Dimethylsulfoniopropionate metabolism by Pfiesteria-associated Roseobacter spp.

Applied and Environmental Microbiology

Volumn 70, Issue 6, 2004, Pages 3383-3391

  Miller, Todd R ^a   Belas, Robert ^a  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL CULTURE; DEGRADATION; METABOLISM; PHYSIOLOGY;

CATABOLISM; DIMETHYLSULFONIOPROPIONATE (DMSP); MARINE BACTERIA;

MICROBIOLOGY;

3 METHYLMERCAPTOPROPIONATE; ACRYLIC ACID DERIVATIVE; DIMETHYL SULFIDE; DIMETHYLSULFONIOPROPIONATE; METHANETHIOL; PROPIONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

MICROBIOLOGY;

ARTICLE; BACTERIAL STRAIN; BACTERIOPLANKTON; BACTERIUM CULTURE; CATABOLISM; CRYPTOPERIDINIOPSIS; DEMETHYLATION; DINOFLAGELLATE; HYPOTHESIS; MARINE ENVIRONMENT; METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PFIESTERIA; ROSEOBACTER;

ANIMALS; CULTURE MEDIA; DINOFLAGELLIDA; DNA, BACTERIAL; DNA, RIBOSOMAL; ECOSYSTEM; MOLECULAR SEQUENCE DATA; PFIESTERIA PISCICIDA; PHYLOGENY; RNA, RIBOSOMAL, 16S; ROSEOBACTER; SULFONIUM COMPOUNDS;

BACTERIA (MICROORGANISMS); DINOPHYCEAE; PFIESTERIA; PFIESTERIA PISCICIDA; PFIESTERIA SHUMWAYAE; PFIESTERIA-LIKE DINOFLAGELLATE; ROSEOBACTER;

EID: 2942627189     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.6.3383-3391.2004     Document Type: Article

References (47)

1. Alavi, M., T. Miller, K. Erlandson, R. Schneider, and R. Belas. 2001. Bacterial community associated with Pfiesteria-like dinoflagellate cultures. Environ. Microbiol. 3:380-396.
2. Ansede, J., P. J. Pellechia, and D. C. Yoch. 1999. Metabolism of acrylate to β-hydroxypropionate and its role in dimethylsulfoniopropionate lyase induction by a salt marsh sediment bacterium, Alcaligenes faecalis M3A. Appl. Environ. Microbiol. 65:5075-5081.
3. 13C]acrylate metabolism by a DMSP lyase-producing marine isolate of the α-subclass of Proteobacteria. Appl. Environ. Microbiol. 67:3134-3139.
4. Ausubel, F. M. 2001. Current protocols in molecular biology. J. Wiley, New York, N.Y.
5. Berry, J. P., K. S. Reece, K. S. Rein, D. G. Baden, L. W. Haas, W. L. Ribeiro, J. D. Shields, R. V. Snyder, W. K. Volgelbein, and R. E. Gawley. 2002. Are Pfiesteria species toxicogenic? Evidence against production of icthyotoxins by Pfiesteria shumwayae. Proc. Natl. Acad. Sci. USA 99:10970-10975.
6. Burkholder, J. M., E. J. Noga, C. H. Hobbs, H. B. Glasgow, Jr., and S. A. Smith. 1992. New 'phantom' dinoflagellate is the causative agent of major estuarine fish kills. Nature 358:407-410.
7. Chambers, S. T., C. M. Kunin, D. Miller, and A. Hamada. 1987. Dimethylthetin can substitute for glycine betaine as an osmoprotectant molecule for Escherichia coli. J. Bacteriol. 169:4845-4847.
8. Dantzer, W. R., and R. E. Levin. 1997. Bacterial influence on the production of paralytic shellfish toxins by dinoflagellate algae. J. Appl. Microbiol. 83:464-469.
9. Dickson, D. M. J., and G. O. Kirst. 1986. The role of β-dimethylsulfoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformes. Planta 167:536-543.
10. Felsenstein, J. 1989. Phylogeny inference package (version 3.2). Cladistics 5:164-166.
11. Fitch, W. M., and E. Margoliash. 1967. Construction of phylogenetic trees. Science 155:279-284.
12. Gallacher, S., K. J. Flynn, J. M. Franco, E. E. Brueggemann, and H. B. Hines. 1997. Evidence for production of paralytic shellfish toxins by bacteria associated with Alexandrium spp. (Dinophyta) in culture. Appl. Environ. Microbiol. 63:239-245.
13. Glasgow, H. B., Jr., J. M. Burkholder, D. E. Schmechel, P. A. Tester, and P. A. Rublee. 1995. Insidious effects of a toxic estuarine dinoflagellate on fish survival and human health. J. Toxicol. Environ. Health 46:501-522.
14. González, J. M., J. S. Covert, W. B. Whitman, J. R. Henriksen, F. Mayer, B. Scharf, R. Schmitt, A. Buchan, J. A. Fuhrman, R. P. Kiene, and M. A. Moran. 2003. Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., DMSP demethylating bacteria from marine environments. Int. J. Syst. Evol. Microbiol. 53:1261-1269.
15. Gonzalez, J. M., R. P. Kiene, and M. A. Moran. 1999. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria. Appl. Environ. Microbiol. 65:3810-3819.
16. Gonzalez, J. M., and M. A. Moran. 1997. Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl. Environ. Microbiol. 63:4237-4242.
17. Gram, L., H. P. Grossart, A. Schlingloff, and T. Kiorboe. 2002. Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl. Environ. Microbiol. 68:4111-4116.
18. Guillard, R. R. L. 1975. Culture of phytoplankton for feeding marine invertebrates. Plenum Press, New York, N.Y.
19. Hold, G. L., E. A. Smith, M. S. Rappe, E. W. Maas, E. R. B. Moore, C. Stroempl, J. R. Stephen, J. I. Prosser, T. H. Birkbeck, and S. Gallacher. 2001. Characterisation of bacterial communities associated with toxic and non-toxic dinoflagellates: Alexandrium spp. and Scrippsiella trochoidea. FEMS Microbiol. Ecol. 37:161-173.
20. Jansen, M., and T. A. Hansen. 2001. Non-growth-associated demethylation of dimethylsulfoniopropionate by (homo)acetogenic bacteria. Appl. Environ. Microbiol. 67:300-306.
21. Jansen, M., and T. A. Hansen. 1998. Tetrahydrofolate serves as a methyl acceptor in the demethylation of dimethylsulfoniopropionate in cell extracts of sulfate-reducing bacteria. Arch. Microbiol. 169:84-87.
22. Jukes, T. H., and C. R. Cantor. 1969. Evolution of protein molecules, p. 21-132. In H. N. Munro (ed.), Mammalian protein metabolism. Academic Press, New York, N.Y.
23. Karsten, U., K. Kuck, C. Vogt, and G. O. Kirst. 1996. Dimethylsulfoniopropionate production in phototrophic organisms and its physiological function as a cryoprotectant, p. 143-153. In R. P. Kiene, P. T. Visscher, M. D. Keller, and G. O. Kirst (ed.), Biological and environmental chemistry of DMSP and related sulfonium compounds. Plenum Press, New York, N.Y.
24. Keller, M. D., and W. Korjeff-Bellows. 1996. Physiological aspects of the production of dimethylsulfoniopropionate (DMSP) by marine phytoplankton, p. 131-153. In R. P. Kiene, P. T. Visscher, M. D. Keller, and G. O. Kirst (ed.), Biological and environmental chemistry of DMSP and related sulfonium compounds. Plenum Press, New York, N.Y.
25. Kiene, R. P. 1996. Production of methanethiol from dimethylsulfoniopropionate in marine surface waters. Mar. Chem. 54:69-83.
26. Kiene, R. P., and L. J. Linn. 2000. Distribution and turnover of dissolved DMSP and its relationship with bacterial production and dimethylsulfide in the Gulf of Mexico. Limnol. Oceanogr. 45:849-861.
27. Kiene, R. P., L. J. Linn, J. Gonzalez, M. A. Moran, and J. A. Bruton. 1999. Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl. Environ. Microbiol. 65:4549-4558.
28. Kitaguchi, H., A. Uchida, and Y. Ishida. 1999. Purification and characterization of L-methionine decarboxylase from Crypthecodinium cohnii. Fisheries Sci. 65:613-617.
29. Kluge, A. G., and F. S. Farris. 1969. Quantitative phyletics and the evolution of annurans. Syst. Zool. 18:1-32.
30. Lafay, B., R. Ruimy, C. R. de Traubenberg, V. Breittmayer, M. J. Gauthier, and R. Christen. 1995. Roseobacter algicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflagellate Prorocentrum lima. Int. J. Syst. Bacteriol. 45:290-296.
31. Miller, T. R., and R. Belas. 2003. Pfiesteria piscicida, P. shumwayae, and other Pfiesteria-like dinoflagellates. Res. Microbiol. 154:85-90.
32. Moeller, P. D., S. L. Morton, B. A. Mitchell, S. K. Sivertsen, E. R. Fairey, T. M. Mikulski, H. Glasgow, N. J. Deamer-Melia, J. M. Burkholder, and J. S. Ramsdell. 2001. Current progress in isolation and characterization of toxins isolated from Pfiesteria piscicida. Environ. Health Perspect. 109:739-743.
33. Niki, T., M. Kunugi, and A. Otsuki. 2000. DMSP-lyase activity in five marine phytoplankton species: its potential importance in DMS production. Mar. Biol. 136:759-764.
34. Osinga, R., K. de Vries, W. Lewis, W. van Raaphorst, L. Dijkhuizen, and F. van Duyl. 1997. Aerobic degradation of phytoplankton debris dominated by Phaeocystis sp. in different physiological stages of growth. Aquat. Microb. Ecol. 12:11-19.
35. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
36. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
37. Sunda, W., D. J. Kieber, R. P. Kiene, and S. Huntsman. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418:317-320.
38. Taylor, B. F., and D. Gilchrist. 1991. New routes for aerobic biodegradation of dimethylsulfoniopropionate. Appl. Environ. Microbiol. 57:3581-3584.
39. Taylor, B. F., and P. T. Visscher. 1996. Metabolic pathways involved in DMSP degradation, p. 265-276. In R. P. Kiene, P. T. Visscher, M. D. Keller, and G. O. Kirst (ed.), Biological and environmental chemistry of DMSP and related sulfonium compounds. Plenum Press, New York, N.Y.
40. Vairavamurthy, A., M. O. Andreae, and R. L. Iverson. 1985. Biosynthesis of dimethylsulfide and dimethylpropiothetin by Hymenemonas carterae in relation to sulfur source. Limnol. Oceanogr. 30:59-70.
41. Visscher, P. T., and B. F. Taylor. 1994. Demethylation of dimethylsulfoniopropionate to 3-mercaptopropionate by an aerobic marine bacterium. Appl. Environ. Microbiol. 60:4617-4619.
42. Visscher, P. T., B. F. Taylor, and R. P. Kiene. 1995. Microbial consumption of dimethyl sulfide and methanethiol in marine coastal sediments. FEMS Microbiol. Ecol. 18:145-154.
43. Vogelbein, W. K., V. J. Lovko, J. D. Shields, K. S. Reece, P. L. Mason, L. W. Haas, and C. C. Walker. 2002. Pfiesteria shumwayae kills fish by micropredation not exotoxin secretion. Nature 418:967-970.
44. Wolfe, G., M. Steinke, and G. Kirst. 1997. Grazing-activated chemical defence in a unicellular marine alga. Nature 387:894-897.
45. Yoch, D. C. 2002. Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl. Environ. Microbiol. 68:5804-5815.
46. Yoch, D. C., J. H. Ansede, and K. S. Rabinowitz. 1997. Evidence for intracellular and extracellular dimethylsulfoniopropionate (DMSP) lyases and DMSP uptake sites in two species of marine bacteria. Appl. Environ. Microbiol. 63:3182-3188.
47. Zubkov, M. V., B. M. Fuchs, S. D. Archer, R. P. Kiene, R. Amann, and P. H. Burkill. 2001. Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulphoniopropionate in an algal bloom in the North Sea. Environ. Microb. 3:304-311.