Previous Article | Next Article 
Applied and Environmental Microbiology, June 2004, p. 3383-3391, Vol. 70, No. 6
0099-2240/04/$08.00+0 DOI: 10.1128/AEM.70.6.3383-3391.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
Dimethylsulfoniopropionate Metabolism by Pfiesteria-Associated Roseobacter spp.
Todd R. Miller and Robert Belas*
Center of Marine Biotechnology, University of Maryland Biotechnology Institute, Baltimore, Maryland 21202
Received 25 August 2003/
Accepted 5 March 2004
The Roseobacter clade of marine bacteria is often found associated with dinoflagellates, one of the major producers of dimethylsulfoniopropionate (DMSP). In this study, we tested the hypothesis that Roseobacter species have developed a physiological relationship with DMSP-producing dinoflagellates mediated by the metabolism of DMSP. DMSP was measured in Pfiesteria and Pfiesteria-like (Cryptoperidiniopsis) dinoflagellates, and the identities and metabolic potentials of the associated Roseobacter species to degrade DMSP were determined. Both Pfiesteria piscicida and Pfiesteria shumwayae produce DMSP with an average intracellular concentration of 3.8 µM. Cultures of P. piscicida or Cryptoperidiniopsis sp. that included both the dinoflagellates and their associated bacteria rapidly catabolized 200 µM DMSP (within 30 h), and the rate of catabolism was much higher for P. piscicida cultures than for P. shumwayae cultures. The community of bacteria from P. piscicida and Cryptoperidiniopsis cultures degraded DMSP with the production of dimethylsulfide (DMS) and acrylate, followed by 3-methylmercaptopropionate (MMPA) and methanethiol (MeSH). Four DMSP-degrading bacteria were isolated from the P. piscicida cultures and found to be taxonomically related to Roseobacter species. All four isolates produced MMPA from DMSP. Two of the strains also produced MeSH and DMS, indicating that they are capable of utilizing both the lyase and demethylation pathways. The diverse metabolism of DMSP by the dinoflagellate-associated Roseobacter spp. offers evidence consistent with a hypothesis that these bacteria benefit from association with DMSP-producing dinoflagellates.
* Corresponding author. Mailing address: Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 East Pratt St., Baltimore, MD 21202. Phone: (410) 234-8876. Fax: (410) 234-8896. E-mail: belas{at}umbi.umd.edu.
This is COMB publication number O4-649 and ECOHAB publication number 121.
Applied and Environmental Microbiology, June 2004, p. 3383-3391, Vol. 70, No. 6
0099-2240/04/$08.00+0 DOI: 10.1128/AEM.70.6.3383-3391.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Porsby, C. H., Nielsen, K. F., Gram, L.
(2008). Phaeobacter and Ruegeria Species of the Roseobacter Clade Colonize Separate Niches in a Danish Turbot (Scophthalmus maximus)-Rearing Farm and Antagonize Vibrio anguillarum under Different Growth Conditions. Appl. Environ. Microbiol.
74: 7356-7364
[Abstract]
[Full Text]
-
Geng, H., Bruhn, J. B., Nielsen, K. F., Gram, L., Belas, R.
(2008). Genetic Dissection of Tropodithietic Acid Biosynthesis by Marine Roseobacters. Appl. Environ. Microbiol.
74: 1535-1545
[Abstract]
[Full Text]
-
Moran, M. A., Belas, R., Schell, M. A., Gonzalez, J. M., Sun, F., Sun, S., Binder, B. J., Edmonds, J., Ye, W., Orcutt, B., Howard, E. C., Meile, C., Palefsky, W., Goesmann, A., Ren, Q., Paulsen, I., Ulrich, L. E., Thompson, L. S., Saunders, E., Buchan, A.
(2007). Ecological Genomics of Marine Roseobacters. Appl. Environ. Microbiol.
73: 4559-4569
[Abstract]
[Full Text]
-
Todd, J. D., Rogers, R., Li, Y. G., Wexler, M., Bond, P. L., Sun, L., Curson, A. R. J., Malin, G., Steinke, M., Johnston, A. W. B.
(2007). Structural and Regulatory Genes Required to Make the Gas Dimethyl Sulfide in Bacteria. Science
315: 666-669
[Abstract]
[Full Text]
-
Bruhn, J. B., Gram, L., Belas, R.
(2007). Production of Antibacterial Compounds and Biofilm Formation by Roseobacter Species Are Influenced by Culture Conditions. Appl. Environ. Microbiol.
73: 442-450
[Abstract]
[Full Text]
-
Howard, E. C., Henriksen, J. R., Buchan, A., Reisch, C. R., Burgmann, H., Welsh, R., Ye, W., Gonzalez, J. M., Mace, K., Joye, S. B., Kiene, R. P., Whitman, W. B., Moran, M. A.
(2006). Bacterial taxa that limit sulfur flux from the ocean.. Science
314: 649-652
[Abstract]
[Full Text]
-
Rao, D., Webb, J. S., Kjelleberg, S.
(2006). Microbial Colonization and Competition on the Marine Alga Ulva australis. Appl. Environ. Microbiol.
72: 5547-5555
[Abstract]
[Full Text]
-
Chen, F., Wang, K., Stewart, J., Belas, R.
(2006). Induction of multiple prophages from a marine bacterium: a genomic approach.. Appl. Environ. Microbiol.
72: 4995-5001
[Abstract]
[Full Text]
-
Hansel, C. M., Francis, C. A.
(2006). Coupled Photochemical and Enzymatic Mn(II) Oxidation Pathways of a Planktonic Roseobacter-Like Bacterium.. Appl. Environ. Microbiol.
72: 3543-3549
[Abstract]
[Full Text]
-
Bruhn, J. B., Nielsen, K. F., Hjelm, M., Hansen, M., Bresciani, J., Schulz, S., Gram, L.
(2005). Ecology, Inhibitory Activity, and Morphogenesis of a Marine Antagonistic Bacterium Belonging to the Roseobacter Clade. Appl. Environ. Microbiol.
71: 7263-7270
[Abstract]
[Full Text]
-
Buchan, A., Gonzalez, J. M., Moran, M. A.
(2005). Overview of the Marine Roseobacter Lineage. Appl. Environ. Microbiol.
71: 5665-5677
[Full Text]
-
Jasti, S., Sieracki, M. E., Poulton, N. J., Giewat, M. W., Rooney-Varga, J. N.
(2005). Phylogenetic Diversity and Specificity of Bacteria Closely Associated with Alexandrium spp. and Other Phytoplankton. Appl. Environ. Microbiol.
71: 3483-3494
[Abstract]
[Full Text]
-
Muller, J. A., DasSarma, S.
(2005). Genomic Analysis of Anaerobic Respiration in the Archaeon Halobacterium sp. Strain NRC-1: Dimethyl Sulfoxide and Trimethylamine N-Oxide as Terminal Electron Acceptors. J. Bacteriol.
187: 1659-1667
[Abstract]
[Full Text]
-
Miller, T. R., Hnilicka, K., Dziedzic, A., Desplats, P., Belas, R.
(2004). Chemotaxis of Silicibacter sp. Strain TM1040 toward Dinoflagellate Products. Appl. Environ. Microbiol.
70: 4692-4701
[Abstract]
[Full Text]
Copyright © 2004 by the American Society for Microbiology. All rights reserved.