Abstract
The 3-dimethylsulphoniopropionate (DMSP) produced by marine algae is the main biogenic precursor of atmospheric dimethylsulphide (DMS)1,2,3. This biogenic DMS, formed by bacterial and algal degradation of DMSP4,5, contributes about 1.5 × 1013 g of sulphur to the atmosphere annually3, and plays a major part in the global sulphur cycle, in cloud formation and potentially in climate regulation1,3. Although DMSP biosynthesis has been partially elucidated in a higher plant6,7, nothing is known about how algae make DMSP except that the whole molecule is derived from methionine8,9,10,11,12. Here we use in vivo isotope labelling to demonstrate that DMSP synthesis in the green macroalga Enteromorpha intestinalis proceeds by a route entirely distinct from that in higher plants. From methionine, the steps are transamination, reduction and S -methylation to give the novel sulphonium compound 4-dimethylsulphonio-2-hydroxybutyrate (DMSHB), which is oxidatively decarboxylated to DMSP. The key intermediate DMSHB was also identified in three diverse phytoplankton species, indicating that the same pathway operates in other algal classes that are important sources of DMS. The fact that a transamination initiates this pathway could help explain how algal DMSP (and thereby DMS) production is enhanced by nitrogen deficiency12.
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References
Charlson, R. J., Lovelock, J. E., Andreae, M. O. & Warren, S. G. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326, 655–661 (1987).
Keller, M. D., Bellows, W. K. & Guillard, R. R. L. in Biogenic Sulfur in the Environment (eds Saltzmann, E. S. & Cooper, W. J.) 167–182 (American Chemical Society, Washington, DC, (1989)).
Malin, G. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) 177–189 (Plenum, New York, (1996).
Stefels, J. & van Boekel, W. H. M. Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Mar. Ecol. Progr. Ser. 97, 11–18 (1993).
Ledyard, K. M. & Dacey, J. W. H. Dimethylsulfide production from dimethylsulfoniopropionate by a marine bacterium. Mar. Ecol. Progr. Ser. 110, 95–103 (1994).
Hanson, A. D., Rivoal, J., Paquet, L. & Gage, D. A. Biosynthesis of 3-dimethylsulfoniopropionate in Wollastonia biflora (L.) DC. Evidence that S -methylmethionine is an intermediate. Plant Physiol. 105, 103–110 (1994).
James, F., Paquet, L., Sparace, S. A., Gage, D. A. & Hanson, A. D. Evidence implicating dimethylsulfoniopropionaldehyde as an intermediate in dimethylsulfoniopropionate biosynthesis. Plant Physiol. 108, 1439–1448 (1995).
Greene, R. C. Biosynthesis of dimethyl-β-propiothetin. J. Biol. Chem. 237, 2251–2254 (1962).
Pokorny, M., Marcenko, E. & Keglevic, D. Comparative studies of L- and D-methionine metabolism in lower and higher plants. Phytochemistry 9, 2175–2188 (1970).
Chillemi, R., Patti, A., Morrone, R., Piatelli, M. & Sciuto, S. The role of methylsulfonium compounds in the biosynthesis of N -methylated metabolites in Chondria coerulescens. J. Nat. Prod. 53, 87–93 (1990).
Uchida, A., Ooguri, T., Ishida, T., Kitaguchi, H. & Ishida, Y. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) 97–107 (Plenum, New York, (1996)).
Kirst, G. O. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) 121–129 (Plenum, New York, (1996)).
Blunden, G. & Gordon, S. M. Betaines and their sulphonio analogues in marine algae. Progr. Phycol. Res. 4, 39–80 (1986).
Mayer, R. R., Cherry, J. H. & Rhodes, D. Effects of heat shock on amino acid metabolism of cowpea cells. Plant Physiol. 94, 796–810 (1990).
Walters, D. S. & Steffens, J. C. Branched chain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucose esters. Plant Physiol. 93, 1544–1551 (1990).
Livesey, G. Methionine degradation: anabolic and catabolic. Trends Biochem. Sci. 9, 27–29 (1984).
Scislowski, W. D., Hokland, B. M., Davis-van Thienen, W. I. A., Bremer, J. & Davis, E. J. Methionine metabolism by rat muscle and other tissues. Biochem. J. 247, 35–40 (1987).
Dibner, J. J. & Knight, C. D. Conversion of 2-hydroxy-4-(methylthio)butanoic acid to L-methionine in the chick: a stereospecific pathway. J. Nutr. 114, 1716–1723 (1984).
Mizayaki, H. H. & Yang, S. F. Metabolism of 5-methylthioribose to methionine. Plant Physiol. 84, 277–281 (1987).
Walsh, C. Enzymatic Reaction Mechanisms (Freeman, New York, (1979)).
Miflin, B. J. & Lea, P. J. Amino acid metabolism. Annu. Rev. Plant Physiol. 28, 299–329 (1977).
Christen, P. & Metzler, D. E. Transaminases (Wiley, New York, (1985)).
Groene, T. Biogenic production and consumption of dimethylsulfide (DMS) and dimethylsulfoniopropionate (DMSP) in the marine epipelagic zone: a review. J. Mar. Syst. 6, 191–209 (1995).
Gooday, G. W. Aphysiological comparison of the symbiotic alga Platymonas convolutae and its free-living relatives. J. Mar. Biol. Assoc. UK 50, 199–208 (1970).
Guillard, R. R. L. & Ryther, J. H. Studies on marine planktonic diatoms I. Cyclotella nana Hustedt and Detulona confervacae (Cleve.) Gran. Can. J. Microbiol. 8, 229–239 (1962).
James, F., Nolte, K. D. & Hanson, A. D. Purification and properties of S -adenosyl-L-methionine:L-methionine S -methyltransferase from Wollastonia biflora leaves. J. Biol. Chem. 270, 22344–22350 (1995).
Lavine, T. F., Floyd, N. F. & Cammaroti, M. S. The formation of sulfonium salts from alcohols and methionine in sulfuric acid. J. Biol. Chem. 207, 107–117 (1954).
Zappia, V., Zydek-Cwick, C. R. & Schlenk, F. The specificity of S -adenosylmethionine derivatives in methyl transfer reactions. J. Biol. Chem. 244, 4499–4509 (1969).
Gage, D. A. & Hanson, A. D. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) 29–44 (Plenum, New York, (1996)).
Huang, Z.-H. et al. Characterization of N -ethoxycarbonyl ethyl esters of amino acids by mass spectrometry. J. Chromatogr. 635, 271–281 (1993).
Acknowledgements
We thank J. Hellebust, O. Schofield and J. S. Davis for algal material. This work was supported by grants from the NSF and ONR to A.D.H. and D.A.G., from the ONR to D.R. and T.L., from the NIH to the MSU-NIH Mass Spectrometry Facility and by the C.V. Griffin Sr Foundation. (Florida Agricultural Experiment Station journal series no. R-05740.)
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Gage, D., Rhodes, D., Nolte, K. et al. A new route for synthesis of dimethylsulphoniopropionate in marine algae. Nature 387, 891–894 (1997). https://doi.org/10.1038/43160
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DOI: https://doi.org/10.1038/43160
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