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Allometric Scaling and Metabolic Ecology of Microorganisms and Major Evolutionary Transitions Jordan G

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Allometric Scaling and Metabolic Ecology of Microorganisms and Major Evolutionary Transitions Jordan G University of New Mexico UNM Digital Repository Biology ETDs Electronic Theses and Dissertations 7-1-2011 Allometric scaling and metabolic ecology of microorganisms and major evolutionary transitions Jordan G. Okie Follow this and additional works at: https://digitalrepository.unm.edu/biol_etds Recommended Citation Okie, Jordan G.. "Allometric scaling and metabolic ecology of microorganisms and major evolutionary transitions." (2011). https://digitalrepository.unm.edu/biol_etds/89 This Dissertation is brought to you for free and open access by the Electronic Theses and Dissertations at UNM Digital Repository. It has been accepted for inclusion in Biology ETDs by an authorized administrator of UNM Digital Repository. For more information, please contact [email protected]. i ii iii ACKNOWLEDGEMENTS I wish to extend my deepest gratitude to Dr. James H. Brown for his thoughtful mentorship and inspiring discussions. I am also very thankful to my committee members Drs. Richard Michod, Melanie Moses, and Robert Sinsabaugh and unofficial members and mentors Drs. Cristina Takacs-Vesbach and Val Smith for their feedback and support. I am also very grateful to Dr. Felisa Smith for her support and feedback throughout my graduate career. I wish to thank Robbie Burger, Bill Burnside, Dan Colman, Ana Davidson, John DeLong, Florence Germain-Robin, Marcus Hamilton, Ryan Hechinger Jesse Okie, Jen Richter, Richard Sibly, David Storch , Dave Van Horn, and Wenyun Zuo for their encouragement and insights, as well as the entire Brown and Smith lab groups for their continual source of support over the years. I am thankful for financial support from: the Howard Hughes Medical Institute (HHMI) under the HHMI–National Institute of Biomedical Imaging and Bioengineering Interfaces Initiative (through the Program in Interdisciplinary Biological and Biomedical Science at the University of New Mexico); and from UNM‘s Grove Research Scholarship, Melinda Bealmer Memorial Scholarship, and Student Research Allocation Committee Grants. iv v Allometric scaling and metabolic ecology of microorganisms and major evolutionary transitions By Jordan G. Okie B.A., Biology, Carleton College, 2003 Ph.D., Biology, University of New Mexico, 2011 ABSTRACT My dissertation centers around investigating big-picture questions related to understanding the consequences of metabolism and energetics on the evolution, ecology, and physiology of life. The evolutionary transitions from prokaryotes to unicellular eukaryotes to multicellular organisms were accompanied by major innovations in metabolic design. In my first chapter, I show that the scaling of metabolic rate, population growth rate, and production efficiency with body size have changed across these transitions. Metabolic rate scales with body mass superlinearly in prokaryotes, linearly in protists, and vi sublinearly in metazoans, so Kleiber‘s 3/4 power scaling law does not apply universally across organisms. This means that major changes in metabolic processes during the early evolution of life overcame existing physical constraints, exploited new opportunities, and imposed new constraints on organism physiology. Surface areas of physiological structures of organisms impose fundamental constraints on metabolic rate. In my second chapter, I demonstrate that organisms have a variety of options for increasing the scaling of the area of their metabolic surfaces with body sizes. I develop models and examples illustrating the role of cell membrane elaborations, mitochondria, vacuoles, vesicles, inclusions, and shape-shifting in the architectural design, evolution, and ecology of unicellular microbes. I demonstrate how these surface-area scaling adaptations have played important roles in the evolution of major biological designs of cells and the physiological ecology of organisms. In my third and final chapter, I integrate and synthesize findings from the previous two chapters with important developments in geochemistry, microbiology, and astrobiology in order to identify the fundamental physical and biological dimensions that characterize a metabolic theory of ecology of microorganisms. These dimensions are thermodynamics, chemical kinetics, physiological harshness, cell size, and levels of biological organization. I show how addressing these dimensions can inform understanding of the physical and biological factors governing the metabolic rate, growth rate, and geographic distribution of cells. I propose a unifying theory to understand how the major ecological and evolutionary transitions that led to increases in levels of organization of life, such as endosymbiosis, multicellularity, eusociality, and multi- vii domain complexes, influences the metabolism and growth and the metabolic scaling of these complexes. viii TABLE OF CONTENTS LIST OF FIGURES ............................................................................................................ x LIST OF TABLES ............................................................................................................. xi CHAPTER 1: Introduction ................................................................................................. 1 References ....................................................................................................................... 5 CHAPTER 2: Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life ............................................................................................ 7 Abstract ........................................................................................................................... 7 Introduction ..................................................................................................................... 7 Results and discussion ................................................................................................... 11 Methods ......................................................................................................................... 22 References ..................................................................................................................... 24 Acknowledgments ......................................................................................................... 28 CHAPTER 3: Surface area scaling strategies: fractality, geometric dissimilitude, and internalization ................................................................................................................... 30 Abstract ......................................................................................................................... 30 Introduction ................................................................................................................... 31 Fractality and the elaboration of surfaces ..................................................................... 35 Theory ........................................................................................................................ 35 Empirical observations .............................................................................................. 39 Geometric dissimilitude and shape-shifting .................................................................. 40 Theory ........................................................................................................................ 40 Empirical observations .............................................................................................. 47 Internalization of surface processes with organelles ..................................................... 48 Theory ........................................................................................................................ 48 Empirical observations .............................................................................................. 53 Other combinations of scaling strategies ...................................................................... 54 Discussion and synthesis ............................................................................................... 55 References ..................................................................................................................... 61 Appendix: Mathematical details of solid-body geometric dissimilitude ...................... 69 ix CHAPTER 4: Towards a metabolic theory of ecology for microorganisms .................... 73 Summary ....................................................................................................................... 73 Introduction ................................................................................................................... 74 Physiological foundations ............................................................................................. 78 Dimension 1: Thermodynamics .................................................................................... 85 Dimension 2: Chemical kinetics ................................................................................... 88 Dimension 3: Physiological harshness and environmental stress ................................. 94 Dimension 4: Cell size .................................................................................................. 97 Dimension 5: Levels of biological organization ......................................................... 102 Community metabolism and the interplay of dimensions ........................................... 110 Concluding remarks ...................................................................................................
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