Carotenoids provide the major antioxidant defence in the globally significant N2-fixing marine cyanobacterium Trichodesmium

Environmental Microbiology

Volumn 11, Issue 7, 2009, Pages 1897-1908

  Kelman, Dovi ^a   Ben Amotz, Ami ^b   Berman Frank, Ilana ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b ISRAEL OCEANOGRAPHIC AND LIMNOLOGICAL RESEARCH   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; BACTERIAL PROTEIN; BETA CAROTENE; DRUG DERIVATIVE; RETINOL; RETINOL PALMITATE;

ARTICLE; CHEMISTRY; CYANOBACTERIUM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOLATION AND PURIFICATION; METABOLISM;

ANTIOXIDANTS; BACTERIAL PROTEINS; BETA CAROTENE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYANOBACTERIA; VITAMIN A;

CYANOBACTERIA; TRICHODESMIUM;

EID: 67649979508     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.01913.x     Document Type: Article

References (77)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215 : 403 410.
2. Anantharaman, V. Aravind, L. (2003) Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol 4 : R11.
3. Andrews, S.S., Caron, S. Zafiriou, O.C. (2000) Photochemical oxygen consumption in marine waters: a major sink for colored dissolved organic matter? Limnol Oceanogr 45 : 267 277. (Pubitemid 30152800)
4. Araujo, K.G.L., Domingues, J.R., Srur, A. da Silva, A.J.R. (2006) Production of antioxidants by Anaboena PCC 7119 and evaluation of their protecting activity against oxidation of soybean oil. Food Biotechnol 20 : 65 77.
5. Asada, K. (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B Biol Sci 355 : 1419 1430.
6. Batten, M.L., Imanishi, Y., Maeda, T., Tu, D.C., Moise, A.R., Bronson, D., et al. (2004) Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J Biol Chem 279 : 10422 10432. (Pubitemid 38372651)
7. Ben-Amotz, A. (1995) Simultaneous profiling and identification of carotenoids, retinols, and tocopherols by high-performance liquid-chromatography equipped with 3-dimensional photodiode-array detection. J Liq Chromatogr 18 : 2813 2825.
8. Ben-Amotz, A. Fishler, R. (1998) Analysis of carotenoids with emphasis on 9-cis beta-carotene in vegetables and fruits commonly consumed in Israel. Food Chem 62 : 515 520. (Pubitemid 28398499)
9. Benzie, I.F.F. Strain, J.J. (1996) The ferric reducing ability of plasma (FRAP) as a measure of 'antioxidant power': the FRAP assay. Anal Biochem 239 : 70 76.
10. Benzie, I.F.F. Strain, J.J. (1999) Ferric reducing antioxidant power assay: Direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Meth Enzymol 299 : 15 27. (Pubitemid 28483878)
11. 2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19 : 139 185.
12. Berman-Frank, I., Lundgren, P., Chen, Y.B., Kupper, H., Kolber, Z., Bergman, B. Falkowski, P. (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294 : 1534 1537. (Pubitemid 33063926)
13. Berman-Frank, I., Bidle, K.D., Haramaty, L. Falkowski, P.G. (2004) The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalysed cell death pathway. Limnol Oceanogr 49 : 997 1005. (Pubitemid 39040337)
14. Berman-Frank, I., Rosenberg, G., Levitan, O., Haramaty, L. Mari, X. (2007) Coupling between autocatalytic cell death and transparent exopolymeric particle production in the marine cyanobacterium Trichodesmium. Environ Microbiol 9 : 1415 1422. (Pubitemid 46763520)
15. Beutner, S., Bloedorn, B., Frixel, S., Blanco, I.H., Hoffmann, T., Martin, H.D., et al. (2001) Quantitative assessment of antioxidant properties of natural colorants and phytochemicals: carotenoids, flavonoids, phenols and indigoids. The role of beta-carotene in antioxidant functions. J Sci Food Agric 81 : 559 568. (Pubitemid 32386131)
16. Blough, N.V. Zepp, R.G. (1995) Reactive oxygen species in natural waters. In Active Oxygen in Chemistry. Foote, C.S., Valentine, J.S., Greenberg, A Liebman, J.F (eds). New York, NY, USA : Blackie Academic and Professional, pp. 280 333.
17. Britton, G. (1995) Structure and properties of carotenoids in relation to function. FASEB J 9 : 1551 1558. (Pubitemid 26012843)
18. Burton, G.W. Ingold, K.U. (1984) Beta-carotene- an unusual type of lipid antioxidant. Science 224 : 569 573. (Pubitemid 14137524)
19. Cahyana, A.H., Shuto, Y. Kinoshita, Y. (1992) Pyropheophytin a as an antioxidative substance from the marine alga, Arame (Eisenia bicyclis). Biosci Biotechnol Biochem 56 : 1533 1535.
20. Capone, D.G., Zehr, J.P., Paerl, H.W., Bergman, B. Carpenter, E.J. (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276 : 1221 1229.
21. Chen, Y.B., Zehr, J.P. Mellon, M. (1996) Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101 in defined media: evidence for a circadian rhythm. J Phycol 32 : 916 923. (Pubitemid 27047802)
22. Chen, Y.B., Dominic, B., Mellon, M.T. Zehr, J.P. (1998) Circadian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous Cyanobacterium Trichodesmium sp. strain IMS101. J Bacteriol 180 : 3598 3605. (Pubitemid 29115089)
23. Chen, Y.B., Dominic, B., Zani, S., Mellon, M.T. Zehr, J.P. (1999) Expression of photosynthesis genes in relation to nitrogen fixation in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101. Plant Mol Biol 41 : 89 104.
24. Conn, P.F., Schalch, W. Truscott, T.G. (1991) The singlet oxygen and carotenoid interaction. J Photochem Photobiol B-Biol 11 : 41 47.
25. Cunningham, K.A. Capone, D.G. (1992) Supoeroxide dismutase as a protective enzyme against oxygen toxicity: an overview and initial studies in Trichodesmium. In Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs. Carpenter, E.J., Capone, D.G. Reuter, J.G (eds). Dordecht, the Netherlands : Kluwer Academic Publishers, pp. 331 341.
26. 2-fixing colonial cyanobacterium Trichodesmium. Science 312 : 1517 1520. (Pubitemid 43865889)
27. Edge, R., McGarvey, D.J. Truscott, T.G. (1997) The carotenoids as anti-oxidants - a review. J Photochem Photobiol B-Biol 41 : 189 200. (Pubitemid 28019766)
28. Eitinger, T. (2004) In vivo production of active nickel superoxide dismutase from Prochlorococcus marinus MIT9313 is dependent on its cognate peptidase. J Bacteriol 186 : 7821 7825. (Pubitemid 39463752)
29. Falkowski, P.G. Raven, J.A. (2007) Aquatic Photosynthesis, 2nd edn. Princeton, NJ, USA : Princeton University Press.
30. Fridovich, I. (1998) Oxygen toxicity: a radical explanation. J Exp Biol 201 : 1203 1209. (Pubitemid 28278324)
31. 2. New Phytol 122 : 71 609.
32. 2 fixation in phototrophs: adaptation to a specialized way of life. Plant Soil 230 : 39 48. (Pubitemid 32320068)
33. Goldman, J.C. McCarthy, J.J. (1978) Steady-state growth and ammonium uptake of a fast-growing marine diatom. Limnol Oceanogr 23 : 695 703.
34. Guillard, R.R.L. (1975) Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrate Animals. Smith, W.L. Chanley, M.H. (eds). New York, NY, USA : Plenum Press, pp. 26 60.
35. Halliwell, B. (1999) Antioxidant defence mechanisms: from the beginning to the end (of the beginning). Free Rad Res 31 : 261 272. (Pubitemid 29452853)
36. Halliwell, B. Gutteridge, J.M.C. (1990) The antioxidants of human extracellular fluids. Arch Biochem Biophys 280 : 1 8. (Pubitemid 20196526)
37. Halliwell, B. Gutteridge, J.M.C. (1995) The definition and measurement of antioxidants in biological systems. Free Rad Biol Med 18 : 125 126.
38. Halliwell, B. Gutteridge, J.M.C. (1999) Free Radicals in Biology and Medicine. Oxford, UK : Oxford University Press.
39. Halvorsen, B.L., Holte, K., Myhrstad, M.C.W., Barikmo, I., Hvattum, E., Remberg, S.F., et al. (2002) A systematic screening of total antioxidants in dietary plants. J Nutr 132 : 461 471. (Pubitemid 34208750)
40. Jahng, W.J., Xue, L.L. Rando, R.R. (2003) Lecithin retinol acyltransferase is a founder member of a novel family of enzymes. Biochemistry 42 : 12805 12812. (Pubitemid 37385811)
41. Kana, T.M. (1992) Oxygen cycling in cyanobacteria with specific reference to oxygen protection in Trichodesmium spp. In Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs. Carpenter, E.J., Capone, D.G. Reuter, J.G. (eds). Dordecht, the Netherlands : Kluwer Academic Publishers, pp. 29 41.
42. Kana, T.M. (1993) Rapid oxygen cycling in Trichodesmium thiebautii. Limnol Oceanogr 38 : 18 24. (Pubitemid 24429281)
43. Kobayashi, M., Kakizono, T., Nishio, N., Nagai, S., Kurimura, Y. Tsuji, Y. (1997) Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Appl Microbiol Biotechnol 48 : 351 356. (Pubitemid 27430085)
44. Kupper, H., Ferimazova, N., Setlik, I. Berman-Frank, I. (2004) Traffic lights in Trichodesmium: regulation of photosynthesis for nitrogen fixation studied by chlorophyll fluorescence kinetic microscopy. Plant Physiol 135 : 2120 2133. (Pubitemid 39182792)
45. Li, H.B., Cheng, K.W., Wong, C.C., Fan, K.W., Chen, F. Jiang, Y. (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102 : 771 776. (Pubitemid 46108280)
46. Liebler, D.C. (1993) Antioxidant reactions of carotenoids. Ann New York Acad Sci 691 : 20 31. (Pubitemid 24099377)
47. Lin, S.J., Henze, S., Lundgren, P., Bergman, B. Carpenter, E.J. (1998) Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Appl Environ Microbiol 64 : 3052 3058. (Pubitemid 28363183)
48. Maeda, H. DellaPenna, D. (2007) Tocopherol functions in photosynthetic organisms. Curr Opin Plant Biol 10 : 260 265. (Pubitemid 46710479)
49. Mallick, N. Mohn, F.H. (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157 : 183 193. (Pubitemid 30656372)
50. Milligan, A.J., Berman-Frank, I., Gerchman, Y., Dismukes, G.C. Falkowski, P.G. (2007) Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection. J Phycol 43 : 845 852. (Pubitemid 47493114)
51. Mondal, M.S., Ruiz, A., Bok, D. Rando, R.R. (2000) Lecithin retinol acyltransferase contains cysteine residues essential for catalysis. Biochemistry 39 : 5215 5220. (Pubitemid 30241644)
52. Nakai, M., Kageyama, N., Nakahara, K. Miki, W. (2006) Phlorotannins as radical scavengers from the extract of Sargassum ringgoldianum. Mar Biotechnol 8 : 409 414. (Pubitemid 44221550)
53. Noctor, G. Foyer, C.H. (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49 : 249 279.
54. Ozben, T. (2007) Oxidative stress and apoptosis: impact on cancer therapy. J Pharm Sci 96 : 2181 2196. (Pubitemid 47477879)
55. Paerl, H.W. Bebout, B.M. (1992) Oxygen dynamics in Trichodesmium spp. aggregates. In Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs. Carpenter, E.J., Capone, D.G. Reuter, J.G. (eds). Dordecht, the Netherlands : Kluwer Academic Publishers, pp. 43 59. (Pubitemid 23405830)
56. Potterat, O. (1997) Antioxidants and free radical scavengers of natural origin. Curr Org Chem 1 : 415 440. (Pubitemid 127681644)
57. Prior, R.L. Cao, G.H. (1999) In vivo total antioxidant capacity: comparison of different analytical methods. Free Rad Biol Med 27 : 1173 1181. (Pubitemid 30001476)
58. Priya, B., Premanandh, J., Dhanalakshmi, R.T., Seethalakshmi, T., Uma, L., Prabaharan, D. Subramanian, G. (2007) Comparative analysis of cyanobacterial superoxide dismutases to discriminate canonical forms. BMC Genomics 8 : 435.
59. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M. Stanier, R.Y. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Genl Microbiol 111 : 1 61. (Pubitemid 9142236)
60. Ruiz, A., Winston, A., Lim, Y.H., Gilbert, B.A., Rando, R.R. Bok, D. (1999) Molecular and biochemical characterization of lecithin retinol acyltransferase. J Biol Chem 274 : 3834 3841. (Pubitemid 29077233)
61. Sanjeev Kumar, P., Vasudevan, D.M. Jayanthi Bai, N. (1981) Antioxidant role of retinyl-palmitate on carbontetrachloride toxicity. Acta Vitaminol Enzymol 3 : 214 218. (Pubitemid 12066592)
62. Schafer, L., Vioque, A. Sandmann, G. (2005) Functional in situ evaluation of photo synthesis-protecting carotenoids in mutants of the cyanobacterium Synechocystis PCC6803. J Photochem Photobiol B-Biol 78 : 195 201. (Pubitemid 40220987)
63. Sies, H. (1991) Oxidative Stress: Oxidants and Antioxidants. London, UK : Academic Press.
64. Sies, H. Stahl, W. (1995) Vitamin-E and vitamin-C, beta-carotene, and other carotenoids as antioxidants. Am J Clin Nutr 62 : S1315 S1321.
65. Son, B.W., Kim, J.C., Choi, H.D. Kang, J.S. (2002) A radical scavenging farnesylhydroquinone from a marine-derived fungus Penicillium sp. Arch Pharmacal Res 25 : 77 79.
66. Soni, B., Trivedi, U. Madamwar, D. (2008) A novel method of single step hydrophobic interaction chromatography for the purification of phycocyanin from Phormidium fragile and its characterization for antioxidant property. Bioresour Technol 99 : 188 194. (Pubitemid 47516653)
67. Starr, R.C. Zeikus, J.A. (1993) UTEX - the culture collection of algae at the University of Texas at Austin 1993 list of cultures. J Phycol 29 : 1 106.
68. Takamatsu, S., Hodges, T.W., Rajbhandari, I., Gerwick, W.H., Hamann, M.T. Nagle, D.G. (2003) Marine natural products as novel antioxidant prototypes. J Nat Prod 66 : 605 608. (Pubitemid 36617880)
69. Telfer, A., Dhami, S., Bishop, S.M., Phillips, D. Barber, J. (1994) Beta-carotene quenches singlet oxygen formed by isolated photosystem-II reaction centers. Biochemistry 33 : 14469 14474.
70. Tesoriere, L., Darpa, D., Re, R. Livrea, M.A. (1997) Antioxidant reactions of all-trans retinol in phospholipid bilayers: effect of oxygen partial pressure, radical fluxes, and retinol concentration. Arch Biochem Biophys 343 : 13 18. (Pubitemid 27274337)
71. Voelker, B.M., Sedlak, D.L. Zafiriou, O.C. (2000) Chemistry of superoxide radical in seawater: reactions with organic Cu complexes. Environ Sci Technol 34 : 1036 1042. (Pubitemid 30155207)
72. Watanabe, N., Yamamoto, K., Ihshikawa, H., Yagi, A., Sakata, K., Brinen, L.S. Clardy, J. (1993) New chlorophyll-a-related compounds isolated as antioxidants from marine bivalves. J Nat Prod 56 : 305 317. (Pubitemid 23104341)
73. Wolfe-Simon, F., Grzebyk, D., Schofield, O. Falkowski, P.G. (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41 : 453 465. (Pubitemid 40832004)
74. Yamamoto, K., Sakata, K., Watanabe, N., Yagi, A., Brinen, L.S. Clardy, J. (1992) Chlorophyllonic acid a methyl-ester, a new chlorophyll-a related compound isolated as an antioxidant from short-necked clam, Ruditapes philippinarum. Tetrahedron Lett 33 : 2587 2588.
75. Yan, X.J., Chuda, Y., Suzuki, M. Nagata, T. (1999) Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed. Biosci Biotechnol Biochem 63 : 605 607. (Pubitemid 129555518)
76. Zhao, W.X., Ye, Z. Zhao, J.D. (2007) RbrA, a cyanobacterial rubrerythrin, functions as a FNR-dependent peroxidase in heterocysts in protection of nitrogenase from damage by hydrogen peroxide in Anabaena sp PCC 7120. Mol Microbiol 66 : 1219 1230. (Pubitemid 350115028)
77. Zolfaghari, R., Wang, Y.P., Chen, Q.Y., Sancher, A. Ross, A.C. (2002) Cloning and molecular expression analysis of large and small lecithin: retinol acyltransferase mRNAs in the liver and other tissues of adult rats. Biochem J 368 : 621 631. (Pubitemid 35454541)