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Natural microbial UV radiation filters — Mycosporine-like amino acids

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Abstract

Ozone depletion by anthropogenic gases has increased the atmospheric transmission of solar ultraviolet-B radiation (UV-B, 280–315 nm). There is a logical link between the natural defenses of terrestrial and marine organisms against UV radiation and the prevention of UV-induced damage to human skin. UV light degrades organic molecules such as proteins and nucleic acids, giving rise to structural changes that directly affect their biological function. These compounds offer the potential for development of novel UV blockers for human use. The biological role of mycosporine-like amino acids (MAAs) and scytonemin as a defense against solar radiation in organisms, together with their structure, synthesis, distribution, regulation and effectiveness, are reviewed in this article. This review points to the role of MAAs as a natural defense against UV radiation.

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Abbreviations

UV-A:

ultraviolet-A radiation (315–400 nm)

UV-B:

ultraviolet-B radiation (280–315 nm)

UV-C:

ultraviolet-C radiation (100–280 nm)

MAA(s):

mycosporine-like amino acid

LC-ESI-MS:

liquid chromatography coupled with electrospray ionization mass spectrometry

References

  • Adhikary S.P., Sahu J.K.: UV protecting pigment of the terrestrial cyanobacterium Tolypothrix byssoidea. J.Plant Physiol. 153, 770–773 (1998).

    Article  CAS  Google Scholar 

  • Arai T., Nishijima M., Adachi K., Sano H.: Isolation and structure of a UV absorbing substance from the marine bacterium Micrococcus sp. Inst.Marine Biotechnol.Rep.Tokyo 334, 88–94 (1992).

    Google Scholar 

  • Arpin N., Curt R., Favre-Bonvin J.: Mycosporines: mise au point et données nouvelles concernant leurs structures, leur distribution, leur localisation et leur biogenèse. Rev.Mycol. 43, 247–257 (1979).

    CAS  Google Scholar 

  • Bandaranayake W.M.: Mycosporines: Are they nature’s sunscreens? Nat.Prod.Rep. 15, 159–172 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Banerjee M., Hader D.P.: Effects of UV radiation on the rice field cyanobacterium, Aulosira fertilissima. Environ.Exper.Botany 36, 281–291 (1996).

    Article  Google Scholar 

  • Bohm G.A., Pfleiderer W., Böger P., Scherer S.: Structure of a novel oligosaccharide-mycosporine-amino acid ultraviolet A/B sunscreen pigment from the terrestrial cyanobacterium Nostoc commune. J.Biol.Chem. 270, 8536–8539 (1995).

    Article  CAS  PubMed  Google Scholar 

  • Büdel B., Karsten U., Garcia-Pichel F.: Ultraviolet-absorbing scytonemin and mycosporine-like amino acid derivatives in exposed, rock-inhabiting cyanobacterial lichens. Oecologia 112, 165–172 (1997).

    Article  Google Scholar 

  • Buscot F., Bernillon J.: Mycosporins and related compounds in field and cultured mycelial structures of Morchella esculenta. Mycol.Res. 95, 752–754 (1991).

    Article  CAS  Google Scholar 

  • Carreto J.I., Carignan M.O., Daleo G., De Marco S.G.: Occurrence of mycosporine-like amino acids in the red-tide dinoflagellate Alexandrium excavatum: UV-photoprotective compounds? J.Plankton Res. 121, 909–921 (1990).

    Article  Google Scholar 

  • de Chazal N.M., Smith G.D.: Characterization of a brown Nostoc sp. from Java that is resistant to high light intensity and UV. Microbiology 140, 3183–3189 (1994).

    Article  Google Scholar 

  • Donkor V.A., Hader D.P.: Effects of ultraviolet irradiation on photosynthetic pigments in some filamentous cyanobacteria. Aquat.Microb.Ecol. 11, 143–149 (1996).

    Article  Google Scholar 

  • Donkor V.A., Hader D.P.: Ultraviolet radiation effects on pigmentation in the cyanobacterium Phormidium uncinatum. Acta Protozool. 36, 49–55 (1997).

    CAS  Google Scholar 

  • Dunlap W.C., Shick J.M.: Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J.Phycol. 34, 418–430 (1998).

    Article  Google Scholar 

  • Dunlap W.C., Yamamoto Y.: Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp. Biochem.Physiol. 112B, 105–114 (1995).

    Article  CAS  Google Scholar 

  • Dunlap W.C., Chalker B.E., Oliver J.K.: Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. III. UV-B absorbing compounds. J.Exp.Mar.Biol.Ecol. 104, 239–248 (1986).

    Article  Google Scholar 

  • Dunlap W.C., Masaki K., Yamamoto Y., Larsen R.M., Karube I.: A novel antioxidant derived from seaweed, pp. 33–35 in New Developments in Marine Biotechnology (Y. LeGal, H. Halvorson, Eds). Plenum Press, New York 1998.

    Chapter  Google Scholar 

  • Ehling-Schulz M., Bilger W., Scherer S.: UV-B-induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune. J.Bacteriol. 179, 1940–1945 (1997).

    PubMed Central  CAS  PubMed  Google Scholar 

  • Enk D.C., Hochberg M., Torres A., Lev O., Dor I., Niddam V., Dembitsky V.M., Srebnik M.: Novel UV-B compound from lichen Collema cristatum. Israel Pat.Appl. IL02/00725 (2002).

    Google Scholar 

  • Favre-Bonvin J., Arpin N., Brevard C.: Structure de la mycosporine (P310). Can.J.Chem. 54, 1105–1113 (1976).

    Article  CAS  Google Scholar 

  • Galun M. (Ed.): Handbook of Lichenology, Vol. 2. CRC Press, Boca Raton (FL) 1988.

    Google Scholar 

  • Garcia-Pichel F., Castenholz R.W.: Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J.Phycol. 27, 395–409 (1991).

    Article  CAS  Google Scholar 

  • Garcia-Pichel F., Castenholz R.W.: Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimation of their screening capacity. Appl.Environ.Microbiol. 59, 163–169 (1993).

    PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia-Pichel F., Sherry N., Castenholz R.W.: Evidence for an ultraviolet sunscreen role of the extracellular pigment scytonemin in the terrestrial cyanobacterium, Chlorogloeposis sp. Photochem.Photobiol. 56, 17–23 (1992).

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Pichel F., Wingard C.E., Castenholz R.W.: Evidence regarding the UV sunscreen role of a mycosporine-like compound in the cyanobacterium Gloeocapsa sp. Appl.Environ.Microbiol. 59, 170–176 (1993).

    PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia-Pichel F., Castenholz R.W.: Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimation of their screening capacity. Appl.Environ.Microbiol. 59, 163–169 (1993).

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gorbushina A.A., Whitehead K., Dornieden T., Niesse A., Schulte A., Hedges J.I.: Black fungal colonies as units of survival: hyphal mycosporines synthesized by rock-dwelling microcolonial fungi. Can.J.Bot. 81, 131–138 (2003).

    Article  CAS  Google Scholar 

  • Gröniger A., Sinha R.P., Klisch M., Hader D.P.: Photoprotective compounds in cyanobacteria, phytoplankton and macroalgae — a database. J.Photochem.Photobiol. B: Biology 58, 115–122 (2000).

    Article  PubMed  Google Scholar 

  • Ha-Duong M., Megie G.: Hauglustaine A pro-active stratospheric ozone protection scenario. Global Environ.Change 13, 43–49 (2003).

    Article  Google Scholar 

  • Hader D.P., Worrest R.C.: Consequences of the effects of increased solar ultraviolet radiation on aquatic ecosystems, pp. 11–30 in The Effects of Ozone Depletion on Aquatic Ecosystems (D.P. Hader, Ed.), chapter 3, Environmental Intelligence Unit. Academic Press-R.G. Landes Co., Austin 1997.

    Google Scholar 

  • Hader D.P., Kumar H.D., Smith R.C., Worrest R.C.: Effects on aquatic ecosystems. J.Photochem.Photobiol. B 46, 53–68 (1998).

    Article  CAS  Google Scholar 

  • Hannach G., Sigleo A.C.: Photoinduction of UV-absorbing compounds in six species of marine phytoplankton. Mar.Ecol.Progr.Ser. 174, 207–222 (1998).

    Article  CAS  Google Scholar 

  • Helbling E.W., Chalker B.E., Dunlap W.C., Holm-Hansen O., Villafane V.E.: Photoacclimation of Antarctic diatoms to solar ultraviolet radiation. J.Exp.Mar.Biol.Ecol. 204, 85–101 (1996).

    Article  Google Scholar 

  • Jiang Y.B., Yung Y.L., Sander S.P., Travis L.D.: Modeling of atmospheric radiative transfer with polarization and its application to the remote sensing of tropospheric ozone. J.Quantit.Spectr.Rad.Transfer 84, 169–179 (2004).

    Article  CAS  Google Scholar 

  • Kane R.P.: Mismatch between variations of solar indices, stratospheric ozone and UV-B observed at ground. J.Atmospher.Solar-Terrestr.Phys. 64, 2063–2074 (2002).

    Article  CAS  Google Scholar 

  • Karentz D.: Chemical defenses of marine organisms against solar radiation exposure: UV-absorbing mycosporine-like amino acids and scytonemin, pp. 481–520 in Marine Chemical Ecology (J.B. McClintock, B.J. Baker, Eds). CRC Press, Boca Raton (FL) 2001.

    Chapter  Google Scholar 

  • Karsten U., Garcia-Pichel F.: Carotenoids and mycosporine-like amino acid compounds in members of the genus Microcoleus (Cyanobacteria): a chemosystematic study. Syst.Appl.Microbiol. 19, 285–294 (1996).

    Article  Google Scholar 

  • Kedar L., Kashman Y., Oren A.: Mycosporine-2-glycine is the major mycosporine-like amino acid in a unicellular cyanobacterium (Euhalothece sp.) isolated from a gypsum crust in a hypersaline saltern pond. FEMS Microbiol.Lett. 208, 233–237 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Kumar A., Tyagi M.B., Srinivas G., Singh N., Kumar H.D., Sinha R.P., Hader D.P.: UV-B shielding role of FeCl3 and certain cyanobacterial pigments. Photochem.Photobiol. 64, 321–325 (1996).

    Article  CAS  Google Scholar 

  • Leach C.M.: Ultraviolet-absorbing substances associated with light-induced sporulation in fungi. Can.J.Bot. 43, 185–200 (1965).

    Article  CAS  Google Scholar 

  • Lee H.W., Oh C.H., Geyer A., Pfeiderer W., Park Y.S.: Characterization of a novel unconjugated pteridine glycoside, cyanopterin, in Synechocystis sp. PCC 6803. Biochim.Biophys.Acta 1410, 61–70 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Lesser M.: Acclimation of phytoplankton to UV-B radiation: oxidative stress and photoinhibition of photosynthesis are not prevented by UV-absorbing compounds in the dinoflagellate Prorocentrum micans. Mar.Ecol.Progr.Ser. 132, 287–297 (1996).

    Article  CAS  Google Scholar 

  • Maragos J.E.: A study of the ecology of Hawaiian reef corals. PhD Thesis. University of Hawaii, Honolulu 1972.

    Google Scholar 

  • Marchant H.J., Davidson A.T., Kelly G.J.: UV-B protecting compounds in the marine alga Phaeocystis pouchetii from Antarctica. Mar.Biol. 109, 391–395 (1991).

    Article  CAS  Google Scholar 

  • McCulloch A.: Fluorocarbons in the global environment: a review of the important interactions with atmospheric chemistry and physics. J.Fluor.Chem. 123, 21–29 (2003).

    Article  CAS  Google Scholar 

  • Montero O., Lubian L.M.: Mycosporine-like amino acid (MAAs) production by Heterocapasa sp. (Dinophyceae) in indoor cultures. Biomol.Engineer. 20, 183–189 (2003).

    Article  CAS  Google Scholar 

  • Neale P.J., Davis R.F., Cullen J.J.: Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton. Nature 392, 585–589 (1998).

    Article  CAS  Google Scholar 

  • de Nys R., Steinberg P.D.: Linking marine biology and biotechnology. Curr.Opin.Biotechnol. 13, 244–248 (2002).

    Article  PubMed  Google Scholar 

  • Okaichi T., Tokumura T.: Isolation of cyclohexene derivatives from Noctiluca miliaris Suriray, pp. 664–671 in 23rd Symp. Chemistry of Natural Products (Nagoya). Chemical Society of Japan, Tokyo 1980.

    Google Scholar 

  • Oren A.: Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria. Geomicrobiol.J. 14, 231–240 (1997).

    Article  CAS  Google Scholar 

  • Pentecost A.: Field relationships between scytonemin density, growth and irradiance in cyanobacteria occurring in low illumination regimes. Microb.Ecol. 26, 101–110 (1993).

    Article  CAS  PubMed  Google Scholar 

  • Platt U., Honninger G.: The role of halogen species in the troposphere. Chemosphere 52, 325–338 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Portwich A., Garcia-Pichel F.: A novel prokaryotic UVB photoreceptor in the cyanobacterium Chlorogloeopsis PCC6912. Photochem.Photobiol. 71, 493–498 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Price J.H., Forrest H.S.: 310 nm absorbance in Physalia physalis: distribution of the absorbance and isolation of a 310 nm absorbing compound. Comp.Biochem.Physiol. 30, 879–888 (1969).

    Article  CAS  Google Scholar 

  • Proteau P.J., Gerwick W.H., Garcia-Pichel F., Castenholz R.W.: The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia 49, 825–829 (1993).

    Article  CAS  PubMed  Google Scholar 

  • Quesada A., Vincent W.F., Lean D.R.S.: Community and pigment structure of Arctic cyanobacterial assemblages: the occurrence and distribution of UV-absorbing compounds. FEMS Microbiol.Ecol. 28, 315–323 (1999).

    Article  CAS  Google Scholar 

  • Rai A.N. (Ed.): CRC Handbook of Symbiotic Cyanobacteria, chapter 2. CRC Press, Boca Raton (FL) 1993.

    Google Scholar 

  • Riegger L., Robinson D.: Photoinduction of UV-absorbing compounds in Antarctic diatoms and Phaeocystis antarctica. Mar.Ecol.Progr.Ser. 160, 13–25 (1997).

    Article  Google Scholar 

  • Roy S.: Strategies for the minimization of UV-induced damage, pp. 177–205 in S. de Mora, S. Demers, M. Vernet, Eds): The Effects of UV Radiation in the Marine Environment. Cambridge University Press, Cambridge (UK) 2000.

    Chapter  Google Scholar 

  • Rozema J., Bjorn L.O., Bornman J.F., Gaberscik A., Hader D.P., Trost T., Germ M., Klisch M., Gröniger A., Sinha R.P., Lebert M., He Y.Y., Buffoni-Hall R., de Bakker N.V.J., van de Staaij J., Meijkamp B.B.: The role of UV-B radiation in aquatic and terrestrial ecosystems — an experimental and functional analysis of the evolution of UV-absorbing compounds. J.Photochem.Photobiol. B 66, 2–12 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Saraf N., Beig G.: Solar response in the vertical structure of ozone and temperature in the tropical stratosphere. J.Atm.Solar-Terrestr.Phys. 65, 1235–1243 (2003).

    Article  CAS  Google Scholar 

  • Scherer S., Chen T.W., Boger P.: A new UV-A/B protecting pigment in the terrestrial cyanobacterium Nostoc commune. Plant Physiol. 88, 1055–1057 (1988).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shashar N., Banaszak A.T., Lesser M.P., Amrani D.: Coral endolithic algae: life in a protected environment. Pacif.Sci. 51, 167–173 (1997).

    Google Scholar 

  • Shibata K.: Pigments and a UV absorbing substance in corals and a blue green alga living in the Great Barrier Reef. Plant Cell Physiol. 10, 325–335 (1969).

    CAS  Google Scholar 

  • Shick J.M., Dunlap W.C.: Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Ann.Rev.Physiol. 64, 223–262 (2002).

    Article  CAS  Google Scholar 

  • Shick J.M., Dunlap W.C., Chalker B.E., Banaszak A.T., Rosenzweig T.K.: Survey of ultraviolet radiation absorbing mycosporine-like amino acids in organs of coral reef holothuroids. Mar.Ecol.Progr.Ser. 90, 139–148 (1992).

    Article  CAS  Google Scholar 

  • Sinha R.P., Hader D.P.: Photobiology and ecophysiology of rice field cyanobacteria. Photochem.Photobiol. 64, 887–896 (1996).

    Article  CAS  Google Scholar 

  • Sinha R.P., Hader D.P.: Impacts of UV-B irradiation on rice-field cyanobacteria, pp. 189–198 in The Effects of Ozone Depletion on Aquatic Ecosystems (D.P. Hader, Ed.), chapter 9. Environmental Intelligence Unit. Academic Press-R.G. Landes Co., Austin 1997.

    Google Scholar 

  • Sinha R.P., Klisch M., Hader D.P.: Induction of a mycosporine-like amino acid (MAA) in the rice-field cyanobacterium Anabaena sp by UV irradiation. J.Photochem.Photobiol. B 52, 59–64 (1999).

    Article  CAS  Google Scholar 

  • Sivalingam P.M., Ikawa T., Nisizawa K.: Possible physiological roles of a substance showing characteristic UV-absorbing patterns in some marine algae. Plant Cell Physiol. 15, 583–586 (1974).

    CAS  Google Scholar 

  • Sommaruga R., Garcia-Pichel F.: UV-absorbing mycosporine-like compounds in planktonic and benthic organisms from a high-mountain lake. Arch.Hydrobiol. 144, 255–269 (1999).

    CAS  Google Scholar 

  • Takahashi T., Feely R.A., Weiss R.F., Wanninkhof R.H., Chipman D.W., Sutherland S.C., Takahashi T.: Global air-sea flux of CO2: an estimate based on measurements of sea-air pCO2 difference. Proc.Nat.Acad.Sci.USA 94, 8282–8299 (1997).

    Google Scholar 

  • Torres A., Pergament I., Smoum R., Niddam V., Dembitsky V.M., Temina M., Hochberg M., Dor I., Enk D.C., Lev O., Srebnik M.: A new UV-B-absorbing mycosporine with photo-protective activity from the lichenized ascomycete Collema cristatum. Eur.J.Biochem. 271, 780–784 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Tsujino I.: Studies on the compounds specific for each group of marine algae. II. Extraction and isolation of characteristic ultraviolet absorbing material in Rhodophyta. Bull.Fac.Fisheries, Hokkaido Univ. 12, 59–65 (1961).

    CAS  Google Scholar 

  • Turian G.: Primary colonisation of concrete walls by a UV-protectively pigmented Chrysocapsa (cyanobacteria). Saussurea 16, 43–48 (1985).

    Google Scholar 

  • Vernet M., Smith R.C.: Effects of ultraviolet radiation on the pelagic Antarctic ecosystem, pp. 247–265 in The Effects of Ozone Depletion on Aquatic Ecosystems (D.-P. Hader, Ed.), chapter 16, Environmental Intelligence Unit. Academic Press-R.G. Landes Co., Austin (USA) 1997.

    Google Scholar 

  • Vernet M., Whitehead K.: Release of ultraviolet-absorbing compounds by the red-tide dinoflagellate Lingulodinium polyedra. Mar. Biol. 127, 35–44 (1996).

    Article  CAS  Google Scholar 

  • Vincent W.F., Downes M.T., Castenholz R.W., Howard-Williams C.: Community structure and pigment organization of cyanobacteria-dominated microbial mats in Antarctica. Eur.J.Phycol. 28, 213–221 (1993).

    Article  Google Scholar 

  • Volkmann M., Whitehead K., Rutters H., Rullkotter J., Gorbushina A.A.: Mycosporine-glutamicol-glucoside: a natural UV-absorbing secondary metabolite of rock-inhabiting microcolonial fungi. Rapid Comm.Mass Spectrom. 17, 897–902 (2003).

    Article  CAS  Google Scholar 

  • Xiong F., Komenda J., Kopecký J., Nedbal L.: Strategies of ultraviolet-B protection in microscopic algae. Physiol.Plant. 100, 378–388 (1997).

    Article  CAS  Google Scholar 

  • Xiong F., Kopecký J., Nedbal L.: The occurrence of UV-B absorbing mycosporine-like amino acids in freshwater and terrestrial microalgae. Aquat.Bot. 63, 37–49 (1999).

    Article  CAS  Google Scholar 

  • Young H., Patterson V.J.: A UV protective compound from Glomerella cingulata — a mycosporine. Phytochemistry 21, 1075–1077 (1982).

    Article  CAS  Google Scholar 

  • Wangberg S.A., Persson A., Karlson B.: Effects of UV-B radiation on synthesis of mycosporine-like amino acids and growth in Heterocapsa triquetra (Dinophyceae). J.Photochem.Photobiol. B 37, 141–146 (1997).

    Article  Google Scholar 

  • Whitehead K., Hedges J.I.: Analysis of mycosporine-like amino acids in plankton by liquid chromatography electrospray ionization mass spectrometry. Mar.Chem. 80, 27–39 (2002).

    Article  CAS  Google Scholar 

  • Wittenburg J.B.: The source of carbon monooxide in the float of the Portugese man-of-war Physalia physalis L. J.Exp.Biol. 37, 698–705 (1960).

    Google Scholar 

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Řezanka, T., Temina, M., Tolstikov, A.G. et al. Natural microbial UV radiation filters — Mycosporine-like amino acids. Folia Microbiol 49, 339–352 (2004). https://doi.org/10.1007/BF03354663

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