1887

Abstract

The facultatively photosynthetic bacterium harbours an unusual light, oxygen, voltage (LOV) domain protein, RsLOV. While showing a characteristic photocycle, the protein lacks a C-terminal output domain, similar to PpSB2 in . Oxygen tension and light quantity are the two factors mainly responsible for controlling the expression of photosynthesis genes in . Two photoreceptor proteins are known to be involved in this regulation: the intensively studied AppA protein and the more recently identified cryptochrome-like protein CryB. Here we show by transcriptome and physiological studies that RsLOV is also involved in the regulation of photosynthetic gene expression. Our data further hint at a connection between RsLOV, carbohydrate metabolism and chemotaxis, as well as with the cellular response to photooxidative stress. RsLOV affects not only blue light-dependent gene expression but also redox-dependent regulation.

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2012-02-01
2020-07-11
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References

  1. Anthony J. R., Warczak K. L., Donohue T. J.. ( 2005;). A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis. Proc Natl Acad Sci U S A102:6502–6507 [CrossRef][PubMed]
    [Google Scholar]
  2. Aravind L., Koonin E. V.. ( 2000;). The STAS domain – a link between anion transporters and antisigma-factor antagonists. Curr Biol10:R53–R55 [CrossRef][PubMed]
    [Google Scholar]
  3. Avila-Pérez M., Hellingwerf K. J., Kort R.. ( 2006;). Blue light activates the σ-dependent stress response of Bacillus subtilis via YtvA. J Bacteriol188:6411–6414 [CrossRef][PubMed]
    [Google Scholar]
  4. Avila-Pérez M., Vreede J., Tang Y., Bende O., Losi A., Gärtner W., Hellingwerf K. J.. ( 2009;). In vivo mutational analysis of YtvA from Bacillus subtilis: mechanism of light activation of the general stress response. J Biol Chem284:24958–24964 [CrossRef][PubMed]
    [Google Scholar]
  5. Beck B. J., Downs D. M.. ( 1998;). The apbE gene encodes a lipoprotein involved in thiamine synthesis in Salmonella typhimurium. J Bacteriol180:885–891[PubMed]
    [Google Scholar]
  6. Boyd D. A., Thevenot T., Gumbmann M., Honeyman A. L., Hamilton I. R.. ( 2000;). Identification of the operon for the sorbitol (glucitol) phosphoenolpyruvate: sugar phosphotransferase system in Streptococcus mutans. Infect Immun68:925–930 [CrossRef][PubMed]
    [Google Scholar]
  7. Braatsch S., Klug G.. ( 2004;). Blue light perception in bacteria. Photosynth Res79:45–57 [CrossRef][PubMed]
    [Google Scholar]
  8. Braatsch S., Gomelsky M., Kuphal S., Klug G.. ( 2002;). A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol Microbiol45:827–836 [CrossRef][PubMed]
    [Google Scholar]
  9. Briggs W. R.. ( 2007;). The LOV domain: a chromophore module servicing multiple photoreceptors. J Biomed Sci14:499–504 [CrossRef][PubMed]
    [Google Scholar]
  10. Briggs W. R., Christie J. M.. ( 2002;). Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci7:204–210 [CrossRef][PubMed]
    [Google Scholar]
  11. Crosson S., Rajagopal S., Moffat K.. ( 2003;). The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry42:2–10 [CrossRef][PubMed]
    [Google Scholar]
  12. Dandanell G., Norris K., Hammer K.. ( 1991;). Long-distance deoR regulation of gene expression in Escherichia coli. Ann N Y Acad Sci646:19–30 [CrossRef][PubMed]
    [Google Scholar]
  13. Drews G.. ( 1983;). Mikrobiologisches Praktikum Heidelberg: Springer Verlag; [CrossRef]
    [Google Scholar]
  14. Eraso J. M., Roh J. H., Zeng X., Callister S. J., Lipton M. S., Kaplan S.. ( 2008;). Role of the global transcriptional regulator PrrA in Rhodobacter sphaeroides 2.4.1: combined transcriptome and proteome analysis. J Bacteriol190:4831–4848 [CrossRef][PubMed]
    [Google Scholar]
  15. Glaeser J., Klug G.. ( 2005;). Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology151:1927–1938 [CrossRef][PubMed]
    [Google Scholar]
  16. Glaeser J., Zobawa M., Lottspeich F., Klug G.. ( 2007;). Protein synthesis patterns reveal a complex regulatory response to singlet oxygen in Rhodobacter. J Proteome Res6:2460–2471 [CrossRef][PubMed]
    [Google Scholar]
  17. Gomelsky M., Kaplan S.. ( 1995;). appA, a novel gene encoding a trans-acting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol177:4609–4618[PubMed]
    [Google Scholar]
  18. Gomelsky M., Kaplan S.. ( 1997;). Molecular genetic analysis suggesting interactions between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol179:128–134[PubMed]
    [Google Scholar]
  19. Gomelsky M., Klug G.. ( 2002;). BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem Sci27:497–500 [CrossRef][PubMed]
    [Google Scholar]
  20. Gomelsky M., Horne I. M., Lee H. J., Pemberton J. M., McEwan A. G., Kaplan S.. ( 2000;). Domain structure, oligomeric state, and mutational analysis of PpsR, the Rhodobacter sphaeroides repressor of photosystem gene expression. J Bacteriol182:2253–2261 [CrossRef][PubMed]
    [Google Scholar]
  21. Gomelsky L., Sram J., Moskvin O. V., Horne I. M., Dodd H. N., Pemberton J. M., McEwan A. G., Kaplan S., Gomelsky M.. ( 2003;). Identification and in vivo characterization of PpaA, a regulator of photosystem formation in Rhodobacter sphaeroides. Microbiology149:377–388 [CrossRef][PubMed]
    [Google Scholar]
  22. Han Y., Meyer M. H., Keusgen M., Klug G.. ( 2007;). A haem cofactor is required for redox and light signalling by the AppA protein of Rhodobacter sphaeroides. Mol Microbiol64:1090–1104 [CrossRef][PubMed]
    [Google Scholar]
  23. Happ H. N., Braatsch S., Broschek V., Osterloh L., Klug G.. ( 2005;). Light-dependent regulation of photosynthesis genes in Rhodobacter sphaeroides 2.4.1 is coordinately controlled by photosynthetic electron transport via the PrrBA two-component system and the photoreceptor AppA. Mol Microbiol58:903–914 [CrossRef][PubMed]
    [Google Scholar]
  24. Haydon D. J., Guest J. R.. ( 1991;). A new family of bacterial regulatory proteins. FEMS Microbiol Lett63:291–295 [CrossRef][PubMed]
    [Google Scholar]
  25. Hendrischk A. K., Braatsch S., Glaeser J., Klug G.. ( 2007;). The phrA gene of Rhodobacter sphaeroides encodes a photolyase and is regulated by singlet oxygen and peroxide in a σE-dependent manner. Microbiology153:1842–1851 [CrossRef][PubMed]
    [Google Scholar]
  26. Hendrischk A. K., Frühwirth S. W., Moldt J., Pokorny R., Metz S., Kaiser G., Jäger A., Batschauer A., Klug G.. ( 2009a;). A cryptochrome-like protein is involved in the regulation of photosynthesis genes in Rhodobacter sphaeroides. Mol Microbiol74:990–1003 [CrossRef][PubMed]
    [Google Scholar]
  27. Hendrischk A. K., Moldt J., Frühwirth S. W., Klug G.. ( 2009b;). Characterization of an unusual LOV domain protein in the α-proteobacterium Rhodobacter sphaeroides. Photochem Photobiol85:1254–1259 [CrossRef][PubMed]
    [Google Scholar]
  28. Hübner P., Willison J. C., Vignais P. M., Bickle T. A.. ( 1991;). Expression of regulatory nif genes in Rhodobacter capsulatus. J Bacteriol173:2993–2999[PubMed]
    [Google Scholar]
  29. Hübner P., Masepohl B., Klipp W., Bickle T. A.. ( 1993;). nif gene expression studies in Rhodobacter capsulatus: ntrC-independent repression by high ammonium concentrations. Mol Microbiol10:123–132 [CrossRef][PubMed]
    [Google Scholar]
  30. Hunter C. N., Tucker J. D., Niederman R. A.. ( 2005;). The assembly and organisation of photosynthetic membranes in Rhodobacter sphaeroides. Photochem Photobiol Sci4:1023–1027 [CrossRef][PubMed]
    [Google Scholar]
  31. Janzon L., Lofdahl S., Arvidson S.. ( 1986;). Evidence for a coordinate transcriptional control of alpha-toxin and protein-A synthesis in Staphylococcus aureus. FEMS Microbiol Lett33:193–198 [CrossRef]
    [Google Scholar]
  32. Klug G., Masuda S.. ( 2009;). Regulation of genes by light. The Purple Phototrophic Bacteria727–741 Thurnauer M. C.. Dordrecht: Springer; [CrossRef]
    [Google Scholar]
  33. Krauss U., Losi A., Gärtner W., Jaeger K. E., Eggert T.. ( 2005;). Initial characterization of a blue-light sensing, phototropin-related protein from Pseudomonas putida: a paradigm for an extended LOV construct. Phys Chem Chem Phys7:2804–2811 [CrossRef][PubMed]
    [Google Scholar]
  34. Losi A.. ( 2007;). Flavin-based blue-light photosensors: a photobiophysics update. Photochem Photobiol83:1283–1300 [CrossRef][PubMed]
    [Google Scholar]
  35. Losi A., Gärtner W.. ( 2008;). Bacterial bilin- and flavin-binding photoreceptors. Photochem Photobiol Sci7:1168–1178 [CrossRef][PubMed]
    [Google Scholar]
  36. Losi A., Polverini E., Quest B., Gärtner W.. ( 2002;). First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys J82:2627–2634 [CrossRef][PubMed]
    [Google Scholar]
  37. Masuda S., Bauer C. E.. ( 2002;). AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell110:613–623 [CrossRef][PubMed]
    [Google Scholar]
  38. Missiakas D., Mayer M. P., Lemaire M., Georgopoulos C., Raina S.. ( 1997;). Modulation of the Escherichia coli σE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol Microbiol24:355–371 [CrossRef][PubMed]
    [Google Scholar]
  39. Moskvin O. V., Gomelsky L., Gomelsky M.. ( 2005;). Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development. J Bacteriol187:2148–2156 [CrossRef][PubMed]
    [Google Scholar]
  40. Newman J. D., Falkowski M. J., Schilke B. A., Anthony L. C., Donohue T. J.. ( 1999;). The Rhodobacter sphaeroides ECF sigma factor, σE, and the target promoters cycA P3 and rpoE P1. J Mol Biol294:307–320 [CrossRef][PubMed]
    [Google Scholar]
  41. Nuss A. M., Glaeser J., Klug G.. ( 2009;). RpoHII activates oxidative-stress defense systems and is controlled by RpoE in the singlet oxygen-dependent response in Rhodobacter sphaeroides. J Bacteriol191:220–230 [CrossRef][PubMed]
    [Google Scholar]
  42. Oliveros J. C.. ( 2007;). venny. An interactive tool for comparing lists with Venn diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html
  43. Pappas C. T., Sram J., Moskvin O. V., Ivanov P. S., Mackenzie R. C., Choudhary M., Land M. L., Larimer F. W., Kaplan S., Gomelsky M.. ( 2004;). Construction and validation of the Rhodobacter sphaeroides 2.4.1 DNA microarray: transcriptome flexibility at diverse growth modes. J Bacteriol186:4748–4758 [CrossRef][PubMed]
    [Google Scholar]
  44. Peña-Sánchez J., Poggio S., Flores-Pérez U., Osorio A., Domenzain C., Dreyfus G., Camarena L.. ( 2009;). Identification of the binding site of the σ54 hetero-oligomeric FleQ/FleT activator in the flagellar promoters of Rhodobacter sphaeroides. Microbiology155:1669–1679 [CrossRef][PubMed]
    [Google Scholar]
  45. Peuser V., Metz S., Klug G.. ( 2011;). Response of the photosynthetic bacterium Rhodobacter sphaeroides to iron limitation and role of a Fur ortholog in this response. Environ Microbiol Rep3:397–404 [CrossRef]
    [Google Scholar]
  46. Pfaffl M. W.. ( 2001;). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res29:e45 [CrossRef][PubMed]
    [Google Scholar]
  47. Plumbridge J.. ( 1995;). Co-ordinated regulation of amino sugar biosynthesis and degradation: the NagC repressor acts as both an activator and a repressor for the transcription of the glmUS operon and requires two separated NagC binding sites. EMBO J14:3958–3965[PubMed]
    [Google Scholar]
  48. Plumbridge J.. ( 2001;). DNA binding sites for the Mlc and NagC proteins: regulation of nagE, encoding the N-acetylglucosamine-specific transporter in Escherichia coli. Nucleic Acids Res29:506–514 [CrossRef][PubMed]
    [Google Scholar]
  49. Pollich M., Klug G.. ( 1995;). Identification and sequence analysis of genes involved in late steps in cobalamin (vitamin B12) synthesis in Rhodobacter capsulatus. J Bacteriol177:4481–4487[PubMed]
    [Google Scholar]
  50. Pollich M., Wersig C., Klug G.. ( 1996;). The bluF gene of Rhodobacter capsulatus is involved in conversion of cobinamide to cobalamin (vitamin B12). J Bacteriol178:7308–7310[PubMed]
    [Google Scholar]
  51. Prentki P., Krisch H. M.. ( 1984;). In vitro insertional mutagenesis with a selectable DNA fragment. Gene29:303–313 [CrossRef][PubMed]
    [Google Scholar]
  52. Purcell E. B., Crosson S.. ( 2008;). Photoregulation in prokaryotes. Curr Opin Microbiol11:168–178 [CrossRef][PubMed]
    [Google Scholar]
  53. Purcell E. B., Siegal-Gaskins D., Rawling D. C., Fiebig A., Crosson S.. ( 2007;). A photosensory two-component system regulates bacterial cell attachment. Proc Natl Acad Sci U S A104:18241–18246 [CrossRef][PubMed]
    [Google Scholar]
  54. Purcell E. B., McDonald C. A., Palfey B. A., Crosson S.. ( 2010;). An analysis of the solution structure and signaling mechanism of LovK, a sensor histidine kinase integrating light and redox signals. Biochemistry49:6761–6770 [CrossRef][PubMed]
    [Google Scholar]
  55. Ritchie M. E., Silver J., Oshlack A., Holmes M., Diyagama D., Holloway A., Smyth G. K.. ( 2007;). A comparison of background correction methods for two-colour microarrays. Bioinformatics23:2700–2707 [CrossRef][PubMed]
    [Google Scholar]
  56. Schilke B. A., Donohue T. J.. ( 1995;). ChrR positively regulates transcription of the Rhodobacter sphaeroides cytochrome c2 gene. J Bacteriol177:1929–1937[PubMed]
    [Google Scholar]
  57. Schwerdtfeger C., Linden H.. ( 2003;). VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J22:4846–4855 [CrossRef][PubMed]
    [Google Scholar]
  58. Simon R., Priefer U., Pühler A.. ( 1983;). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Nat Biotechnol1:784–791 [CrossRef]
    [Google Scholar]
  59. Smyth G. K.. ( 2005;). Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor397–420 Huber W.. New York: Springer; [CrossRef]
    [Google Scholar]
  60. Smyth G. K., Speed T.. ( 2003;). Normalization of cDNA microarray data. Methods31:265–273 [CrossRef][PubMed]
    [Google Scholar]
  61. Spudich J. L.. ( 2006;). The multitalented microbial sensory rhodopsins. Trends Microbiol14:480–487 [CrossRef][PubMed]
    [Google Scholar]
  62. Swartz T. E., Tseng T. S., Frederickson M. A., Paris G., Comerci D. J., Rajashekara G., Kim J. G., Mudgett M. B., Splitter G. A.. & other authors ( 2007;). Blue-light-activated histidine kinases: two-component sensors in bacteria. Science317:1090–1093 [CrossRef][PubMed]
    [Google Scholar]
  63. Tarutina M., Ryjenkov D. A., Gomelsky M.. ( 2006;). An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J Biol Chem281:34751–34758 [CrossRef][PubMed]
    [Google Scholar]
  64. Taylor B. L., Zhulin I. B.. ( 1999;). PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev63:479–506[PubMed]
    [Google Scholar]
  65. van Aalten D. M., DiRusso C. C., Knudsen J., Wierenga R. K.. ( 2000;). Crystal structure of FadR, a fatty acid-responsive transcription factor with a novel acyl coenzyme A-binding fold. EMBO J19:5167–5177 [CrossRef][PubMed]
    [Google Scholar]
  66. von Gabain A., Belasco J. G., Schottel J. L., Chang A. C., Cohen S. N.. ( 1983;). Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc Natl Acad Sci U S A80:653–657 [CrossRef][PubMed]
    [Google Scholar]
  67. Zeller T., Moskvin O. V., Li K., Klug G., Gomelsky M.. ( 2005;). Transcriptome and physiological responses to hydrogen peroxide of the facultatively phototrophic bacterium Rhodobacter sphaeroides. J Bacteriol187:7232–7242 [CrossRef][PubMed]
    [Google Scholar]
  68. Zoltowski B. D., Crane B. R.. ( 2008;). Light activation of the LOV protein Vivid generates a rapidly exchanging dimer. Biochemistry47:7012–7019 [CrossRef][PubMed]
    [Google Scholar]
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