SpringerLink
Log in

Coexisting properties of thermostability and ultraviolet radiation resistance in the main S-layer complex of Deinococcus radiodurans

  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Deinococcus radiodurans is well known for its unusual resistance to different environmental stresses. Recently, we have described a novel complex composed of the surface (S)-layer protein DR_2577 and the carotenoid deinoxanthin. We also showed a role of this complex in the UV resistance under desiccation. Both these properties, UV and desiccation resistance, suggest a selective pressure generated by Sun irradiation. In order to confirm this hypothesis we checked whether this S-layer Deinoxanthin Binding Complex (SDBC) has features of thermo-resistance, a property also expected in proteins evolved under solar irradiative pressure. We performed the spectroscopic characterization of the SDBC by means of thermal shift assay, circular dichroism and related in silico analysis. Our findings identify a stability typical of thermo-adapted proteins and provide a new insight into the origin of specific S-layer types. The results are discussed in terms of co-evolutionary mechanisms related to Sun-induced desiccation and heat.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. W. Baumeister, F. Karrenberg, R. Rachel, A. Engel, B. Heggeler and W. O. Saxton, The major cell envelope protein of Micrococcus radiodurans (R1). Structural and chemical characterization, Eur. J. Biochem., 1982, 125, 535–544.

    Article  CAS  PubMed  Google Scholar 

  2. D. Farci, C. Slavov, E. Tramontano and D. Piano, The S-layer protein DR_2577 binds the carotenoid deinoxanthin and under desiccation conditions protect against UV- radiation in Deinococcus radiodurans, Front. Microbiol., 2016, 7, 155.

    Article  PubMed  PubMed Central  Google Scholar 

  3. D. Farci, M. W. Bowler, F. Esposito, S. McSweeney, E. Tramontano and D. Piano, Purification and characteriz- ation of DR_2577 (SlpA) a major S-layer protein from Deinococcus radiodurans, Front. Microbiol., 2015, 6, 414.

    PubMed  Google Scholar 

  4. V. Mattimore and J. R. Battista, Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation, J. Bacteriol., 1996, 178, 633–637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. M. X. Ruiz-González, G. Á. Czirják, P. Genevaux, A. P. Moller, T. A. Mousseau and P. Heeb, Resistance of Feather-Associated Bacteria to Intermediate Levels of Ionizing Radiation near Chernobyl, Sci. Rep., 2016, 6, 22969.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. M. Wassmann, R. Moeller, G. Reitz and P. Rettberg, Adaptation of Bacillus subtilis cells to Archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance, Astrobiology, 2010, 10, 605–615.

    Article  CAS  PubMed  Google Scholar 

  7. K. Harada, M. Moriwaki and S. Oda, Arrhenius plot ana- lysis of the mechanism of the thermotolerance induction in the radioresistant bacterium Deinococcus radiodurans, J. Gen. Appl. Microbiol., 1988, 34, 209–212.

    Article  Google Scholar 

  8. Y. Liu, J. Zhou, M. V. Omelchenko, A. S. Beliaev, A. Venkateswaran, J. Stair, L. Wu, D. K. Thompson, D. Xu, I. B. Rogozin, E. K. Gaidamakova, M. Zhai, K. S. Makarova, E. V. Koonin and M. J. Daly, Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation, Proc. Natl. Acad. Sci. U. S. A., 2003, 100, 4191–4196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. A. Airo, S. L. Chan, Z. Martinez, M. O. Platt and J. D. Trent, Heat shock and cold shock in Deinococcus radiodurans, Cell Biochem. Biophys., 2004, 40, 277–288.

    Article  CAS  PubMed  Google Scholar 

  10. D. Asker, T. Beppu and K. Ueda, Unique diversity of caro- tenoid-producing bacteria isolated from Misasa, a radio- active site in Japan, Appl. Microbiol. Biotechnol., 2007, 77, 383–392.

    Article  CAS  PubMed  Google Scholar 

  11. J. R. Battista, Against all odds: the survival strategies of Deinococcus radiodurans, Annu. Rev. Microbiol., 1997, 51, 203.

    Article  CAS  PubMed  Google Scholar 

  12. M. M. Mathews and N. I. Krisky, The relationship between carotenoid pigments and resistance to radiation in non- photosynthetic bacteria, Photochem. Photobiol., 1965, 4, 813–817.

    Article  CAS  PubMed  Google Scholar 

  13. W. Stahl and H. Sies, Carotenoids and protection against solar UV radiation, Skin Pharmacol. Appl. Skin Physiol., 2002, 15, 291–296.

    Article  CAS  PubMed  Google Scholar 

  14. H. Sies and W. Stahl, Carotenoids and UV protection, Photochem. Photobiol. Sci., 2004, 3, 749–752.

    Article  CAS  PubMed  Google Scholar 

  15. W. Stahl and H. Sies, β-Carotene and other carotenoids in protection from sunlight, Am. J. Clin. Nutr., 2012, 96, 1179S–1184S.

    Article  CAS  PubMed  Google Scholar 

  16. B. Tian and Y. Hua, Carotenoid biosynthesis in extremophi- lic Deinococcus-Thermus bacteria, Trends Microbiol., 2010, 18, 512–520.

    Article  CAS  PubMed  Google Scholar 

  17. A. Krisko and M. Radman, Biology of extreme radiation re- sistance: they way of Deinococcus radiodurans, Cold Spring Harbor Perspect. Biol., 2013, 5, a012765.

    Article  CAS  Google Scholar 

  18. F. Peng, L. Zhang, X. Luo, J. Dai, H. An, Y. Tang and C. Fang, Deinococcus xinjiangensis sp. nov., isolated from desert soil, Int.J. Syst. Evol. Microbiol., 2009, 59, 709–713.

    Article  CAS  PubMed  Google Scholar 

  19. Y. Yang, T. Itoh, S. Yokobori, S. Itahashi, H. Shimada, K. Satoh, H. Ohba, I. Narumi and A. Yamagishi, Deinococcus aerius sp. nov., isolated from the high atmo- sphere, Int.J. Syst. Evol. Microbiol., 2009, 59, 1862–1866.

    Article  CAS  PubMed  Google Scholar 

  20. H. Bouraoui, M. B. Aissa, F. Abbassi, J. P. Touzel, M. O’donohue and M. Manai, Characterization of Deinococcus sahariens sp. nov., a radiation-resistant bacter- ium isolated from a Saharan hot spring, Arch. Microbiol., 2012, 194, 315–322.

    Article  CAS  PubMed  Google Scholar 

  21. R. G. E. Murray, The family Deinococcaceae. The Prokaryotes, Springer, New York, 1992, pp. 3732–3744.

    Book  Google Scholar 

  22. D. Farci, M. W. Bowler, J. Kirkpatrick, S. McSweeney, E. Tramontano and D. Piano, New features of the cell wall of the radio-resistant bacterium Deinococcus radiodurans, Biochim. Biophys. Acta, 2014, 1838, 1978–1984.

    Article  CAS  PubMed  Google Scholar 

  23. N. Poklar and G. Vesnaver, Thermal denaturation of proteins studied by UV spectroscopy, J. Chem. Educ., 2000, 77, 380.

    Article  Google Scholar 

  24. A. Micsonai, F. Wien, L. Kernya, Y. H. Lee, Y. Goto, M. Réfrégiers and J. Kardos, Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy, Proc. Natl. Acad. Sci. U. S. A., 2015, 112, E3095–103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. R. Apweiler, A. Bairoch and C. H. Wu, Protein sequence databases, Curr. Opin. Chem. Biol., 2004, 8, 76–80.

    Article  CAS  PubMed  Google Scholar 

  26. E. Gasteiger, C. Hoogland, A. Gattiker, S. Duvaud, M. R. Wilkins, R. D. Appel and A. Bairoch, Protein Identification and Analysis Tools on the ExPASy Server, in The Proteomics Protocols Handbook, ed. J. M. Walker, Humana Press, 2005, pp. 571–607.

    Chapter  Google Scholar 

  27. H. Rothfuss, J. C. Lara, A. K. Schmid and M. E. Lidstrom, Involvement of the S-layer proteins HPI and SlpA in the maintenance of cell envelope integrity in Deinococcus radio- durans, R1, Microbiology, 2006, 152, 2779–2787.

    Article  CAS  PubMed  Google Scholar 

  28. B. Folch, Y. Dehouck and M. Rooman, Thermo- and mesostabilizing protein interactions identified by tempera- ture-dependent statistical potentials, Biophys. J., 2010, 98, 667–677.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. L. Lemee, E. Peuchant, M. Clerc, M. Brunner and H. Pfander, Deinoxanthin: A new carotenoid isolated from Deinococcus radiodurans, Tetrahedron, 1997, 53, 919–926.

    Article  CAS  Google Scholar 

  30. N. E. Gentner and R. E. Mitchel, Ionizing radiation- induced release of a cell surface nuclease from Micrococcus radiodurans, Radiat. Res., 1975, 61, 204–215.

    Article  CAS  PubMed  Google Scholar 

  31. S. Karlin and J. Mrazek, Predicted highly expressed and putative alien genes of Deinococcus radiodurans and impli- cations for resistance to ionizing radiation damage, Proc. Natl. Acad. Sci. U. S. A., 2001, 98, 5240–5245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. L. Zhang, Q. Yang, X. Luo, C. Fang, Q. Zhang and Y. Tang, Knockout of crtB or crtI gene blocks the carotenoid biosyn- thetic pathway in Deinococcus radiodurans R1 and influ- ences its resistance to oxidative DNA-damaging agents due to change of free radicals scavenging ability, Arch. Microbiol., 2007, 188, 411–419.

    Article  CAS  PubMed  Google Scholar 

  33. C. S. Cockell, The ultra-violate radiation environment of Earth and Mars: past and present, in Astrobiology: The Quest for the Conditions of Life, ed. G. Horneck and C. Baumstark-Khan, Springer-Verlag, Berlin, 2002, pp. 219–232.

    Chapter  Google Scholar 

  34. C. E. Blank, Evolutionary timing of the origins of meso- philis sulphate reduction and oxygenic photosynthesis: a phylogenomic dating approach, Geobiology, 2004, 2, 1–20.

    Article  CAS  Google Scholar 

  35. C. E. Blank, Not so old Archaea - the antiquity of biogeo- chemical processes in the archael domain of life, Geobiology, 2009, 7, 495–514.

    Article  CAS  PubMed  Google Scholar 

  36. E. G. Nisbet and N. H. Sleep, The habitat and nature of early life, Nature, 2001, 409, 1083–1091.

    Article  CAS  PubMed  Google Scholar 

  37. J. H. Cleaves and S. L. Miller, Oceanic protection of prebio- tic organic compounds from UV radiation, Proc. Natl. Acad. Sci. U. S. A., 1998, 95, 7260–7263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. E. D. Brodie and B. J. Ridenhour, Reciprocal selection at the phenotypic interface of coevolution, Integr. Comp. Biol., 2003, 43, 408–418.

    Article  PubMed  Google Scholar 

  39. T. Held, A. Nourmohammad and M. Lässig, Adaptive evol- ution of molecular phenotypes, J. Stat. Mech.: Theory Exp., 2014, P09029.

    Google Scholar 

  40. A. Anderson, H. Nordon, R. Cain, G. Parrish and D. Duggan, Studies on a radio-resistant Micrococcus. I. (1956). Isolation, morphology, cultural characteristics, and resistance to gamma radiation, Food Technol., 1956, 10, 575.

    Google Scholar 

  41. D. E. Duggan, A. W. Anderson, P. R. Elliker and R. F. Cain, Ultraviolet exposure studies on a gamma radiation-resistant micrococcus isolated from food, Food Res., 1959, 24, 376–382.

    Article  Google Scholar 

  42. J. R. Battista, A. M. Earl and M. J. Park, Why is Deinococcus radiodurans so resistant to ionizing radiation?, Trends Microbiol., 1999, 7, 362–365.

    Article  CAS  PubMed  Google Scholar 

  43. M. M. Cox and J. R. Battista, Deinococcus radiodurans - the consummate survivor, Nat. Rev. Microbiol., 2005, 3, 882–892.

    Article  CAS  PubMed  Google Scholar 

  44. J. K. Fredrickson, S. M. Li, E. K. Gaidamakova, V. Y. Matrosova, M. Zhai, H. M. Sulloway, J. C. Scholten, M. G. Brown, D. L. Balkwill and M. J. Daly, Protein oxi- dation: key to bacterial desiccation resistance?, ISME J., 2008, 2, 393–403.

    Article  CAS  PubMed  Google Scholar 

  45. D. Slade and M. Radman, Oxidative stress resistance in Deinococcus radiodurans, Microbiol. Mol. Biol. Rev., 2011, 75, 133–191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. A. D. Das and H. Misra, Hypothetical proteins present during recovery phase of radiation resistant bacterium Deinococcus radiodurans are under purifying selection, J. Mol. Evol., 2013, 77, 31–42.

    Article  CAS  PubMed  Google Scholar 

  47. A. Szilágyi and P. Závodszky, Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey, Structure, 2000, 8, 493–504.

    Article  PubMed  Google Scholar 

  48. S. Ngarize, H. Herman, A. Adams and N. Howell, Comparison of changes in the secondary structure of unheated, heated, and high-pressure-treated beta-lacto- globulin and ovalbumin using fourier transform raman spectroscopy and self-deconvolution, J. Agric. Food Chem., 2004, 52, 6470–6477.

    Article  CAS  PubMed  Google Scholar 

  49. U. Opitz, R. Rudolph, R. Jaenicke, L. Ericsson and H. Neurath, Proteolytic Dimers of Porcine Muscle Lactate Dehydrogenase: Characterization, Folding, and Reconstitution of the Truncated and Nicked Polypeptide Chain, Biochem, 1987, 26, 1399–1406.

    Article  CAS  Google Scholar 

  50. M. Kohlhoff, A. Dahm and R. Hensel, Tetrameric triose- phosphate isomerase from hyperthermophilic Archaea, FEBS Lett., 1996, 383, 245–250.

    Article  CAS  PubMed  Google Scholar 

  51. V. Villeret, B. Clantin, C. Tricot, C. Legrain, M. Roovers, V. Stalon, N. Glansdorff and J. van Beeumen, The crystal structure of Pyrococcus furiosus ornithine carbamoyltrans- ferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures, Proc. Natl. Acad. Sci. U. S. A., 1998, 95, 2801–2806.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. X. C. Abrevaya, I. G. Paulino-Lima, D. Galante, F. Rodrigues, P. J. Mauas, E. Cortón and A. Lage Cde, Comparative survival analysis of Deinococcus radiodurans and the haloarchaea Natrialba magadii and Haloferax volca- nii exposed to vacuum ultraviolet irradiation, Astrobiology, 2011, 11, 1034–1040.

    Article  CAS  PubMed  Google Scholar 

  53. K. Zerulla and J. Soppa, Polyploidy in haloarchaea: advantages for growth and survival, Front. Microbiol., 2014, 5, 274.

    Article  PubMed  PubMed Central  Google Scholar 

  54. J. Soppa, Polyploidy in archaea and bacteria: about desicca- tion resistance, giant cell size, long-term survival, enforce- ment by eukaryotic host and additional aspects, J. Mol. Microbiol. Biotechnol., 2014, 24, 409–419.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

DP is grateful to the European Synchrotron Research Facility and the Partnership for Structural Biology (Grenoble, France) for preliminary studies. The ΔDR_2577 strain was kindly provided by Professor Mary E. Lidstrom (University of Washington, Seattle, USA). DF gratefully acknowledges the support from the L’Oréal-UNESCO Fellowship for Women in Science 2017, Italy (L’Oréal Italia Per le Donne e la Scienza). The authors acknowledge the reviewers for the helpful comments and suggestions.

Author information

Authors and Affiliations

  1. Department of Life and Environmental Sciences, Laboratory of Plant Physiology and Photobiology, University of Cagliari, V.le S. Ignazio da Laconi 13, 09123, Cagliari, Italy

    Domenica Farci & Dario Piano

  2. Institute of Physical and Theoretical Chemistry, Goethe University, Max von Laue-Straße 7, D-60438, Frankfurt am Main, Germany

    Chavdar Slavov

Authors
  1. Domenica Farci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chavdar Slavov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dario Piano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Domenica Farci or Dario Piano.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farci, D., Slavov, C. & Piano, D. Coexisting properties of thermostability and ultraviolet radiation resistance in the main S-layer complex of Deinococcus radiodurans. Photochem Photobiol Sci 17, 81–88 (2018). https://doi.org/10.1039/c7pp00240h

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c7pp00240h

Search

Navigation