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Mixotrophic Magnetosome-Dependent Magnetoautotrophic Metabolism of Model Magnetototactic Bacterium Magnetospirillum Magneticum A

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Mixotrophic Magnetosome-Dependent Magnetoautotrophic Metabolism of Model Magnetototactic Bacterium Magnetospirillum Magneticum A Mixotrophic Magnetosome-Dependent Magnetoautotrophic Metabolism of Model Magnetototactic Bacterium Magnetospirillum magneticum AMB-1 Dissertation Presented In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Eric Keith Mumper, BA Graduate Program in the School of Earth Sciences The Ohio State University 2019 Dissertation Committee: Steven K. Lower, Adviser Brian H. Lower Ratnasingham Sooryakumar Ann E. Cook Copyright by Eric Keith Mumper 2019 Abstract Magnetospirillum magneticum AMB-1 is a member of a phylogenetically diverse group of bacteria characterized by their ability to biomineralize magnetic minerals known collectively as magnetotactic bacteria (MTB).1,2,3 MTB produce chains of membrane- bound intracellular magnetic nanocrystals, collectively known as magnetosomes.1,2,3 The current scientific consensus is that magnetosomes are used by MTB to orient themselves in vertically stratified water columns in order to achieve optimal oxygen concentrations in a process known as magnetoaerotaxis.4,5 Biomineralization of magnetosomes is an energy intensive process which accounts for roughly 33% of the cell's metabolic budget.6 This high metabolic cost seems to contradict with the amount of time MTB cells spend aligned with external magnetic fields.5 Due to this apparent discrepancy, I examined the potential role the magnetosome may play in bacterial metabolism. Through analysis of comparative growth on a variety of media compositions both magnetic, wild type and non-magnetic, mutant strains of AMB-1, I discovered that cells grown under stress conditions exhibit an inversion of growth dynamics which indicates some advantage for magnetic cells. Non-magnetic, mutant cells display a direct relationship between external magnetic field strength and growth, indicating magnetic field dependence. I believe that this represents a novel magnetosome-dependant mixotrophic metabolism. Due to the i ubiquity of MTB1,2,3 and the diversity of sessile eukaryotes which either produce biogenic magnetite or exhibit magnetosensing,7 this system may be part of a widespread, previously unknown component of global carbon cycling. ii Dedication This work is dedicated to Alicia Mumper, my wife of seventeen years and counting, who has supported me through sickness and in health, for richer and for poorer, through better and through worse, and, most impressively of all, through eleven years of college. iii Acknowledgments The completion of this thesis would not have been possible without the help of the friends, family and colleagues listed below: Thanks to both my current and former committee members: Drs. Steven K Lower, Brian H. Lower, Ratnasingham Sooryakumar, Ann E. Cook, Michael Barton and Mike J. Wilkins for their advice, encouragement, and criticism of my research. Thanks to my children: Padraig, Briona, and Nevin for their patience and understanding as their dad spent ten years in college. Thanks to my parents: John and Terri Mumper as well as Richard and Roxy Witmer for their financial support and emotional encouragement through this experience. Thanks to my colleagues Anne Booker, Kelsey Danner, James Dunn, Mike Johnston, Dr. Nicola Lorenz, Rowan McLachlan, Dr. Zachery Oestreicher, Chris Pierce, Casey Saup, Kylienne Shaul, and Max Wheeler for their expertise, advice, and encouragement with various aspects of this research. Thanks to the Dick, EMSL, Sawyer, Wilkins, and Wrighton labs to access to equipment and materials while pursuing various aspects of this research. iv Vita Education BA in Geology / minor in Biology 2007-2012 Ohio Wesleyan University Delaware, OH Teaching Graduate Teaching Assistant 2012-current School of Earth Sciences, The Ohio State University Facilitator 2016 University Center for the Advancement of Teaching Research Publications Pierce Chrostopher J, Wijesinghe Hiran, Mumper Eric, Lower Brian H, Lower Steven K, Sooryakumar Ratnasingham. “Hydrodynamic Interactions, Hidden Order, and Emergentt Collective Behavior in an Active Bacterial Suspension.” Phys. Rev. Lett. (submitted 2018) Pierce Christopher J, Mumper Eric, Brangham, Jack T, Lower Brian H, Lower Steven K, Yang Fengyuan Y, Sooryakumar Ratnasingham. “Tuning Bacterial Hydrodynamics with Magnetic Fields” 2017. Phys. Rev. E. 10.1103/PhysRevE.95.062612. Oestreicher Zachery, Mumper Eric, Gassman Carol, Bazylinski Dennis, Lower Steven K, Lower Brian H. “Spatial Localization of Mms6 During Biomineralization of Fe3O4 Nanocrystals in Magnetospirllum magneticum AMB-1”2016. J. Mat. Res. 31(5):527-535. Conference Posters “Pushed, Poked, and Prodded: Documenting Changes in Magnetotactic Bacteria from Wetland to Pure Culture” Goldschmidt Conference 2015, Prague, Cz. “Iron-sulfide Concretions of the Ohio Shale: Glimpses of Deep Subseafloor Microbial Ecosystems of the Late Devonian” Geologic Society of America 2012, Dayton, OH v Presentations “Magnetotactic bacterium Magnetosprillum magneticum AMB-1 displays magnetic field dependent growth” American Geophysical Union 2018, Washington, DC. “Biologically Controlled Mineralization of Magnetite Nanocrystals” Goldschmidt Conference 2014, Sacramento, CA. Awards School of Earth Sciences Distinguished Teaching Award 2016 Robert E. Shanklin Distinguished Scholar Award in Geology 2012 Fields of Study Major Field: Earth Sciences Minor Fields: Geomicrobiology, biomineralization, biochemistry, geochemistry vi Table of Contents Abstract i Dedication iii Acknowledgements iv Vita v List of Tables x List of Figures xii Chapter 1: Characteristics of magnetotactic bacteria and magnetoaeroaxis 1 1.1: Introduction to magnetotactic bacteria 1 1.2: Magnetoaerotaxis model 3 1.3: MTB diversity and magnetosome formation and diversity 4 1.4: Energetics of magnetosome biomineralization 6 1.5: Interesting MTB characteristics 7 1.6: Highly unusual MTB characteristics 8 1.7: Critiquing magnetoaerotaxis model 11 1.8: Alternative possibilities for the magnetosome 13 Chapter 2: Magnetotactic bacteria grown in various media 17 2.1: Magnetotrophic Model 17 vii 2.2: Media rationale, recipes and experimental design 19 2.3: Autotrophic media version 1 – Modified MSGM 24 2.4: Autotrophic media version - BG11 26 2.5: Autotrophic media version – Bazylinski / Frankel formula 27 2.6: Enhanced growth on mixed media 36 Chapter 3: Magnetotactic bacteria grown on reduced organic carbon media 51 3.1: Dynamics of mixed media growth of M. magneticum AMB-1 51 3.2: Analysis of nitrogen sources 58 3.3: Fixation of radiolabeled bicarbonate 61 3.4: Role of organic carbon 63 3.5: Summary of mixed media growth 65 Chapter 4: Magnetic-field-dependent growth of Magnetospirillum magneticum AMB-1 66 4.1: Preface 66 4.2: Rationale for alternative to magnetoaerotaxis 66 4.3: Methods 67 4.4: Growth of AMB-1 strains on MSGM and BFM50 68 4.5: Growth in variable strength external magnetic fields 72 4.6: Magnetic-field-dependent biology 73 4.7: Magnetic-field-dependent growth as a novel metabolism 76 References 78 Appendix A: Growth of AMB-1 on MSGM without organic carbon 78 viii Appendix B: AMB-1 growth on MSGM and BG11 79 Appendix C: Growth of AMB-1 in Multivariable Experiment 80 Appendix D: Comparison of Growth of AMB-1 on BFAM of Various Oxygen Concentrations 86 Appendix E: Mixed Media Growth of Wild-type and Mutant AMB-1 strains 88 Appendix F: Growth of Wild-type and Mutant AMB-1 Strains on Mixed Media 97 Appendix G: AMB-1 growth on NO3 vs NH4 106 Appendix H: Incorporation of Radiolabeled Bicarbonates 107 Appendix I: Organic-carbon Pulse on 100% BFAM 108 ix List of Tables Table 1: Comparison between MTB and E. coli 9 Table 2: Revised Magnetospirillum Growth Media (MSGM) recipe (ATCC1653) 20 Table 3: Wolfe's Vitamin Solution 20 Table 4: Wolfe's Mineral Solution 21 Table 5: Ferric Quinate (0.01 M) 21 Table 6: Magnetic Spirillum growth medium organic carbon removed 22 Table 7: Modified BG-11 Media 22 Table 8: Bazylinski / Frankel Autotrophic Media (BFAM) 23 Table 9: Modified Wolfe's Mineral Solution 23 Table 10: Frankel's Vitamin Solution 24 Table 11: Variables, controls, and expected results of multivariable experiments 29 Table 12: Oxygen experiment media preparation 35 Table 13: Modified Magnetospirillum Growth Media (MSGM) recipe 37 Table 14: Mixed media composition 37 Table 15: Bazylinski / Frankel Media (BFM) 50 Table 16: Mixed media composition II 52 x Table 17: Calculated variations in the composition of mixed media recipes 59 xi List of Figures Figure 1: Image of magnetic AMB-1 cells, under field and no field 2 Figure 2: Diagram of magnetoaerotaxis 4 Figure 3: Magnetic vs non magnetic gammaproteobacteria comparison 13 Figure 4: Iron-oxide precipitate in autotrophic media 25 Figure 5: M. magneticum AMB-1 cells in autotrophic media precipitate 25 Figure 6: Growth of AMB-1 on MSGM without organic carbon 26 Figure 7: AMB-1 growth on MSGM and BG-11 27 Figure 8: Growth of M. magneticum AMB-1 on MSGM 30 Figure 9: Growth of M. magneticum AMB-1 on BFAM in dark 31 Figure 10: Growth of M. magneticum AMB-1 on BFAM in blue light 31 Figure 11: Growth of M. magneticum AMB-1 on BFAM in red light 32 Figure 12: Growth of M. magneticum AMB-1 on BFAM in increased magnetic field 32 Figure 13: Sterile BFAM in dark 33 Figure 14: Average growoth of M. magneticum AMB-1 in multivariable experiments 33 Figure 15: Comparison of growth of AMB-1 on BFAM of various oxygen xii concentrations 35 Figure 16: Growth of magnetic M. magneticum AMB-1 100% MSGM / 0% BFAM 38 Figure 17: Growth of magnetic M. magneticum AMB-1 95% MSGM / 5% BFAM 39 Figure 18: Growth of magnetic M. magneticum AMB-1 90% MSGM / 10% BFAM 39 Figure 19: Growth of magnetic M. magneticum AMB-1 75% MSGM / 25% BFAM 40 Figure 20: Growth of magnetic M. magneticum AMB-1 50% MSGM / 50% BFAM 40 Figure 21: Growth of magnetic M. magneticum AMB-1 25% MSGM / 75% BFAM 41 Figure 22: Growth of magnetic M. magneticum AMB-1 10% MSGM / 90% BFAM 41 Figure 23: Growth of magnetic M. magneticum AMB-1 5% MSGM / 95% BFAM 42 Figure 24: Growth of magnetic M.
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