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Applied and Environmental Microbiology, March 2008, p. 1535-1545, Vol. 74, No. 5
0099-2240/08/$08.00+0     doi:10.1128/AEM.02339-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Genetic Dissection of Tropodithietic Acid Biosynthesis by Marine Roseobacters{triangledown} ,{ddagger}

Haifeng Geng,1,{dagger} Jesper Bartholin Bruhn,2,{dagger} Kristian F. Nielsen,3 Lone Gram,2 and Robert Belas1*

Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 East Pratt Street, Baltimore, Maryland 21202,1 Danish Institute for Fisheries Research, Department of Seafood Research, Technical University of Denmark, Bldg. 221, Soeltofts Plads, DK-2800 Kongens Lyngby, Denmark,2 Center for Microbial Biotechnology, BioCentrum, Technical University of Denmark, Bldg. 221, Soeltofts Plads, DK-2800 Kongens Lyngby, Denmark3

Received 16 October 2007/ Accepted 2 January 2008

The symbiotic association between the roseobacter Silicibacter sp. strain TM1040 and the dinoflagellate Pfiesteria piscicida involves bacterial chemotaxis to dinoflagellate-produced dimethylsulfoniopropionate (DMSP), DMSP demethylation, and ultimately a biofilm on the surface of the host. Biofilm formation is coincident with the production of an antibiotic and a yellow-brown pigment. In this report, we demonstrate that the antibiotic is a sulfur-containing compound, tropodithietic acid (TDA). Using random transposon insertion mutagenesis, 12 genes were identified as critical for TDA biosynthesis by the bacteria, and mutation in any one of these results in a loss of antibiotic activity (Tda–) and pigment production. Unexpectedly, six of the genes, referred to as tdaA-F, could not be found on the annotated TM1040 genome and were instead located on a previously unidentified plasmid (ca. 130 kb; pSTM3) that exhibited a low frequency of spontaneous loss. Homologs of tdaA and tdaB from Silicibacter sp. strain TM1040 were identified by mutagenesis in another TDA-producing roseobacter, Phaeobacter sp. strain 27-4, which also possesses two large plasmids (ca. 60 and ca. 70 kb, respectively), and tda genes were found by DNA-DNA hybridization in 88% of a diverse collection of nine roseobacters with known antibiotic activity. These data suggest that roseobacters may use a common pathway for TDA biosynthesis that involves plasmid-encoded proteins. Using metagenomic library databases and a bioinformatics approach, differences in the biogeographical distribution between the critical TDA synthesis genes were observed. The implications of these results to roseobacter survival and the interaction between TM1040 and its dinoflagellate host are discussed.

* Corresponding author. Mailing address: Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 East Pratt Street, Baltimore, MD 21202. Phone: (410) 234-8876. Fax: (410) 234-8896. E-mail: belas{at}umbi.umd.edu

{triangledown} Published ahead of print on 11 January 2008.

{ddagger} Supplemental material for this article may be found at http://aem.asm.org/.

{dagger} H.G. and J.B.B. contributed equally to this study.

Applied and Environmental Microbiology, March 2008, p. 1535-1545, Vol. 74, No. 5
0099-2240/08/$08.00+0     doi:10.1128/AEM.02339-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Slightom, R. N., Buchan, A. (2009). Surface Colonization by Marine Roseobacters: Integrating Genotype and Phenotype. Appl. Environ. Microbiol. 75: 6027-6037 [Abstract] [Full Text]  
  • Belas, R., Horikawa, E., Aizawa, S.-I., Suvanasuthi, R. (2009). Genetic Determinants of Silicibacter sp. TM1040 Motility. J. Bacteriol. 191: 4502-4512 [Abstract] [Full Text]  
  • Mann, E., Zaunbrecher, M. A, Hitz, K., Churchward, G. (2008). The 52nd Annual Wind River Conference on Prokaryotic Biology--2008. J. Bacteriol. 190: 7871-7875 [Full Text]  
  • 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]  


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