Effects of iron and light stress on the biochemical composition of antarctic Phaeocystis sp. (Prymnesiophyceae). I. Intracellular DMSP concentrations

Journal of Phycology

Volumn 34, Issue 3, 1998, Pages 486-495

  Stefels, Jacqueline ^a   Van Leeuwe, Maria A ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

Antarctic Phaeocystis; Biochemical composition; Dimethylsulfoniopropionate; DMSP; Iron; Light

Indexed keywords

BACTERIA (MICROORGANISMS); HAPTOPHYCEAE; PHAEOCYSTIS;

EID: 0031869876     PISSN: 00223646     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1529-8817.1998.340486.x     Document Type: Article

References (74)

1. Andreae, M. O. 1990. Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Mar. Chem. 30:1-29.
2. Bates, T. S., Cline, J. D., Gammon, R. H. & Kelly-Hansen, S. R. 1987. Regional and seasonal variation in the flux of oceanic dimethylsulfide to the atmosphere. J. Geophys. Res. 92:2930-8.
3. Bates, T. S., Lamb, B. K., Guenther, A., Dignon, J. & Stoiber, R. E. 1992. Sulfur emissions to the atmosphere from natural sources. J. Atmos. Chem. 14:315-37.
4. Baumann, M. E. M., Lancelot, C., Brandini, F. P., Sakshaug, E. & John, D. M. 1994. The taxonomic identity of the cosmopolitan prymnesiophyte Phaeocystis: a morphological and ecophysiological approach. In Lancelot, C. & Wassmann, P. [Eds.] Ecology of Phaeocystis-dominated Ecosystems. J. Mar. Syst. 5: 5-22.
5. Buma, A. G. J., Bano, N., Veldhuis, M. J. W. & Kraay, G. W. 1991a. Comparison of the pigmentation of two strains of the Prymnesiophyte Phaeocystis sp. Neth. J. Sea Res. 27:173-82.
6. Buma, A. G. J., de Baar, H. J. W., Nolting, R. F. & van Bennekom, A. J. 1991b. Metal enrichment experiments in the Weddell-Scotia Seas: effects of iron and manganese on various plankton communities. Limnol. Oceanogr. 36:1865-78.
7. Buma, A. G. J., Noordeloos, A. A. M. & Larsen, J. 1993. Strategies and kinetics of photoacclimation in three Antarctic nanophytoflagellates. J. Phycol. 29:407-17.
8. Charlson, R. J., Lovelock, J. E., Andreae, M. O. & Warren, S. G. 1987. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655-61.
9. Choi, J. W. & Stoecker, D. K. 1989. Effects of fixation on cell volume of marine planktonic protozoa. Appl. Environ. Mirrobiol. 55:1761-5.
10. Crocker, K. M., Ondrusek, M. E., Petty, R. L. & Smith, R. C. 1995. Dimethylsulfide, algal pigments and light in an Antarctic Phaeocystis sp. bloom. Mar. Biol 124:335-40.
11. Dacey, J. W. H. & Blough, N. 1987. Hydroxide decomposition of dimethylsulfoniopropionate to form dimethylsulfide. Geophys. Res. Lett. 14:1246-9.
12. Dacey, J. W. H., King, G. M. & Wakeham, S. G. 1987. Factors controlling emission of dimethylsulphide from salt marshes. Nature 330:643-5.
13. de Baar, H. J. W., de Jong, J. T. M., Bakker, D. C. E., Loscher, B. M., Veth, C., Bathmann, U. & Smetacek, V. 1995. Importance of iron for plankton blooms and carbon dioxide drawdown in the Southern Ocean. Nature 373:412-5.
14. Dickson, D. M. J. & Kirst, G. O. 1986. The role of ß-dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta 167:536-43.
15. _ 1987a. Osmotic adjustment in marine eukaryotic algae: the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. I. Diatoms and a Rhodophyte. New Phytol. 106:645-55.
16. _ 1987b. Osmotic adjustment in marine eukaryotic algae: the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. II. Prasinophytes and Haptophytes. New Phytol. 106:657-66.
17. DiTullio, G. R. & Smith, W. O. J. 1995. Relationship between dimethylsulfide and phytoplankton pigment concentrations in the Ross Sea, Antarctica. Deep-Sea Res. 42:873-92.
18. Doucette. G. J. & Harrison, P. J. 1991. Aspects of iron and nitrogen nutrition in the red tide dinoflagellate Gymnodinium sanguine-urn. I. Effects of iron depletion and nitrogen source on biochemical composition. Mar. Biol. 110:165-73.
19. Falkowski, P. G., Dubinsky, Z. & Wyman, K. 1985. Growth-irradiance relationships in phytoplankton. Limnol. Oceanogr. 30: 311-21.
20. Gage, D. A., Rhodes, D., Nolte, K. D., Hicks, W. A., Leustek, T., Cooper, A. J. L. & Hanson, A. D. 1997. A new route for synthesis of dimethylsulphoniopropionate in marine algae. Nature 387:891-4.
21. Geider, R. J. & LaRoche, J. 1994. The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosyn. Res. 39:275-301.
22. Geider, R. J., LaRoche, J., Greene, R. M. & Olaizola, M. 1993. Response of photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J. Phycol. 29:755-66.
23. Gibson, J. A. E., Garrick, R. C., Burton, H. R. & McTaggart, A. R. 1989. Dimethylsulfide concentrations in the ocean close to the Antarctic continent. Geomicrobiol. J. 6:179-84.
24. _ 1990. Dimethylsulfide and the alga Phaeocystis pouchetii in antarctic coastal waters. Mar. Biol. 104:339-46.
25. Greene, R. C. 1962. Biosynthesis of dimethyl-β-propiothetin. J. Biol. Chem. 237:2251-4.
26. Greene, R. M., Geider. R. J. & Falkowski, P. G. 1991. Effect of iron limitation on photosynthesis in a marine diatom. Limnol. Oceanogr. 36:1772-82.
27. Greene, R. M., Geider, R. J., Kolber. Z. & Falkowski, P. G. 1992. Iron-induced changes in light harvesting and photochemical energy conversion processes in eukaryotic marine algae. Plant Physiol. 100:565-75.
28. Greene, R. M., Kolber, Z. S., Swift, D. G., Tindale, N. W. & Falkowski, P. G. 1994. Physiological limitation of phytoplankton photosynthesis in the eastern equatorial Pacific determined from variability in the quantum yield of fluorescence. Limnol. Oceanogr. 39:1061-74.
29. Gröne, T. & Kirst. G. O. 1991. Aspects of dimethylsulfoniopropionate effects on enzymes isolated from the marine phytoplankter Tetraselmis subcordiformis (Stein). J. Plant Physiol. 138: 85-91.
30. _ 1992. The effect of nitrogen deficiency, methionine and inhibitors of methionine metabolism on the DMSP contents of Tetraselmis subcordiformis (Stein). Mar. Biol. 112:497-503.
31. Herzig, R. & Falkowski, P. G. 1989. Nitrogen limitation in Isochrysis galbana (Haptophyceae). I. Photosynthetic energy conversion and growth efficiencies. J. Phycol. 25:462-71.
32. Hudson, R. J. & Morel, F. M. M. 1993. Trace metal transport by marine microorganisms: implications of metal coordination kinetics. Deep-Sea Res. 40:129-50.
33. Huppe, H. C. & Turpin, D. H. 1994. Integration of carbon and nitrogen metabolism in plant and algal cells. Annu. Rev. Plant Physiol. Plant Mol. Bial. 45:577-607.
34. + by a green alga. Plant Physiol. 100:2096-9.
35. Rarsten. U., Kück, K., Vogt, C. & Kirst, G. O. 1996. Dimethylsulfoniopropionate production in phototrophic organisms and its physiological function as a cryoprotectant. In Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O. [Eds.] Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds. Plenum Press, New York, pp. 143-53.
36. Karsten, U., Wiencke, C. & Kirst, G. O. 1991. Growth pattern and ß-dimethylsulphoniopropionate (DMSP) content of green macroalgae at different irradiance. Mar. Biol. 108:151-5.
37. _ 1992. Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biol. 12:603-7.
38. Keller, M. D., Bellows, W. K. & Guillard, R. R. L. 1989. Dimethyl sulfide production in marine phytoplankton. In Saltzman, E. S. & Cooper, W. J. [Eds.] Biogenic Sulfur in the Environment. American Chemical Society, Washington, D.C., pp. 167-82.
39. Kirst, G. O., Thiel, C., Wolff, H., Nothnagel, J., Wanzek, M. & Ulmke, R. 1991. Dimethylsulfoniopropionate (DMSP) in icealgae and its possible biological role. Mar. Chem. 35:381-8.
40. Kolber, Z., Zehr, J. & Falkowski, P. 1988. Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol. 88:923-9.
41. Kolber, Z. S., Barber, R. T., Coale, K. H., Fitzwater, S. E., Greene, R. M., Johnson, K. S., Lindley, S. & Falkowski, P. G. 1994. Iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 371:145-9.
42. Konopka, A. & Schnur, M. 1981. Biochemical composition and photosynthetic carbon metabolism of nutrient limited cultures of Merismopedia tenuissima (Cyanophyceae). J. Phycol. 17: 118-22.
43. Kudo, I. & Harrison, P. J. 1997. Effect of iron nutrition on the marine cyanobacterium Synechococcus grown on different N sources and irradiances. J. Phycol. 33:232-40.
44. Lapointe, B. E. & Duke. C. S. 1984. Biochemical strategies for growth of Gracilaria tikvahiae (Rhodophyta) in relation to light intensity and nitrogen availability. J. Phycol. 20:488-95.
45. LaRoche. J., Geider, R. J., Graziano, L. M., Murray, H. & Lewis, K. 1993. Induction of specific proteins in eukaryotic algae grown under iron-, phosphorus-, or nitrogen-deficient conditions. J. Phycol. 29:767-77.
46. Maldonado. M. T. & Price, N. M. 1996. Influence of N substrate on Fe requirements of marine centric diatoms. Mar. Ecol. Prog. Ser: 141:161-72.
47. Martin. J. H., Coale, K. H., Johnson, K. S., Fitzwater, S. E., Gordon, R. M., Tanner, S. J., Hunter, C. N., Elrod, V. A., Nowicki, J. L., Coley, T. L., Barber, R. T., Lindley, S., Watson, A. J., Van Scoy, K., Law, C. S., Liddicoat, M. I., Ling. R., Stanton, T., Stockel, J., Collins, C., Anderson, A., Bidigare, R., Ondrusek, M., Latasa, M., Millero, F. J., Lee, K., Yao, W., Zhang, J. Z., Friederich, G., Sakamoto, C., Chavez, F., Buck. K., Kolber, Z., Greene, R., Falkowski, P., Chisholm, S. W., Hoge, F., Swift, R., Yungel, J., Turner, S., Nightingale, P., Hatton. A., Liss, P. & Tindale, N. W. 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371:123-9.
48. Martin, J. H. & Fitzwater, S. E. 1988. Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic, Nature 331:341-3.
49. Martin, J. H., Gordon, R. M. & Fitzwater, S. E. 1990. Iron in Antarctic waters. Nature 345:156-8.
50. Medlin, L. K., Lange, M. & Baumann, M. E. M. 1994. Genetic differentiation among three colony-forming species of Phaeocystis: further evidence for the phylogeny of the Prymnesiophyta. Phycologia 33:199-212.
51. Morel, F. M. M., Rueter, J. G., Anderson, D. M. & Guillard, R. R. L. 1979. AQUIL: a chemically defined phytoplankton culture medium for trace metal studies. J. Phycol. 15:135-41.
52. Muggli, D. L. & Harrison, P. J. 1996. Effects of nitrogen source on the physiology and metal nutrition of Emiliania huxleyi grown under different iron and light conditions. Mar. Ecol Prog. Ser. 130:255-67.
53. Muggli, D. L., Lecourt, M. & Harrison, P. J. 1996. Effects of iron and nitrogen source on the sinking rate, physiology and metal composition of an oceanic diatom from the subarctic Pacific. Mar. Ecol. Prog. Ser. 132:215-27.
54. Nolting, R. F. & de Jong, J. T. M. 1994. Sampling and analytical methods for the determination of trace metals in surface sea-water. Int. J. Environ. Anal. Chem. 57:189-96.
55. Palmisano, A. C., SooHoo, J. B., SooHoo, S. L., Kottmeier, S. T., Craft, L. L. & Sullivan, C. W. 1986. Photoadaptation in Phaeocystis pouchetii advected beneath annual sea ice in McMurdo Sound, Antarctica. J. Plankton Res. 8:891-906.
56. Pascal, N. & Douce, R. 1993. Effect of iron deficiency on the respiration of sycamore (Acer pseudoplatanus L.) cells. Plant Physiol. 103:1329-38.
57. Raven, J. A. 1990. Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway. New Phytol. 116:1-18.
58. Rueter, J. G. & Ades, D. R. 1987. The role of iron nutrition in photosynthesis and nitrogen assimilation in Scenedesmus quadricauda (Chlorophyceae). J. Phycol. 23:452-7.
59. Stefels, J. & Dijkhuizen, L. 1996. Characteristics of DMSP-lyase in Phaeocystis sp. (Prymnesiophyceae). Mar. Ecol. Prog. Ser. 131:307-13.
60. Stefels, J. & van Boekel, W. H. M. 1993. Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Mar. Ecol. Prog. Ser. 97:11-8.
61. Stoecker, D. K., Putt, M. & Moisan, T. 1995. Nano-and micro-plankton dynamics during the spring Phaeocystis sp. bloom in McMurdo Sound, Antarctica. J. Mar. Biol. Assoc. U.K. 75:815-32.
62. Sunda, W. G. & Huntsman, S. A. 1997. Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390:389-92.
63. Tarrasón, L., Turner, S. & Fløisand, I. 1995. Estimation of seasonal dimethyl sulphide fluxes over the North Atlantic Ocean and their contribution to European pollution levels. J. Geophys. Res. 100:11.623-39.
64. Thompson, P. A., Harrison, P. J. & Parslow, J. S. 1991. Influence of irradiance on cell volume and carbon quota for ten species of marine phytoplankton. J. Phycol. 27:351-60.
65. Thompson, P. A., Levasseur, M. E. & Harrison, P. J. 1989. Light-limited growth on ammonium vs. nitrate: what is the advantage for marine phytoplankton? Limnol. Oceanogr. 34:1014-24.
66. Turner, S. M., Malin, G., Liss, P. S., Harbour, D. S. & Holligan, P. M. 1988. The seasonal variation of dimethylsulfoniopropionate concentrations in near-shore waters. Limnol. Oteanogr. 33:364-75.
67. Turner, S. M., Nightingale, P. D., Broadgate, W. & Liss, P. S. 1995. The distribution of dimethyl sulphide and dimethylsulphoniopropionate in Antarctic waters and sea ice. Deep-Sea Res. 42:1059-80.
68. Turpin, D. H. 1991. Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J. Phycol. 27:14-20.
69. Vairavamurthy, A., Andreae, M. O. & Iverson, R. L. 1985. Biosynthesis of dimethyl sulfide and dimethylpropiothetin by Hymenomonas carterae in relation to sulfur source and salinity variations. Limnol. Oceanogr. 30:59-70.
70. van Leeuwe, M. A., Scharek, R., de Baar, H. J. W., de Jong, J. T. M. & Goeyens, L. 1997. Iron enrichment experiments in the Southern Ocean: physiological responses of plankton communities. Deep-Sea Res. II 44:189-207.
71. van Leeuwe, M. A. & Stefels, J. 1998. Effects of iron and light stress on the biochemical composition of Antarctic Phaeocystis sp. (Prymnesiophyceae). II. Pigment composition. J. Phycol. 34:496-503.
72. Verity, P. G., Robertson. C. Y., Tronzo, C. R., Andrews, M. G., Nelson, J. R. & Sieracki. M. E. 1992. Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol. Oceanogr. 37:1434-46.
73. Verstreate, D. R., Storch, T. A. & Dunham, V. L. 1980. A comparison of the influence of iron on the growth and nitrate metabolism of Anabaena and Scenedesmus. Physiol. Plant. 50: 47-51.
74. Zhuang, G., Yi, Z., Duce, R. A. & Brown, P. R. 1992. Link between iron and sulphur cycles suggested by detection of Fe(II) in remote marine aerosols. Nature 355:537-9.