SWIMMING FOR SULFUR: ANALYSIS OF THE ROSEOBACTER-DINOFLAGELLATE INTERACTION

Abstract

Marine algae are some of the most productive organisms on earth, and their survival is dependent upon a diverse community of bacteria that consume algal products. The identity of these bacteria and mechanisms used to interact with their algal partner are not well understood. Recently it has been shown that -Proteobacteria of the Roseobacter clade are the primary consumers of the algal osmolyte, dimethylsulfoniopropionate (DMSP). In addition, their production and activity is highly correlated with DMSP producing algal blooms, especially those containing dinoflagellates. To understand more about this relationship, I have studied Roseobacter-dinoflagellate interactions in laboratory cultures of Pfiesteria dinoflagellates, a ubiquitous group of estuarine, heterotrophic dinoflagellates. The results show that cultures of P. piscicida and a similar dinoflagellate, Cryptoperidiniopsis sp., harbor a robust DMSP degrading bacterial community that contains members of the Roseobacter clade. One of these bacteria, Silicibacter sp. TM1040 degrades DMSP by demethylation producing 3-methymercaptopropionate (MMPA). Interestingly, this bacterium senses and actively moves toward P. piscicida cells. It is highly chemotactic toward amino acids, especially methionine, and DMSP metabolites, including DMSP and MMPA. Chemotaxis of TM1040 toward P. piscicida cells is mediated in part by the presence of these compounds in the dinoflagellates. Using a fluorescent tracer dye, this bacterium was found attached and/or within P. piscicida cells. The apparent intracellular occurence of Silicibacter sp. TM1040 requires both flagella and motility since mutants lacking motility and/or flagella are not found within the dinoflagellate, although they can be found attached. The presence of Silicibacter sp. TM1040 in axenic dinoflagellate cultures enhances dinoflagellate growth, a process that does not require the bacteria to be intracellular. The genome sequence of Silicibacter sp. TM1040 indicates that this bacterium contains a large number (20) of chemoreceptors and a full complement of flagellar and other chemotaxis genes. In addition, this bacterium contains all of the genes necessary to produce a type IV secretion system similar to the vir pilus of Agrobacterium tumefaciens. Taken together, the data suggest that Silicibacter sp. TM1040 is an attached and/or intracellular symbiont of P. piscicida. The significance of this study to microbial and algal bloom ecology is discussed.