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Metabolites  2013 

Multiple Roles of Photosynthetic and Sunscreen Pigments in Cyanobacteria Focusing on the Oxidative Stress

DOI: 10.3390/metabo3020463

Keywords: anhydrobiosis, antioxidant, glycosylation, oxidative stress, photosynthetic pigment, sunscreen pigment, UV stress

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Abstract:

Cyanobacteria have two types of sunscreen pigments, scytonemin and mycosporine-like amino acids (MAAs). These secondary metabolites are thought to play multiple roles against several environmental stresses such as UV radiation and desiccation. Not only the large molar absorption coefficients of these sunscreen pigments, but also their antioxidative properties may be necessary for the protection of biological molecules against the oxidative damages induced by UV radiation. The antioxidant activity and vitrification property of these pigments are thought to be requisite for the desiccation and rehydration processes in anhydrobiotes. In this review, the multiple roles of photosynthetic pigments and sunscreen pigments on stress resistance, especially from the viewpoint of their structures, biosynthetic pathway, and in vitro studies of their antioxidant activity, will be discussed.

References

[1]  Castenholz, R.W.; Phylum, B.X. Cyanobacteria. Oxygenic photosynthetic bacteria. In Bergey’s Manual of Systematic Bacteriology. Volume 1: The Archaea and the Deeply Branching and Phototropic Bacteria; Garrity, G., Boone, D.R., Castenholz, R.W., Eds.; Springer-Verlag: New York, NY, USA, 2001; pp. 474–487.
[2]  Namikoshi, M.; Rinehart, K.L. Bioactive compounds produced by cyanobacteria. J. Ind. Microbiol. 1996, 17, 373–384, doi:10.1007/BF01574768.
[3]  Abed, R.M.M.; Dobretsov, S.; Sudesh, K. Applications of cyanobacteria in biotechnology. J. Appl. Microbiol. 2009, 106, 1–12, doi:10.1111/j.1365-2672.2008.03918.x.
[4]  Nagarajan, M.; Maruthanayagam, V.; Sundararaman, M. A review of pharmacological and toxicological potentials of marine cyanobacterial metabolites. J. Appl. Toxicol. 2012, 32, 153–185, doi:10.1002/jat.1717.
[5]  Tamaru, Y.; Takani, Y.; Yoshida, T.; Sakamoto, T. Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc. Commune. Appl. Environ. Microbiol. 2005, 71, 7327–7333, doi:10.1128/AEM.71.11.7327-7333.2005.
[6]  Rebecchi, L.; Altiero, T.; Guidetti, R. Anhydrobiosis: The extreme limit of desiccation tolerance. Invertebr. Surv. J. 2007, 4, 65–81.
[7]  Sakamoto, T.; Yoshida, T.; Arima, H.; Hatanaka, Y.; Takani, Y.; Tamaru, Y. Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc. Commune. Phycol. Res. 2009, 57, 66–73, doi:10.1111/j.1440-1835.2008.00522.x.
[8]  Crowe, J.; Carpenter, J.; Crowe, L. The role of vitrification on anhydrobiosis. Annu. Rev. Physiol. 1998, 60, 73–103, doi:10.1146/annurev.physiol.60.1.73.
[9]  Leslie, S.B.; Israeli, E.; Lighthart, B.; Crowe, J.H.; Crowe, L.M. Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl. Environ. Microb. 1995, 61, 3592–3597.
[10]  Morgan, C.A.; Herman, N.; White, P.A.; Vesey, G. Preservation of microorganisms by drying: A review. J. Microbiol. Meth. 2006, 66, 183–193.
[11]  Tunnacliffe, A.; Lapinski, J. Resurrecting Van Leeuwenhoek’s rotifers: A reappraisal of the role of disaccharides in anhydrobiosis. Phil. Trans. R. Soc. 2003, 358, 1755–1771, doi:10.1098/rstb.2002.1214.
[12]  Sakamoto, T.; Kumihashi, K.; Kunita, S.; Masaura, T.; Inoue-Sakamoto, K.; Yamaguchi, M. The extracellular-matrix-retaining cyanobacterium Nostoc. verrucosum accumulates trehalose, but is sensitive to desiccation. FEMS Microbiol. Ecol. 2011, 77, 385–394, doi:10.1111/j.1574-6941.2011.01114.x.
[13]  Dadheech, N. Desiccation tolerance in cyanobacteria. Afr. J. Microbiol. Res. 2010, 4, 1584–1593.
[14]  Altiero, T.; Guidetti, R.; Boschini, D.; Rebecchi, L. Heat shock proteins in encysted and anhydrobiotic eutardigrades. J. Limnol. 2012, 71, 211–215.
[15]  Shimizu, T.; Kanamori, Y.; Furuki, T.; Kikawada, H.; Okuda, T.; Takahashi, T.; Mihara, H.; Sakurai, M. Desiccation-induced structuralization and glass formation of group 3 late embryogenesis abundant protein model peptides. Biochemistry 2010, 49, 1092–1104.
[16]  Latifi, A.; Ruiz, M.; Zhang, C.-C. Oxidative stress in cyanobacteria. FEMS Microbiol. Rev. 2009, 33, 258–278, doi:10.1111/j.1574-6976.2008.00134.x.
[17]  Kranner, I.; Birtic, S. A modulating role for antioxidants in desiccation tolerance. Integr. Comp. Biol. 2005, 45, 734–740, doi:10.1093/icb/45.5.734.
[18]  Fredrickson, J.K.; Li, S.W.; Gaidamakova, E.K.; Matrosova, V.Y.; Zhai, M.; Sulloway, H.M.; Scholten, J.C.; Brown, M.G.; Balkwill, D.L.; Daly, M.J. Protein oxidation: key to bacterial desiccation resistance? ISME J. 2008, 2, 393–403, doi:10.1038/ismej.2007.116.
[19]  Crowe, J.H.; Hoekstra, F.A.; Crowe, L.M. Anhydrobiosis. Annu. Rev. Physiol. 1992, 54, 579–599.
[20]  Hoekstra, F.A.; Golovina, E.A. Membrane behavior during dehydration: Implications for desiccation tolerance. Russ. J. Plant. Physiol. 1999, 46, 295–306.
[21]  Miyashita, H.; Adachi, K.; Kurano, N.; Ikemoto, H.; Chihara, M.; Miyachi, S. Chlorophyll d as a major pigment. Nature 1996, 383, 402, doi:10.1038/383402a0.
[22]  Blankenship, R.E. Photosynthetic Pigments: Structure and Spectroscopy. In Molecular Mechanisms of Photosynthesis; Wiley-Blackwell: Hoboken, NJ, USA, 2002; pp. 42–60.
[23]  Kehoe, D.M. Chromatic adaptation in cyanobacteria. PNAS 2010, 107, 9029–9030, doi:10.1073/pnas.1004510107.
[24]  Richa, M.K.; Sinha, R.P. Antioxidants as natural arsenal against multiple stresses in cyanobacteria. Int. J. Pharma. Biosci. 2011, 2, B168–B187.
[25]  Ferruzzi, M.G.; Bohm, V.; Courtney, P.D.; Schwarts, S.J. Antioxidant and antimutagenic activity of dietary chlorophyll derivatives determined by radical scavenging and bacterial reverse mutagenesis assays. J. Food Sci. 2002, 67, 2589–2595, doi:10.1111/j.1365-2621.2002.tb08782.x.
[26]  Krieger-Liszkay, A. Singlet oxygen production in photosynthesis. J. Exp. Bot. 2004, 56, 337–346, doi:10.1093/jxb/erh237.
[27]  Hirata, T.; Tanaka, M.; Ooike, M.; Tsunomura, T.; Sakaguchi, M. Antioxidant activities of phycocyanobilin prepared from Spirulina. platensis. J. App. Phycol. 2000, 12, 435–439, doi:10.1023/A:1008175217194.
[28]  Zhou, Z.P.; Liu, L.N.; Chen, X.L.; Wang, J.X.; Chen, M.; Zhang, Y.Z.; Zhou, B.C. Factors that effect antioxidant activity of C-phycocyanins from Spirulina. platensis. J. Food Biochem. 2005, 29, 313–322.
[29]  Takaichi, S.; Maoka, T.; Mochimaru, M. Unique carotenoids in the terrestrial cyanobacterium Nostoc. Commune NIES-24: 2-Hydroxymyxol 20-fucoside, nostoxanthin and canthaxanthin. Curr. Microbiol. 2009, 59, 413–419, doi:10.1007/s00284-009-9453-4.
[30]  Kerfeld, C.A.; Sawaya, M.R.; Brahmandam, V.; Cascio, D.; Ho, K.K.; Trevithick-Sutton, C.C.; Krogmann, D.W.; Yeates, T.O. The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure 2003, 11, 55–65, doi:10.1016/S0969-2126(02)00936-X.
[31]  Boulay, C.; Abasova, L.; Six, C.; Vass, I.; Kirilovsky, D. Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochim. Biophy. Acta 2008, 1777, 1344–1354, doi:10.1016/j.bbabio.2008.07.002.
[32]  Wilson, A.; Gall, A.; Bonetti, C.; Alexandre, M.; Routaboul, J.M.; Kerfeld, C.A.; van Grondelle, R.; Robert, B.; Kennis, J.T.M.; Kirilovsky, D. A photoactive carotenoid protein acting as light intensity sensor. Proc. Natl. Acad. Sci. USA 2008, 105, 12075–12080, doi:10.1073/pnas.0804636105.
[33]  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. 1997, 179, 1940–1945.
[34]  Wachi, Y.; Burgess, J.G.; Iwamoto, K.; Yamada, N.; Nakamura, N.; Matsunaga, T. Effect of ultraviolet-A (UV-A) light on growth, photosynthetic activity and production of biopterin glucoside by the marine UV-A resistant cyanobacterium Oscillatoria. sp. Biochim. Biophys. Acta 1995, 1244, 165–168, doi:10.1016/0304-4165(94)00219-N.
[35]  Sindhu, E.R.; Preethi, K.C.; Kuttan, R. Antioxidant activity of carotenoid lutein in vitro and in vivo. Ind. J. Exp. Biol. 2010, 48, 843–848.
[36]  Shimizu, N.; Goto, M.; Miki, W. Carotenoids as singlet oxygen quenchers in marine organisms. Fisheries Sci. 1996, 62, 134–137.
[37]  Starcevic, A.; Akthar, S.; Dunlap, W.C.; Shick, J.M.; Hranueli, D.; Cullum, J. Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella. vectensis, have microbial origins. Proc. Natl. Acad. Sci. USA 2008, 105, 2533–2537.
[38]  Sinha, R.P.; H?der, D.P. UV-protectants in cyanobacteria. Plant Sci. 2008, 174, 278–289, doi:10.1016/j.plantsci.2007.12.004.
[39]  Wu, J.J.; Chalker, B.E.; Rideout, J.A. Two new UV-absorbing compounds from Stylophora. pistillata: Sulfate esters of mycosporine-like amino acids. Tetrahedron Lett. 1997, 38, 2525–2526, doi:10.1016/S0040-4039(97)00391-2.
[40]  B?hm, G.A.; Pfleiderer, W.; B?ger, 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. 1995, 270, 8536–8539.
[41]  Shick, J.M.; Dunlap, W.C. Mycosporine-like amino acids and related gadusols: Biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 2002, 64, 223–262, doi:10.1146/annurev.physiol.64.081501.155802.
[42]  Balskus, E.P.; Walsh, C.T. The genetic and molecular basis for sunscreen biosynthesis in cyanobacteria. Science 2010, 329, 1653–1656, doi:10.1126/science.1193637.
[43]  Spence, E.; Dunlap, W.C.; Shick, J.M.; Long, P.F. Redundant pathways of sunscreen biosynthesis in a cyanobacterium. Chem. BioChem. 2012, 13, 531–533.
[44]  Portwich, A.; Garcia-Pichel, F. Biosynthetic pathway of mycosporines (mycosporine-like amino acids) in the cyanobacterium Chlorogloeopsis. sp. strain PCC 6912. Phycologia. 2003, 42, 384–392, doi:10.2216/i0031-8884-42-4-384.1.
[45]  Gao, Q.; Garcia-Pichel, F. An ATP-grasp ligase involved in the last biosynthetic step of the iminomycosporine shinorine in Nostoc. punctiforme ATCC 29133. J. Bacteriol. 2011, 193, 5923–5928, doi:10.1128/JB.05730-11.
[46]  Singh, S.P.; Klisch, M.; Sinha, R.P.; H?der, D.P. Effects of abiotic stressors on synthesis of the mycosporine-like amino acid shinorine in the cyanobacterium Anabaena variabilis PCC 7937. Photochem. Photobiol. 2008, 84, 1500–1505, doi:10.1111/j.1751-1097.2008.00376.x.
[47]  Castenholz, R.W.; Garcia-Pichel, F. Cyanobacterial responses to UV-radiation. In The Ecology of Cyanobacteria: Their Diversity in Time and Space; Whitton, B.A., Potts, M., Eds.; Springer: Heidelberg, Germany, 2002; pp. 591–611.
[48]  Shick, J.M. The continuity and intensity of ultraviolet irradiation affect the kinetics of biosynthesis, accumulation, and conversion of mycosporine-like amino acids (MAAs) in the coral Stylophora. pistillata. Limnol. Oceanogr. 2004, 49, 442–458.
[49]  Klisch, M.; Richter, P.; Puchta, R.; H?der, D.P; Bauer, W. The stereostructure of porphyra-334: An experimental and calculational NMR investigation. evidence for an efficient “proton sponge”. Helvetica Chim. Acta. 2007, 90, 488–511.
[50]  Conde, F.R.; Churio, M.S.; Previtali, C.M. The photoprotector mechanism of mycosporine-like amino acids. Excited state properties and photostability of porphyra-334 in aqueous solution. J. Photochem. Photobiol. B 2000, 56, 139–144.
[51]  Conde, F.R.; Churio, M.S.; Previtali, C.M. The deactivation pathways of the excited-states of the mycosporine-like amino acids shinorine and porphyra-334 in aqueous solution. Photochem. Photobiol. Sci. 2004, 3, 960–967.
[52]  Conde, F.R.; Churio, M.S.; Previtali, C.M. Experimental study of excited-state properties and photostability of the mycosporine-like amino acid palythine in water solution. Photochem. Photobiol. Sci. 2007, 6, 669–674, doi:10.1039/b618314j.
[53]  Dunlap, W.C.; Yamamoto, Y. Small-molecule antioxidants in marine organisms: Antioxidant activity of mycosporine-glycine. Comp. Biochem. Physiol. 1995, 112, 105–114, doi:10.1016/0305-0491(95)00086-N.
[54]  De la Coba, F.; Aguilera, J.; Figueroa, F.L.; de Gálvez, M.V.; Herrera, E. Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J. Appl. Phycol. 2009, 21, 161–169, doi:10.1007/s10811-008-9345-1.
[55]  Nakayama, R.; Tamura, Y.; Kikuzaki, H.; Nakatani, N. Antioxidant effect of the constituents of susabinori (Porphyra yezoensis). J. Am. Oil Chem. Soc. 1999, 76, 649–653, doi:10.1007/s11746-999-0017-3.
[56]  Furusaki, A.; Matsumoto, T.; Tsujino, I.; Sekikawa, I. The crystal and molecular structure of palythine, trihydrate. Bull. Chem. Soc. Jpn. 1980, 53, 319–323.
[57]  Matsui, K.; Nazifi, E.; Kunita, S.; Wada, N.; Matsugo, S.; Sakamoto, T. Novel glycosylated mycosporine-like amino acids with radical scavenging activity from the cyanobacterium Nostoc. commune. J. Photochem. Photobiol. B: Biol. 2011, 105, 81–89.
[58]  Wright, D.J.; Smith, S.C.; Joardar, V.; Scherer, S.; Jervis, J.; Warren, A.; Helm, R.F.; Potts, M. UV irradiation and desiccation modulate the three-dimensional extracellular matrix of Nostoc. commune (Cyanobacteria). J. Biol. Chem. 2005, 280, 40271–40281.
[59]  Hill, D.R.; Peat, A.; Potts, M. Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc. commune (Cyanobacteria). Protoplasma. 1994, 182, 126–148, doi:10.1007/BF01403474.
[60]  Proteau, P.J.; Gerwick, W.H.; Garcia-Pichel, F.; Castenholz, R. The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia. 1993, 49, 825–829, doi:10.1007/BF01923559.
[61]  Bultel-Poncé, V.; Felix-Theodore, F.; Sarthon, C.; Ponge, J.F.; Bodo, B. New pigments from the terrestrial cyanobacterium Scytonema. sp. collected on the Mitaraka Inselberg, French Guyana. J. Nat. Prod. 2004, 67, 678–681, doi:10.1021/np034031u.
[62]  Soule, T.; Stout, V.; Swingley, W.D.; Meeks, J.C.; Garcia-Pichel, F. Molecular genetics and genomic analysis of scytonemin biosynthesis in Nostoc. punctiforme ATCC 29133. J. Bacteriol. 2007, 189, 4465–4472.
[63]  Ohshima, T.; Nishida, N.; Bakthavatsalam, S.; Kataoka, K.; Takada, H.; Yoshimura, T.; Esaki, N.; Soda, K. The purification, characterization, cloning and sequencing of the gene for a halostable and thermostable leucine dehydrogenase from Thermoactinomyces. intermedius. Eur. J. Biochem. 1994, 222, 305–312, doi:10.1111/j.1432-1033.1994.tb18869.x.
[64]  Chipman, D.; Barak, Z.A.; Schloss, J.V. Biosynthesis of 2-aceto-2-hydroxy acids: Acetolactate synthases and acetohydroxyacid synthases. Biochim. Biophys. Acta 1998, 1385, 401–419, doi:10.1016/S0167-4838(98)00083-1.
[65]  Balskus, E.P.; Walsh, C.T. An enzymatic cyclopentyl[b]indole formation involved in scytonemin biosynthesis. J. Am. Chem. Soc. 2009, 131, 14648–14649, doi:10.1021/ja906752u.
[66]  Sinha, R.P.; Klisch, M.; Gr?niger, A.; H?der, D.P. Responses of aquatic algae and cyanobacteria to solar UV-B. Plant. Ecol. 2001, 154, 219–236.
[67]  Dillon, J.G.; Tatsumi, C.M.; Tandingan, P.G.; Castenholz, R.W. Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis. sp.). Arch. Microbiol. 2002, 177, 322–331, doi:10.1007/s00203-001-0395-x.
[68]  Fleming, E.D.; Castenholz, R.W. Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria. Environ. Microbiol. 2007, 9, 1448–1455, doi:10.1111/j.1462-2920.2007.01261.x.
[69]  Fleming, E.D.; Castenholz, R.W. Effects of nitrogen source on the synthesis of the UV-screening compound, scytonemin, in the cyanobacterium Nostoc. punctiforme PCC 73102. FEMS Microbiol. Ecol. 2008, 63, 301–308, doi:10.1111/j.1574-6941.2007.00432.x.
[70]  Vincent, W.F.; Downes, M.T.; Castenholz, R.W.; Howard-Williams, C. Community structure and pigment organisation of cyanobacteria-dominated microbial mats in Antarctica. Eur. J. Phycol. 1993, 28, 213–221, doi:10.1080/09670269300650321.
[71]  Garcia-Pichel, F.; Sherry, N.D.; Castenholz, R.W. Evidence for an ultra-violet sunscreen role of the extracellular pigment scytonemin in the terrestrial cyanobacterium Chlorogloeopsis. sp. Photochem. Photobiol. 1992, 56, 17–23, doi:10.1111/j.1751-1097.1992.tb09596.x.
[72]  Matsui, K.; Nazifi, E.; Hirai, Y.; Wada, N.; Matsugo, S.; Sakamoto, T. The cyanobacterial UV-absorbing pigment scytonemin displays radical scavenging activity. J. Gen. Appl. Microbiol. 2012, 58, 137–144, doi:10.2323/jgam.58.137.
[73]  Hunsucker, S.W.; Tissue, B.A.; Potts, M.; Helm, R.F. Screening protocol for the ultraviolet-photoprotective pigment scytonemin. Anal. Biochem. 2001, 288, 227–230, doi:10.1006/abio.2000.4895.
[74]  Richter, P.R.; Sinha, R.P.; H?der, D.P. Scytonemin-rich epilithic cyanobacteria survive acetone treatment. Curr. Trends Microbiol. 2006, 2, 13–19.

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