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Densely Packed Yeast: a Tool to Study Evolution of Group Dynamics and to Enhance Biomanufacturing

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Densely Packed Yeast: a Tool to Study Evolution of Group Dynamics and to Enhance Biomanufacturing DENSELY PACKED YEAST: A TOOL TO STUDY EVOLUTION OF GROUP DYNAMICS AND TO ENHANCE BIOMANUFACTURING. A Dissertation Presented to The Academic Faculty by Jordan Gulli In Partial Fulfillment of the Requirements for the Doctor of Philosophy in Biology in the School of Biological Sciences Georgia Institute of Technology December 2019 COPYRIGHT © 2019 BY JORDAN GULLI DENSELY PACKED YEAST: A TOOL TO STUDY EVOLUTION OF GROUP DYNAMICS AND TO ENHANCE BIOMANUFACTURING. Approved by: Dr. Frank Rosenzweig, Advisor Dr. Francesca Storici School of Biology School of Biology Georgia Institute of Technology Georgia Institute of Technology Dr. William Ratcliff Dr. Peter Yunker School of Biology School of Physics Georgia Institute of Technology Georgia Institute of Technology Dr. Brian Hammer Dr. Arthur Kruckeberg School of Biology Senior Research Scientist Georgia Institute of Technology Trait Biosciences Date Approved: August 03, 2019 To my parents, who always knew I could do it. And to Alex, who helped me get there. ACKNOWLEDGEMENTS I would like to first thank all those who have provided me with exemplary scientific training over the years, including mentors Dr. Amy Schmid, Dr. Alexander Pavlov, Dr. William Ratcliff, and Dr. Frank Rosenzweig, as well as less formal sources of instruction, including Kriti Sharma, Jennifer Pentz, Shane Jacobeen, and Emily Cook. I would also like to express gratitude for my sources of funding, including NSF Graduate Research Predoctoral Fellowship DGE-1148903, NSF iCorps 1743464 and the Georgia Research Alliance (GRA.Vl18.B16). Last, but not least, I would like to thank all those whose support has been less tangible, though no less important: my parents Mick and Karen Gulli, my godparents Buzz and Rho Griffin, Alexander Radek, and, of course, Emma. iv TABLE OF CONTENTS ACKNOWLEDGEMENTS iv LIST OF TABLES ix LIST OF FIGURES x LIST OF SYMBOLS AND ABBREVIATIONS xii SUMMARY xiv CHAPTER 1. Introduction 1 1.1 Group formation 1 1.2 A brief history of gasoline and ethanol production 5 1.3 Current gasoline and ethanol demand 8 1.4 An overview of modern ethanol production 9 1.5 Cellulosic ethanol 11 1.6 Political regulations impact ethanol production 13 1.7 Technical difficulties associated with cellulosic ethanol production 14 1.8 Project goals 16 CHAPTER 2. Evolution of altruistic cooperation among nascent multicellular organisms Error! Bookmark not defined. 2.1 Introduction 17 2.2 Methods 21 2.2.1 Yeast culture 21 2.2.2 Aggregate discovery and creation of t227b.15 21 2.2.3 Evolving aggregate formation from an ancestral snowflake yeast 24 2.2.4 Measuring cluster size 25 2.2.5 Measuring cell death 25 2.2.6 Aggregate formation, cell death, and cluster size in ancestral strains 25 2.2.7 Heritability of aggregate formation 26 2.2.8 Aggregate composition 26 2.2.9 Cell death and aggregate formation 27 2.2.10 Divergent selection experiment 28 2.2.11 Settling speed 29 2.2.12 Aggregate formation and survival 29 2.2.13 Determining if aggregates discriminate against unicellular yeast 30 2.2.14 Determining if aggregate formation is a common good 30 2.3 Results 31 2.3.1 Snowflake yeast evolved a novel form of cooperation under strong settling-rate selection 31 2.3.2 De novo evolution of aggregation 35 2.3.3 Aggregates form in snowflake yeast with high levels of cell death 35 2.3.4 Heritability of aggregate formation 36 v 2.3.5 Proteins are the main structural component of aggregates 39 2.3.6 Aggregates result from cell death 39 2.3.7 Aggregate formation is advantageous when fast settling is favoured 41 2.3.8 Aggregates settle faster than individual clusters, increasing survival 43 2.3.9 Aggregates are a common good 45 2.4 Discussion 46 CHAPTER 3. Diverse conditions support near-zero growth in yeast: implications for the study of cell lifespan 51 3.1 Introduction 51 3.2 Chronological aging in starved planktonic cultures 53 3.3 Chronological aging in yeast colonies 55 3.3.1 Cells in a colony display slower growth, and higher viability than aging planktonic cells 55 3.3.2 Yeast in aging colonies become physiologically-differentiated 57 3.3.3 Cell stratification benefits some cell types at the expense of others, contributing to colony longevity 60 3.3.4 Giant colonies as a model to study aging and cancer 62 3.4 Chronological aging in continuous culture: the retentostat 63 3.4.1 Retentostat growth and viability 64 3.4.2 Transcriptomics 64 3.4.3 Proteomics 66 3.4.4 Starvation vs. caloric restriction 67 3.4.5 Yeast retentostats as a model for the study of chronological aging 69 3.5 Chronological aging in continuously-fed immobilized cell reactors 70 3.5.1 Industrial applications 71 3.5.2 Potential for social interactions among encapsulated yeast 72 3.5.3 Physiology and transcriptomics 73 3.5.4 Proteomics and metabolomics 78 3.5.5 ICRs for the identification of anti-aging compounds 79 3.5.6 Encapsulated, continuously-fed yeast as a model for studying chronological lifespan 80 3.6 Conclusions and Future Directions 81 CHAPTER 4. Matrices (re)loaded: Durability, viability and fermentative capacity of yeast encapsulated in beads of different composition during long-term fed-batch culture 84 4.1 Introduction 84 4.2 Materials and Methods 88 4.2.1 Strains and culture conditions 88 4.2.2 Preparation of encapsulation matrices and cell encapsulation 89 4.2.3 Estimation of Young’s modulus, viscosity, and bead size via Universal Testing Machine 91 4.2.4 Estimation of wet weight bead mass 92 4.2.5 Fermentative capacity 92 4.2.6 Cell enumeration and cell viability 93 4.2.7 Heat shock tolerance 95 vi 4.2.8 Statistical analyses 96 4.3 Results and Discussion 96 4.3.1 Young’s modulus and viscosity of alginate beads declined over time 96 4.3.2 Bead size and mass increased over time 102 4.3.3 Ethanol yield (g/g) from dextrose varied among treatments 104 4.3.4 Following outgrowth, total cell number was similar across encapsulated and planktonic cultures 107 4.3.5 Cell escape increased over time, except in Pr beads 109 4.3.6 Cell viability declined over time in both encapsulated and planktonic cell cultures 111 4.3.7 Encapsulated cells are more heat-shock resistant than planktonic cells, but no one matrix confers greater heat-shock resistance than another 115 4.3.8 Encapsulation matrices vary in cost 117 4.4 Conclusions 119 CHAPTER 5. Encapsulation increases genome stability of yeast dikaryons produced via protoplast fusion 120 5.1 Introduction 120 5.2 Materials and Methods 123 5.2.1 Strains and culture conditions 123 5.2.2 Protoplast formation and fusion 126 5.2.3 Verification of dikaryons using PI staining 127 5.2.4 Verification of dikaryons using DAPI staining 128 5.2.5 Preparation of encapsulation matrices and cell encapsulation 128 5.2.6 Cell enumeration, viability, and population dynamics 130 5.2.7 Fermentation parameters 132 5.2.8 Statistical analyses 133 5.3 Results and Discussion 133 5.3.1 Verification of dikaryons 134 5.3.2 Encapsulation impacts cell viability over repeated fed-batch culture 134 5.3.3 Encapsulation reduces the accumulation of biomass 136 5.3.4 Encapsulation enhances genetic stability 138 5.3.5 Encapsulation increases ethanol production on a per-cell basis 142 5.4 Conclusions 146 CHAPTER 6. Discussion 148 6.1 Overview 148 6.2 Aggregate formation is temporary 149 6.3 Aggregates are unlikely to represent a new level of selection 150 6.4 Aggregates lack a mechanism of fitness alignment 152 6.5 Suggestions for future work with aggregates 153 6.6 Feasibility of using encapsulated yeast at industry scales 155 6.7 Suggestions for future experiments on the use of encapsulated yeast for conventional ethanol production 158 6.8 Genome instability: the problem 160 6.9 Encapsulation as a means of improving genome stability 163 6.10 Encapsulated dikaryons for cellulosic ethanol production 163 vii 6.11 Suggestions for future experiments utilizing encapsulated dikaryons 164 6.12 General Conclusions 165 REFERENCES 168 viii LIST OF TABLES Table 1. Selective regime and aggregate production of yeast strains ....................... 34 Table 2. Types of matrices utilized in this manuscript.. ........................................... 90 Table 3. Differences in Young’s modulus over time ................................................ 98 Table 4. Differences in viscosity over time. ............................................................. 99 Table 5. Chemical composition of different alginates. ........................................... 100 Table 6. Differences in bead size (mm) over time. ................................................. 101 Table 7. Differences in bead mass (g) over time. ................................................... 103 Table 8. Differences in ethanol yield (g/g) from dextrose over time. ..................... 105 Table 9. A comparison of total cell number across different bead types over time. ................................................................................................................................. 108 Table 10. Differences in viability over time ........................................................... 112 Table 11. Differences in heat shock resistance over time. ...................................... 116 Table 12. Strains of yeast used in this chapter. ....................................................... 125 ix LIST OF FIGURES Figure 1. A schematic of modern ethanol production. .................................................. 6 Figure 2. US ethanol production. .................................................................................. 7 Figure 3. A correlation between the cost of corn
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