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Molecular and Ecological Analysis of Cellular Attachment and Induction of Transparent Exopolymeric Particle Formation in Diatom-Bacteria Interactions

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Molecular and Ecological Analysis of Cellular Attachment and Induction of Transparent Exopolymeric Particle Formation in Diatom-Bacteria Interactions Molecular and ecological analysis of cellular attachment and induction of transparent exopolymeric particle formation in diatom-bacteria interactions by Shalin Seebah A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Marine Microbiology Approved Thesis Committee Prof. Dr. Matthias Ullrich Jacobs University Bremen Prof. Dr. Laurenz Thomsen Jacobs University Bremen Dr. habil. Uta Passow Marine Science Institute University of California Santa Barbara Date of defense: 23 March 2012 Jacobs University Bremen School of Engineering and Science ACKNOWLEDGEMENTS ................................................................................................................... I ABSTRACT .......................................................................................................................................... III LIST OF ABBREVIATIONS ............................................................................................................. IV INTRODUCTION ................................................................................................................................. 1 1.1 THE GLOBAL CARBON CYCLE ........................................................................................................... 1 1.1.1 Pre-industrial global carbon cycle .................................................................. 1 1.1.2 Present-day global carbon cycle ..................................................................... 2 1.2 OCEANIC CARBON CYCLE ................................................................................................................ 4 1.3 BIOLOGICAL PROCESSES OF THE OCEAN .......................................................................................... 8 1.3.1 The biological pump ....................................................................................... 8 1.3.2 Dissolved organic carbon ................................................................................ 9 1.3.3 Particulate organic carbon............................................................................... 9 1.4 MARINE SNOW............................................................................................................................... 12 1.4.1 Marine snow formation ................................................................................. 12 1.4.2 Marine gel particles....................................................................................... 13 1.5 TRANSPARENT EXOPOLYMERIC PARTICLES .................................................................................... 15 1.6 MICROSCALE INTERACTIONS ......................................................................................................... 17 1.6.1 Bacterial chemotaxis and motility ................................................................ 18 1.7 BILATERAL MODEL SYSTEM ........................................................................................................... 22 1.7.1 The diatom Thalassiosira weissflogii ........................................................... 22 1.7.2 The marine bacterium Marinobacter adhaerens sp. nov. HP15 ................... 24 AIMS OF THIS STUDY ...................................................................................................................... 26 SUMMARY OF RESULTS .................................................................................................................. 27 CHAPTER 1 .......................................................................................................................................... 29 3.1.1 Marinobacter adhaerens sp. nov., prominent in aggregate formation with the diatom Thalassiosira weissflogii............................................................................ 30 3.1.2 Complete genome sequence of Marinobacter adhaerens type strain (HP15), a diatom-interacting marine microorganism .......................................................... 49 3.1.3 Development of a genetic system for Marinobacter adhaerens HP15 involved in marine aggregate formation by interacting with diatom cells ............ 68 CHAPTER 2 ......................................................................................................................................... 97 3.1.4 Attachment of Marinobacter adhaerens HP15 to Thalassiosira weissflogii is not essential for the induction of transparent exopolymeric particle formation .... 98 CHAPTER 3 ....................................................................................................................................... 123 3.1.5 Combined effects of lowered pH and elevated temperature on diatom- bacteria interactions ............................................................................................. 124 DISCUSSION ..................................................................................................................................... 156 BIBLIOGRAPHY ............................................................................................................................... 164 DECLARATION ................................................................................................................................ 174 Acknowledgements This work was carried out from April 2009 to February 2012 as part of the Helmholtz Graduate School for Polar and Marine Research. The work presented in this thesis was carried out in the laboratories of Prof. Dr. Matthias Ullrich, at the Jacobs University Bremen and that of Dr. habil. Uta Passow at the University of California Santa Barbara. Prof. Dr. Laurenz Thomsen was an additional committee supervisor and helped guide the project. This work was performed in close collaboration with Dr. Astrid Gaerdes and Dr. Eva Sonnenschein from April 2009 until January 2011. They both vastly contributed to the project as a whole. This work was funded by Jacobs University Bremen, the Helmholtz association and the Marine Science Institute, University of California Santa Barbara. I would firstly like to thank Prof. Dr. Matthias Ullrich for the opportunity to learn and develop in his laboratory, for his unwavering support and for constantly prioritizing his busy schedule to closely supervise and interact with me. Dr. habil. Uta Passow is thanked for giving me the unique opportunity to work and learn from her during a three-month exchange at the Marine Science Institute, University of California Santa Barbara. It has been a humbling experience to work under her wings with constant optimism, motivation and good vibes. Prof. Laurenz Thomsen is thanked for accepting to review my work and for providing to the point criticism, which often prompted me to take a step back and re-focus on the aims of the project. For all the caricatures of scientists as creative loners, science is a richly social endeavor. And for that, I would like to express my heartfelt gratitude to my colleagues for a joyful laboratory atmosphere and for intellectual sustenance. To all the former and current members of the laboratory thank you: Dr. Astrid Gaerdes, Dr. Eva Sonnenschein, Ingrid Torres Monroy, Daniel Pletzer, Gabriela Alfaro, I Shaunak Khandekar, Amna Mehmood, Maria Johansson, Antje Stahl, Desalegne Abebew, Dr. Helge Weingart, Dr. Yannic Ramaye, Dr. Daria Zhurina, Dr. Nehaya Al-Karablieh and Dr. Abhishek Srivastava. My students, Sumana Sharma, Zheyna Kircheva, Yesim Yurtdas and Katharina Flenke are also thanked for giving me the pleasure of supervising them and for their help in the advancement of my project. Sabine Meier and Peter Tsvetkov are thanked for easing the administration and technical matters. Likewise, I extend my warmest thanks to the UCSB team for graciously offering me their help and sharing their equipment whenever I needed them. I would like to especially thank Caitlin Fairfield, the invaluable technician of the laboratory, who contributed on a daily basis both with technical help and experience. Dr. Craig Nelson and Dr. Mary Raven are thanked for their assistance with the epifluorescence microscope. Dr. Konrad Kulacki, Dr. Steve Sadro and Prof. Alice Alldredge are thanked for making feel part of Building 408. I would also like to extend my appreciation to the Bio workshop personnel who promptly repaired the roller tanks which I inadvertly cracked. I am grateful to the POLMAR graduate school and thank everyone who has in a way or the other contributed to the setting up and maintenance of the program. I thank the POLMAR coordinators: Prof. Jelle Bijma, Dr. Claudia Hanfland, Dr. Claudia Sprengel, Dörte Burhop and Dr. Tania Michler-Cieluch who have offered me much more support - moral, educational and financial – than I imagined. I am proud to have been a part of this prestigious program. I would also like to thank Claudia Daniel and Andreas Wagner for providing us with North Sea Water whenever we were in need. In the world beyond my experimental work, I have been extremely lucky for the solid foundation and support of my parents and sisters, even during the times when it was difficult for them that I left home to pursue my aspirations. Thank you for always encouraging me and being a phone call away whenever I needed to vent. My dear friends, Petra Pop Ristova, Tim Kalvelage, Abdul Rahiman Sheik, Renzo Kottmann, Marianne Jacob, Pier-Luigi Buttigieg and Pelin Yilmaz are thanked for making life in Bremen abound with happy memories. Finally, I thank Maté for being my pillar of love, support and fun and without whom none of this would have been possible.
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