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Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria

Abstract

Plants use a set of light sensors to control their growth and development in response to changes in ambient light. In particular, phytochromes exert their regulatory activity by switching between a biologically inactive red-light-absorbing form (Pr) and an active far-red-light absorbing form (Pfr)1,2. Recently, biochemical and genetic studies have demonstrated the occurrence of phytochrome-like proteins in photosynthetic and non-photosynthetic bacteria3,4,5,6,7—but little is known about their functions. Here we report the discovery of a bacteriophytochrome located downstream from the photosynthesis gene cluster in a Bradyrhizobium strain symbiont of Aeschynomene. The synthesis of the complete photosynthetic apparatus is totally under the control of this bacteriophytochrome. A similar behaviour is observed for the closely related species Rhodopseudomonas palustris, but not for the more distant anoxygenic photosynthetic bacteria of the genus Rhodobacter, Rubrivivax or Rhodospirillum. Unlike other (bacterio)phytochromes, the carboxy-terminal domain of this bacteriophytochrome contains no histidine kinase features. This suggests a light signalling pathway involving direct protein–protein interaction with no phosphorelay cascade. This specific mechanism of regulation may represent an important ecological adaptation to optimize the plant–bacteria interaction.

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Figure 1: Molecular characterization of phytochromes.
Figure 2: In vitro assembly of Bradyrhizobium bacteriophytochrome.
Figure 3: Action spectra for photosystem synthesis.
Figure 4: Effect of illumination on photosynthetic activity and pigmentation.

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References

  1. Quail, P. H. et al. Phytochromes: photosensory perception and signal transduction. Science 268, 675–680 (1995)

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Smith, H. Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407, 585–591 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Kehoe, D. M. & Grossman, A. R. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273, 1409–1412 (1996)

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Hughes, J. et al. A prokaryotic phytochrome. Nature 386, 663 (1997)

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Jiang, Z.-Y. et al. Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes. Science 285, 406–409 (1999)

    Article  CAS  PubMed  Google Scholar 

  6. Davis, S. J., Vener, A. V. & Vierstra, R. D. Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286, 2517–2520 (1999)

    Article  CAS  PubMed  Google Scholar 

  7. Schmitz, O., Katayama, M., Williams, S. B., Kondo, T. & Golden, S. S. CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science 289, 765–768 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Giraud, E., Hannibal, L., Fardoux, J., Verméglio, A. & Dreyfus, B. Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva. Proc. Natl Acad. Sci. USA 97, 14795–14800 (2000)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Muratomo, T., Kohchi, T., Yokota, A., Hwang, I. & Goodman, H. M. The Arabidopsis photomorphogenesis mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11, 335–347 (1999)

    Article  Google Scholar 

  10. Parkinson, J. S. & Kofoid, E. C. Communications modules in bacterial signalling proteins. Annu. Rev. Genet. 26, 71–112 (1992)

    Article  CAS  PubMed  Google Scholar 

  11. Zhulin, I. B., Taylor, B. L. & Dixon, R. PAS domain S-boxes in Archaea, Bacteria and sensors for oxygen and redox. Trends Biochem. Sci. 22, 331–337 (1997)

    Article  CAS  PubMed  Google Scholar 

  12. Taylor, B. L. & Zhulin, I. B. PAS domains: Internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63, 479–506 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Ponnampalam, S. N., Buggy, J. J. & Bauer, C. E. Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light harvesting-II expression in Rhodobacter capsulatus. J. Bacteriol. 177, 2990–2997 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gomelsky, M. & Kaplan, S. Molecular genetic analysis suggesting interaction between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J. Bacteriol. 179, 128–134 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Li, L. & Lagarias, J. C. Phytochrome assembly. J. Biol. Chem. 267, 19204–19210 (1992)

    CAS  PubMed  Google Scholar 

  16. Bhoo, S.-H., Davis, S. J., Walker, J., Karniol, B. & Vierstra, R. D. Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414, 776–779 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Fleischman, D. & Kramer, D. Photosynthetic rhizobia. Biochim. Biophys. Acta 1364, 17–36 (1998)

    Article  CAS  PubMed  Google Scholar 

  18. Clayton, R. K. The induced synthesis of catalase in Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 37, 503–512 (1960)

    Article  CAS  PubMed  Google Scholar 

  19. Kokotek, W. & Lotz, W. Construction of a lacZ-kanamycine–resistance cassette, useful for site-directed mutagenesis and as a promoter probe. Gene 84, 467–471 (1989)

    Article  CAS  PubMed  Google Scholar 

  20. Boivin, C., Camut, S., Malpica, C. A., Truchet, G. & Rosenberg, C. Rhizobium meliloti genes encoding catabolism of trigonelline are induced under symbiotic conditions. Plant Cell. 2, 1157–1170 (1990)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Yurkov, V., Schoepp, B. & Verméglio, A. Photoinduced electron transfer and cytochrome content in obligate aerobic phototrophic bacteria from genera Erythromicrobium, Sandaracinobacter, Erythromonas, Roseococcus and Erythrobacter. Photosynth. Res. 57, 117–128 (1998)

    Article  CAS  Google Scholar 

  22. Quandt, J. & Hynes, M. F. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127, 15–21 (1993)

    Article  CAS  PubMed  Google Scholar 

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Correspondence to André Verméglio.

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Giraud, E., Fardoux, J., Fourrier, N. et al. Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417, 202–205 (2002). https://doi.org/10.1038/417202a

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