Skip to main content
Log in

UV Radiation and Visible Light Induce hsp70 Gene Expression in the Antarctic Psychrophilic Ciliate Euplotes focardii

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The psychrophilic ciliate Euplotes focardii inhabits the shallow marine coastal sediments of Antarctica, where, over millions of years of evolution, it has reached a strict molecular adaptation to such a constant-temperature environment (about −2 °C). This long evolution at sub-zero temperatures has made E. focardii unable to respond to heat stress with the activation of its heat shock protein (hsp) 70 genes. These genes can, however, be expressed in response to other stresses, like the oxidative one, thus indicating that the molecular adaptation has exclusively altered the heat stress signaling pathways, while it has preserved hsp70 gene activation in response to other environmental stressors. Since radiative stress has proved to be affine to oxidative stress in several organisms, we investigated the capability of UV radiation to induce hsp70 transcription. E. focardii cell cultures were exposed to several different irradiation regimes, ranging from visible only to a mixture of visible, UV-A and UV-B. The irradiation values of each spectral band have been set to be comparable with those recorded in a typical Antarctic spring. Using Northern blot analysis, we measured the expression level of hsp70 immediately after irradiation (0-h-labeled samples), 1 h, and 2 h from the end of the irradiation. Surprisingly, our results showed that besides UV radiation, the visible light was also able to induce hsp70 expression in E. focardii. Moreover, spectrophotometric measurements have revealed no detectable endogenous pigments in E. focardii, making it difficult to propose a possible explanation for the visible light induction of its hsp70 genes. Further research is needed to conclusively clarify this point.

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

Access this article

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

Similar content being viewed by others

References

  1. Malloy KD, Holman MA, Mitchell D, Detrich HW III (1997) Solar UVB-induced DNA damage and photoenzymatic DNA repair in Antarctic zooplankton. Proc Natl Acad Sci U S A 94(4):1258–1263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Acevedo J, Nolan C (eds) (1993) Environmental UV radiation: causes — effects — consequences. Commission of the European Communities, Directorate-General XII for Science, Research and Development, Environment Programme, Brussels

  3. Caldwell MM, Björn LO, Bornman JF, Flint SD, Kulandaivelu G, Teramura AH, Tevini M (1998) Effects of increased solar ultraviolet radiation on terrestrial ecosystems. J Photochem Photobiol B Biol 46:40–52

    Article  CAS  Google Scholar 

  4. Kennedy AD (1995) Antarctic terrestrial ecosystem response to global environmental change. Annu Rev Ecol Syst 26:683–704

    Article  Google Scholar 

  5. Karsten U (2008) Defense strategies of algae and cyanobacteria against solar ultraviolet radiation. In: Amsler DC (ed) Algal chemical ecology. Springer, Berlin, pp 273–296

    Chapter  Google Scholar 

  6. Agustí A (2008) The impact of increased ultraviolet radiation on the polar oceans. In: Duarte CM (ed) Impacts of global warming on polar ecosystems. Fundación BBVA, Bilbao, pp 25–45

    Google Scholar 

  7. Llabrés M, Agustí S (2010) Effects of ultraviolet radiation on growth, cell death and the standing stock of Antarctic phytoplankton. Aquat Microb Ecol 59:151–160

    Article  Google Scholar 

  8. Häder DP, Helbling EW, Williamson CE, Worrest RC (2011) Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 10(2):242–60

    Article  PubMed  Google Scholar 

  9. Hansson L-A, Hylander S (2009) Effects of ultraviolet radiation on pigmentation, photoenzymatic repair, behavior, and community ecology of zooplankton. Photochem Photobiol Sci 8:1266–1275

    Article  CAS  PubMed  Google Scholar 

  10. Thomas DN, Dieckmann GS (2002) Antarctic sea ice—a habitat for extremophiles. Science 295:641–644

    Article  CAS  PubMed  Google Scholar 

  11. Whitley D, Goldberg SP, Jordan WD (1999) Heat shock proteins: a review of the molecular chaperones. J Vasc Surg 29(4):748–751

    Article  CAS  PubMed  Google Scholar 

  12. Sarkar S, Singh DM, Yadav R, Arunkumar KP, Pittman GW (2011) Heat shock proteins: molecules with assorted functions. Front Biol 6:312–327

    CAS  Google Scholar 

  13. La Terza A, Barchetta S, Buonanno F, Ballarini P, Miceli C (2008) The protozoan ciliate Tetrahymena thermophila as biosensor of sublethal levels of toxicants in the soil. Fresenius Environ Bull 17:1144–1150

    Google Scholar 

  14. Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in drosophila. Experientia 18:571–573

    Article  CAS  Google Scholar 

  15. Clark MS, Peck LS (2009) HSP70 heat shock proteins and environmental stress in Antarctic marine organisms: a mini-review. Mar Genomics 2:11–18

    Article  PubMed  Google Scholar 

  16. Pirkkala L, Nykänen P, Sistonen L (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15:1118–1131

    Article  CAS  PubMed  Google Scholar 

  17. Bosch TCG, Krylow SM, Bode HR, Steele RE (1988) Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. Proc Natl Acad Sci U S A 85:7927–7931

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Brennecke T, Gellner K, Bosch TC (1998) The lack of a stress response in Hydra oligactis is due to reduced hsp70 mRNA stability. Eur J Biochem 255:703–709

    Article  CAS  PubMed  Google Scholar 

  19. Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN (2000) Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (family Nototheniidae). J Exp Biol 203:2331–2339

    CAS  PubMed  Google Scholar 

  20. La Terza A, Papa G, Miceli G, Luporini P (2001) Divergence between two Antarctic species of the ciliate Euplotes, E. focardii and E. nobilii, in the expression of heat shock protein 70 genes. Mol Ecol 10:1061–1067

    Article  PubMed  Google Scholar 

  21. Valbonesi A, Luporini P (1993) Biology of Euplotes focardii, an Antarctic ciliate. Polar Biol 13:489–493

    Article  Google Scholar 

  22. Pucciarelli S, Ballarini P, Miceli C (1997) Cold-adapted microtubules: characterization of tubulin posttranslational modifications in the antarctic ciliate Euplotes focardii. Cell Motil Cytoskeleton 38:329–340

    Article  CAS  PubMed  Google Scholar 

  23. Pucciarelli S, Miceli C (2002) Characterization of the cold-adapted a-tubulin from the psychrophilic ciliate Euplotes focardii. Extremophiles 6:385–389

    Article  CAS  PubMed  Google Scholar 

  24. La Terza A, Miceli C, Luporini P (2004) The gene for the heat-shock protein 70 of Euplotes focardii, an Antarctic psychrophilic ciliate. Antarct Sci 16(1):23–28

    Article  Google Scholar 

  25. Di Giuseppe G, Cervia D, Vallesi A (2012) Divergences in the responses to ultraviolet radiation between polar and non-polar ciliated protozoa. Microb Ecol 63:634–638

    Article  Google Scholar 

  26. Booth CR, Lucas TB, Morrow JH, Weiler CS, Penhale PA (1994) The United States National Science Foundation’s Polar Network for monitoring ultraviolet radiation. In: Weiler CS, Penhale PA (eds) Ultraviolet radiation in Antarctica: measurements and biological effects, Antarct. Res. Ser. vol. 62. AGU, Washington, pp 17–37

    Chapter  Google Scholar 

  27. Sambrook J, Fritsch EF, Maniatis T (eds) (1989) Molecular cloning—a laboratory manual, 2nd edn. New York, Cold Spring Habour Laboratory Press

    Google Scholar 

  28. Feinberg AP, Vogelstein B (1984) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137(1):266–267

    Article  CAS  PubMed  Google Scholar 

  29. La Terza A, Miceli C, Luporini P (2007) Adaptive evolution of the heat-shock response in the Antarctic psychrophilic ciliate, Euplotes focardii: hints from a comparative determination of the hsp70 gene structure. Antarct Sci 16(2):239–244

    Article  Google Scholar 

  30. Fernandes M, Xiao H, Lis JT (1994) Fine structure analyses of the Drosophila and Saccharomyces heat shock factor—heat shock element interactions. Nucl Acids Res 22:167–173

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Kobayashi N, McEntee K (1993) Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol 13:248–256

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Ruis H, Schüller C (1995) Stress signaling in yeast. BioEssays 17:959–965

    Article  CAS  PubMed  Google Scholar 

  33. Feder ME, Hofmann GE (1999) Heat-shock proteins molecular chaperones, and the stress response: evolutionary and ecological physiology. Ann Rev Physiol 61:243–282

    Article  CAS  Google Scholar 

  34. Estruch F (2000) Stress-controlled transcription factors stress-induced genes and stress tolerance in budding yeast. FEMS Microb Rev 24:469–486

    Article  CAS  Google Scholar 

  35. Kielbassa C, Roza L, Epe B (1997) Wavelength dependence of oxidative DNA damage induced by UV and visible light. Carcinogenesis 18:811–816

    Article  CAS  PubMed  Google Scholar 

  36. Epe B, Pflaum M, Boiteux S (1993) DNA damage induced by photosensitizers in cellular and cell-free systems. Mutat Res 299:135–145

    Article  CAS  PubMed  Google Scholar 

  37. Pflaum M, Kielbassa C, Garmyn M, Epe B (1998) Oxidative DNA damage induced by visible light in mammalian cells: extent, inhibition by antioxidants and genotoxic effects. Mutat Res/DNA Repair 408(2):137–146

    Article  CAS  Google Scholar 

  38. Kropat J, Gromoff ED, Müller FW, Beck CF (1995) Heat shock and light activation of a Chlamydomonas HSP70 gene are mediated by independent regulatory pathways. Mol Gen Genet 248:727–734

    Article  CAS  PubMed  Google Scholar 

  39. Kropat J, Oster U, Rüdiger W, Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci U S A 94:14168–14172

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Kropat J, Beck CF (1998) Characterization of photoreceptor and signaling pathway for light induction of the Chlamydomonas heat-shock gene HSP70A. Photochem Photobiol 68:414–419

    Article  CAS  Google Scholar 

  41. Kropat J, Oster U, Rüdiger W, Beck CF (2000) Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24:523–531

    Article  CAS  PubMed  Google Scholar 

  42. Cadetti L, Marroni F, Marangoni R, Kuhlmann H-W, Gioffre D, Colombetti G (2004) Phototaxis in the ciliated protozoan Ophryoglena flava: dose–effect curves and action spectrum determination. J Photochem Photobiol B Biol 80:78–83

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Antonietta La Terza or Roberto Marangoni.

Additional information

Antonietta La Terza and Roberto Marangoni are joint last authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fulgentini, L., Passini, V., Colombetti, G. et al. UV Radiation and Visible Light Induce hsp70 Gene Expression in the Antarctic Psychrophilic Ciliate Euplotes focardii . Microb Ecol 70, 372–379 (2015). https://doi.org/10.1007/s00248-015-0566-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0566-y

Keywords

Navigation