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Todd Rex Miller, Doctor of Philosophy, 2004

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Todd Rex Miller, Doctor of Philosophy, 2004 ABSTRACT Title of Dissertation / Thesis: SWIMMING FOR SULFUR: ANALYSIS OF THE ROSEOBACTER- DINOFLAGELLATE INTERACTION Todd Rex Miller, Doctor of Philosophy, 2004 Dissertation / Thesis Directed By: Dr. Robert Belas, University of Maryland Biotechnology Institute, Center of Marine Biotechnology 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 α-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. SWIMMING FOR SULFUR: ANALYSIS OF THE ROSEOBACTER- DINOFLAGELLATE INTERACTION By Todd R. Miller Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2004 Advisory Committee: Dr. Robert Belas, Chair Dr. Russell Hill Dr. Allen Place Dr. Kevin Sellner Dr. Kevin Sowers © Copyright by Todd R. Miller 2004 Dedication To my loving wife Jenn, the source of all that inspires me. ii Acknowledgements I am eternally grateful to all those who have taught me the joy of seeking knowledge, most especially my brother Dr. Adam C. Miller, my advisor Dr. Robert Belas who recognized my potential and taught me how to think like a scientist, my parents Boyd and Susan Miller for giving me an inspired life, my wife Jennifer Robers Miller for her undying love and support and Dr. Michael Rosewall who taught me to be free with my voice and my convictions. I would also like to thank my PhD committee members, the Belas Laboratory, the Center of Marine Biotechnology, especially the fifth floor prokaryotes, Nona Krupatkina for helping with algal cell culture, Dr. Pongpan and Anchalee Laksanalamai for nutritional support and Dr. Joy Watts for numerous helpful suggestions in the preparation of this thesis. This work was supported by grants from NOAA ECOHAB (NA860PO492), NIH NIEHS (ES9563), and the Center of Marine Biotechnology. iii Table of Contents Dedication..................................................................................................................... ii Acknowledgements......................................................................................................iii Table of Contents......................................................................................................... iv List of Tables .............................................................................................................. vii List of Figures.............................................................................................................. ix Chapter 1: Introduction................................................................................................. 1 1.1 Harmful algal blooms (HABs) and toxic dinoflagellates ............................. 1 1.1.1 Harmful algal blooms (HABs).............................................................. 1 1.1.2 Factors that contribute to algal bloom formation.................................. 2 1.1.3 Toxic dinoflagellates............................................................................. 5 1.1.4 Distribution of toxic dinoflagellate blooms in the United States.......... 9 1.2 Pfiesteria dinoflagellates ............................................................................ 13 1.2.1 Discovery of Pfiesteria dinoflagellates............................................... 13 1.2.2 General characteristics........................................................................ 15 1.2.3 Life History......................................................................................... 17 1.2.4 Toxicity............................................................................................... 21 1.3 Bacterial interactions with dinoflagellates.................................................. 28 1.3.1 Attached and intracellular bacteria. .................................................... 28 1.3.2 Physiological interactions. .................................................................. 29 1.4 The Roseobacter clade and dimethylsulfoniopropionate............................ 33 1.4.1 General characteristics of the Roseobacter clade ............................... 33 1.4.2 Pathways involved in the degradation of DMSP ................................ 35 1.4.3 Roseobacter interactions with dinoflagellates .................................... 39 1.5 Production of DMSP in the marine ecosystem........................................... 40 1.5.1 Biochemistry of DMSP production .................................................... 40 1.5.2 Role of DMSP metabolites in dinoflagellate physiology ................... 44 1.5.3 Distribution of DMSP production in the environment ....................... 47 1.5.4 DMSP and the global sulfur cycle ...................................................... 49 1.6 Chemotaxis and motility in non-enteric bacteria........................................ 50 1.6.1 General aspects of motility and chemotaxis in bacteria...................... 50 1.6.2 Chemotaxis and motile behavior of non-enteric bacteria. .................. 52 1.6.3 Chemotaxis, motility and bacterial interactions with host cells. ........ 57 1.7 Bacteria associated with Pfiesteria (preliminary data) ............................... 60 1.7.1 Identification of the bacterial community members. .......................... 61 1.7.2 Analysis of Community Structure ...................................................... 63 1.7.3 Attached and intracellular bacteria ..................................................... 67 1.7.4 Physiological effects of bacteria ......................................................... 69 1.8 Specific aims of this study .......................................................................... 72 1.8.1 Metabolism of DMSP in Pfiesteria cultures........................................... 72 1.8.2 Chemotaxis of Silicibacter sp. TM1040 toward dinoflagellates ............ 72 1.8.3 Motility and interactions with P. piscicida............................................. 72 1.8.4 Annotate flagellar and chemotaxis genes ............................................... 73 Chapter 2: Dimethylsulfoniopropionate (DMSP) metabolism by Pfiesteria-associated Roseobacter................................................................................................................. 74 iv 2.1 Summary........................................................................................................... 74 2.2 Introduction....................................................................................................... 75 2.3 Materials and Methods...................................................................................... 78 2.3.1 Dinoflagellate strains and culturing........................................................... 78 2.3.2 Bacterial strains and media. ....................................................................... 79 2.3.3 Chemicals................................................................................................... 79 2.3.4 DMSP content and metabolism. ................................................................ 80 2.3.5 Analytical techniques................................................................................. 82 2.3.6 Statistics. ...................................................................................................
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