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Environmental Regulation of Bioluminescence in Vibrio

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Environmental Regulation of Bioluminescence in Vibrio ENVIRONMENTAL REGULATION OF BIOLUMINESCENCE IN VIBRIO FISCHERI ES114 by NOREEN LORETTA LYELL (Under the Direction of Eric V. Stabb) ABSTRACT The pheromone-mediated circuitry that governs bioluminescence in Vibrio fischeri is well understood; however, less is known about the environmental conditions that influence pheromone and light production. The environment has been shown to have a profound effect on luminescence in V. fischeri, as cells in symbiotic association with the Hawaiian bobtail squid, Euprymna scolopes, are ~1000-fold brighter than non- symbiotic cells despite reaching similar cell densities. In this dissertation, I show that luminescence is governed by a complex regulatory web and that certain environmental conditions mediate the regulation of pheromone circuitry. My first goal was to identify and characterize previously unidentified regulators that control luminescence in V. fischeri strain ES114. I helped develop and employed a transposon mutagenesis system to discover novel negative regulators of luminescence. In this study, I characterized twenty-eight independent luminescence-up mutants with insertions in 14 loci. This work revealed that environmental conditions such as inorganic phosphate and Mg2+ concentrations are integrated into the regulation of the pheromone-dependent lux system. Furthermore, I showed that competition between the LuxI- and AinS-generated pheromones is an important and density-dependent factor in the level of light produced by V. fischeri ES114 cells, such that C8-HSL inhibits luminescence in dense populations. The second goal of this work was to clarify the role of cAMP receptor protein (CRP) in luminescence. Attempts to study the effects of glucose on V. fischeri luminescence have been contradictory and inconclusive, possibly due to strain-specific effects. I confirmed that both cAMP and glucose modulate light production in ES114, which is consistent with CRP regulation of luminescence. Previous researchers proposed a model wherein CRP regulates transcription of luxR, which encodes a pheromone-dependent activator known to induce luminescence. The data reported in this dissertation indicates that CRP is involved in the expression of not only luxR but also ainS. Using qRT-PCR and purified CRP, I show that CRP significantly increases transcript levels of both luxR and ainS, and that the CRP protein binds the upstream promoter regions of both genes. Taken together, this dissertation illustrates and clarifies how environmentally responsive regulators are integrated with pheromone-mediated circuitry in the regulation of V. fischeri bioluminescence. INDEX WORDS: Aliivibrio, Photobacterium, quorum sensing, luminescence, CRP ENVIRONMENTAL REGULATION OF BIOLUMINESCENCE IN VIBRIO FISCHERI ES114 by NOREEN LORETTA LYELL B. S., University of Arizona, 2004 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2011 © 2011 Noreen Loretta Lyell All Rights Reserved ENVIRONMENTAL REGULATION OF BIOLUMINESCENCE IN VIBRIO FISCHERI ES114 by NOREEN LORETTA LYELL Major Professor: Eric V. Stabb Committee: Timothy R. Hoover Mark A. Schell Lawrence J. Shimkets Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia August 2011 DEDICATION I dedicate this dissertation to Loretta, you have given me the strength and courage to accomplish my dreams, and to Aubrey, you will always be my sunshine. iv ACKNOWLEDGEMENTS There are several individuals that have aided me throughout graduate school. I especially have to thank my advisor, Eric Stabb. His support and guidance have been essential to my success. Furthermore, he has enabled me to attend meetings and participate in programs that have been instrumental in defining my career goals. I also thank my committee members, Mark Schell, Larry Shimkets, and Tim Hoover. I am a better researcher because of their insight. In addition, I want to acknowledge Anna Karls as her advice and input have advanced me as an instructor and mentor. v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .................................................................................................v LIST OF TABLES ............................................................................................................. ix LIST OF FIGURES .............................................................................................................x CHAPTER 1 Introduction and literature review ......................................................................1 Overview ......................................................................................................2 Pheromone-mediated regulation and common bacterial pheromones .........3 Environmental control of AI synthesis ........................................................5 Catabolite repression and pheromone-mediated regulation .......................11 Quorum sensing circuitry and the V. fischeri-E.scolopes symbiosis .........12 Purpose of this research .............................................................................19 References ..................................................................................................21 2 Effective mutagenesis of Vibrio fischeri using hyperactive mini-Tn5 derivatives ........................................................................................................39 Abstract ......................................................................................................40 Introduction ................................................................................................41 Results and Discussion ..............................................................................43 Acknowledgements ....................................................................................52 References ..................................................................................................53 vi 3 Bright mutants of Vibrio fischeri ES114 reveal conditions and regulators that control bioluminescence and expression of the lux operon .............................62 Abstract ......................................................................................................63 Introduction ................................................................................................64 Materials and Methods ...............................................................................68 Results ........................................................................................................74 Discussion ..................................................................................................92 Acknowledgements ....................................................................................98 References ..................................................................................................99 4 CRP regulates pheromone-mediated bioluminescence at multiple levels in Vibrio fischeri ES114 .....................................................................................111 Abstract ....................................................................................................112 Introduction ..............................................................................................113 Materials and Methods .............................................................................115 Results ......................................................................................................129 Discussion ................................................................................................142 Acknowledgements ..................................................................................149 References ................................................................................................150 5 Conclusions and future directions ..................................................................158 Elucidating the regulatory web governing the pheromone-dependent lux system ......................................................................................................160 Elucidating the role of CRP in the regulation of luminescence ...............163 Conclusion ...............................................................................................166 vii References ................................................................................................167 APPENDICES A Colonization and motility phenotypes of Vibrio fischeri ES114 luminescence- up mutants ......................................................................................................169 B Method for extracting symbiotic Vibrio fischeri cells from the Euprymna scolopes light organ .......................................................................................180 viii LIST OF TABLES Page Table 2.1: Oligonucleotides designed for this study ..........................................................46 Table 3.1: Analysis of luminescence-up transposon mutants ............................................75 Table 3.2: Luminescence analysis of mutants involved in the AinS signaling pathways .85 Table 4.1: Bacterial strains, plasmids, and oligonucleotides used in this study ..............116 Table A.1: Ability of mutant strains to compete with ES114 in co-cultures ...................175 ix LIST OF FIGURES Page Figure 1.1: Representative AHL molecule ..........................................................................3 Figure 1.2: Schematic of quorum
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