Abstract
Increased awareness regarding the harmful effects of ultraviolet (UV)-B radiation has led to the search for new sources of natural UV-B protecting compounds. Mycosporine-like amino acids are one of such promising compounds found in several organisms. Cyanobacteria are ideal organisms for isolation of these compounds due to their compatibility and adaptability to thrive under harsh environmental conditions. In the following investigation, we report the production of shinorine in Leptolyngbya sp. isolated from the intertidal region. Based on the spectral characteristics and liquid chromatography-mass spectrometry analysis, the UV-absorbing compound was identified as shinorine. To the best of our knowledge, this is the first report on the occurrence of shinorine in Leptolyngbya sp. We also investigated the effect of artificial UV-B radiation and periodic desiccation on chlorophyll-a, total carotenoids, and mycosporine-like amino acids (MAAs) production. The UV-B radiation had a negative effect on growth and chlorophyll concentration, whereas it showed an inductive effect on the production of total carotenoids and MAAs. Desiccation along with UV-B radiation led to an increase in the concentration of photoprotective compounds. These results indicate that carotenoids and MAAs thus facilitate cyanobacteria to avoid and protect themselves from the deleterious effects of UV-B and desiccation.
Similar content being viewed by others
References
McKenzie, R. L., Aucamp, P. J., Bais, A. F., Björn, L. O., Ilyas, M., & Madronich, S. (2011). Ozone depletion and climate change: impacts on UV radiation. Photochemical & Photobiological Science, 10, 182–198.
Wu, Y., Polvani, L. M., & Seager, R. (2013). The importance of the Montreal protocol in protecting Earth’s hydroclimate. Journal of Climate, 26, 4049–4068.
Häder, D. P., Kumar, H. D., Smith, R. C., & Worrest, R. C. (2007). Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochemical & Photobiological Science, 6, 267–285.
Sinha, R. P., & Häder, D. P. (2002). Life under solar UV radiation in aquatic organisms. Advances in Space Research, 30, 1547–1556.
Rastogi, R. P., & Sinha, R. P. (2009). Biotechnological and industrial significance of cyanobacterial secondary metabolites. Biotechnology Advances, 27, 521–539.
Rastogi, R. P., & Incharoensakdi, A. (2015). Occurrence and induction of a ultraviolet-absorbing substance in the cyanobacterium Fischerella muscicola TISTR8215. Phycological Research, 63, 51–55.
Schopf, J. W. (1996). Cyanobacteria: pioneers of the early Earth. Beihefte zur Nova Hedwigia, 112, 13–32.
Ehling-Schulz, M., & Scherer, S. (1999). UV protection in cyanobacteria. European Journal of Phycology, 34, 329–338.
Singh, S. P., Kumari, S., Rastogi, R. P., Singh, K. L., & Sinha, R. P. (2008a). Mycosporine-like amino acids (MAAs): chemical structure, biosynthesis and significance as UV-absorbing/screening compounds. Indian Journal of Experimental Biology, 46, 7–17.
Shibata, K. (1969). Pigments and a UV-absorbing substance in corals and a blue-green alga living in the Great Barrier Reef. Plant and Cell Physiology, 10, 325–335.
Oren, A., & Gunde-Cimerman, N. (2007). Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiology Letters, 269, 1–10.
Waditee-Sirisattha, R., Kageyama, H., Fukaya, M., Rai, V., & Takabe, T. (2015). Nitrate and amino acid availability affects glycine betaine and mycosporine-2-glycine in response to changes of salinity in a halotolerant cyanobacterium Aphanothece halophytica. FEMS Microbiology Letters, 362, fnv198.
Richa, & Sinha, R. P. (2015). Biochemical characterization of sunscreening mycosporine-like amino acids from two Nostoc species inhabiting diverse habitats. Protoplasma, 252, 199–208.
Abed, R. M., Polerecky, L., Al-Habsi, A., Oetjen, J., Strous, M., & de Beer, D. (2014). Rapid recovery of cyanobacterial pigments in desiccated biological soil crusts following addition of water. PloS One, 9, e112372.
Potts, M. (1999). Mechanisms of desiccation tolerance in cyanobacteria. European Journal of Phycology, 34, 319–328.
Potts, M. (1994). Desiccation tolerance of prokaryotes. Microbiological Reviews, 58, 755–805.
Karsten, U. (2002). Effects of salinity and ultraviolet radiation on the concentration of mycosporine-like amino acids in various isolates of the benthic cyanobacterium Microcoleus chthonoplastes. Phycological Research, 50, 129–134.
Gao, K., Yu, H., & Brown, M. T. (2007). Solar PAR and UV radiation affects the physiology and morphology of the cyanobacterium Anabaena sp. PCC 7120. Journal of Photochemistry and Photobiology B: Biology, 89, 117–124.
Pattanaik, B., Roleda, M. Y., Schumann, R., & Karsten, U. (2008). Isolate-specific effects of ultraviolet radiation on photosynthesis, growth and mycosporine-like amino acids in the microbial mat-forming cyanobacterium Microcoleus chthonoplastes. Planta, 227, 907–916.
Desikachary, T. V. (1959). Cyanophyta. New Delhi: Indian Council of Agricultural Research.
Konstantinos, A., & Jiří, K. (1988). Modern approach to the classification system of cyanophytes. 3–Oscillatoriales. Algological Studies/ArchivfürHydrobiologie, Supplement Volumes, 50–53, 327–472.
Nübel, U., Garcia-Pichel, F., & Muyzer, G. (1997). PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology, 63, 3327–3332.
Klisch, M., & Häder, D. P. (2000). Mycosporine-like amino acids in the marine dinoflagellate Gyrodinium dorsum: induction by ultraviolet irradiation. Journal of Photochemistry and Photobiology B: Biology, 55, 178–182.
Rastogi, R. P., & Incharoensakdi, A. (2014). Characterization of UV-screening compounds, mycosporine-like amino acids, and scytonemin in the cyanobacterium Lyngbya sp. CU2555. FEMS Microbiology Ecology, 87, 244–256.
Whitehead, K., & Hedges, J. I. (2002). Analysis of mycosporine-like amino acids in plankton by liquid chromatography electrospray ionization mass spectrometry. Marine Chemistry, 80, 27–39.
Fleming, E. D., & Castenholz, R. W. (2007). Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria. Environmental Microbiology, 9, 1448–1455.
Sorokin, C., & Stein, J. (Eds.). (1973). Handbook of phycological methods: culture methods and growth measurement. Cambridge and New York: Cambridge University Press.
Mackinney, G. (1941). Absorption of light by chlorophyll solutions. The Journal of Biological Chemistry, 140, 315–322.
Jensen, A., Hellebust, J. A., & Craige, J. S. (Eds.). (1978). Handbook of phycological methods: physiological and biochemical methods. Cambridge: Cambridge University Press.
Foster, J. S., Green, S. J., Ahrendt, S. R., Golubic, S., Reid, R. P., Hetherington, K. L., & Bebout, L. (2009). Molecular and morphological characterization of cyanobacterial diversity in the stromatolites of Highborne Cay, Bahamas. The ISME Journal, 3, 573–587.
Komárek, J. (2007). Phenotype diversity of the cyanobacterial genus Leptolyngbya in the maritime Antarctic. Polish Polar Research, 28, 211–231.
Bruno, L., Billi, D., Bellezza, S., & Albertano, P. (2009). Cytomorphological and genetic characterization of troglobitic Leptolyngbya strains isolated from Roman hypogea. Applied and Environmental Microbiology, 75, 608–617.
Garcia-Pichel, F., & Castenholz, R. W. (1993). Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Applied and Environmental Microbiology, 59, 163–169.
Matsuyama, K., Matsumoto, J., Yamamoto, S., Nagasaki, K., Inoue, Y., Nishijima, M., & Mori, T. (2015). pH-independent charge resonance mechanism for UV protective functions of shinorine and related mycosporine-like amino acids. The Journal of Physical Chemistry, 119, 12722–12729.
Volkmann, M., & Gorbushina, A. A. (2006). A broadly applicable method for extraction and characterization of mycosporines and mycosporine-like amino acids of terrestrial, marine and freshwater origin. FEMS Microbiology Letters, 255, 286–295.
Lesser, M. P. (2008). Effects of ultraviolet radiation on productivity and nitrogen fixation in the cyanobacterium, Anabaena sp. (Newton’s strain). Hydrobiologia, 598, 1–9.
Worrest, R. C., Thomson, B. E., & Dyke, H. V. (1981). Impact of UV-B radiation upon estuarine microcosms. Photochemistry and Photobiology, 33, 861–867.
He, Y. Y., Klisch, M., & Häder, D. P. (2002). Adaptation of cyanobacteria to UV-B stress correlated with oxidative stress and oxidative damage. Photochemistry and Photobiology, 76, 188–196.
Singh, S. P., Klisch, M., Häder, D. P., & Sinha, R. P. (2008b). Role of various growth media on shinorine (mycosporine-like amino acid) concentration and photosynthetic yield in Anabaena variabilis PCC 7937. World Journal of Microbiology and Biotechnology, 24, 3111–3115.
Hirschberg, J., & Chamovitz, D. (2006) Carotenoids in cyanobacteria. In: Bryant, D. A. (Ed.). The molecular biology of cyanobacteria (Vol. 1, pp 559–579). Dordrecht: Springer Science & Business Media.
Rastogi, R. P., Madamwar, D., & Incharoensakdi, A. (2015). Sun-screening bioactive compounds mycosporine-like amino acids in naturally occurring cyanobacterial biofilms: role in photoprotection. Journal of Applied Microbiology, 119, 753–762.
Sinha, R. P., Klisch, M., Helbling, E. W., & Häder, D. P. (2001). Induction of mycosporine-like amino acids (MAAs) in cyanobacteria by solar ultraviolet-B radiation. Journal of Photochemistry and Photobiology B: Biology, 60, 129–135.
Tirkey, J., & Adhikary, S. P. (2005). Cyanobacteria in biological soil crusts of India. Current Science-Bangalore, 89, 515.
Nishiyama, Y., Yamamoto, H., Allakhverdiev, S. I., Inaba, M., Yokota, A., & Murata, N. (2001). Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. The EMBO Journal, 20, 5587–5594.
De la Coba, F., Aguilera, J., Figueroa, F. L., De Gálvez, M. V., & Herrera, E. (2009). Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. Journal of Applied Phycology, 21, 161–169.
Sindhu, E. R., Preethi, K. C., & RamadasanKuttan. (2010). Antioxidant activity of carotenoid lutein in vitro and in vivo. Indian Journal of Experimental Biology, 48, 843–848.
Kelman, D., Ben-Amotz, A., & Berman-Frank. (2009). Carotenoids provide the major antioxidant defence in the globally significant N2-fixing marine cyanobacterium Trichodesmium. Environmental Microbiology, 11, 1897–1908.
Shimidzu, N., Goto, M., & Miki, W. (1996). Carotenoids as singlet oxygen quenchers in marine organisms. Fisheries Science, 62, 134–137.
Acknowledgements
We thank the Director, CSIR-NIO, for the facilities provided and Dr. N. Ramaiah, Head, Biological Oceanography Division, for his constant support. Authors thank Mr. RM. Meena for the DNA sequencing, Mr. Areef Sardar for SEM analysis, Dr. Dattesh Desai for the Lux meter and Dr. Prabhat Kumar Sharma, Goa University for Digital Radiometer. Devika Joshi acknowledges the Council of Scientific and Industrial Research (CSIR), India, for the financial assistance in the form of Research Fellowship and support provided by Academy of Scientific and Innovative Research (AcSIR). The NIO contribution number is 6056.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Joshi, D., Mohandass, C. & Dhale, M. Effect of UV-B Radiation and Desiccation Stress on Photoprotective Compounds Accumulation in Marine Leptolyngbya sp.. Appl Biochem Biotechnol 184, 35–47 (2018). https://doi.org/10.1007/s12010-017-2523-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-017-2523-3