paramecium bursaria as an experimental model for evolutionary emergence of primitive photosynthetic eukaryotes. Plant Signal Behav 2011;6:773–776 [CrossRef][PubMed]
    [Google Scholar]
  29. David C, Bühler K, Schmid A. Stabilization of single species Synechocystis biofilms by cultivation under segmented flow. J Ind Microbiol Biotechnol 2015;42:1083–1089 [CrossRef][PubMed]
    [Google Scholar]
  30. Schuergers N, Mullineaux CW, Wilde A. Cyanobacteria in motion. Curr Opin Plant Biol 2017;37:109–115 [CrossRef][PubMed]
    [Google Scholar]
  31. Mitschke J, Georg J, Scholz I, Sharma CM, Dienst D et al. An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci USA 2011;108:2124–2129 [CrossRef][PubMed]
    [Google Scholar]
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