Establishing a novel beneficial association using a nematode-bacterium model through experimental evolution Restricted; Files Only

Abstract

Microbes confer many benefits to their hosts, from nutrient provisioning to protection from enemies. These microbial symbioses are ubiquitous in nature, many of which evolved millions of years ago. However, it is unclear how these associations arise. My dissertation explores the roles of environmental and evolutionary contexts in the evolution of novel beneficial associations. I use the nematode Caenorhabditis elegans and the bacterium Bacillus subtilis as a model system to investigate these questions by experimentally evolving them under different conditions. Before experimental evolution, I find that B. subtilis protects C. elegans from heat shock by increasing host fecundity compared to the C. elegans standard diet, E. coli. To examine how B. subtilis influence C. elegans adaptation, I evolve nematodes in the presence or absence of ancestral B. subtilis with or without heat stress. Hosts evolving with ancestral B. subtilis under stress evolve the greatest fitness gain compared to in the absence of heat stress or in the absence of B. subtilis. These results show that association with novel beneficial microbes can help hosts adapt to stress under the right context. To determine how microbial evolutionary history affects host fitness, I passage B. subtilis through ancestral nematodes, in the absence of nematodes, or through co-passaged nematodes. I find that B. subtilis passaged through ancestral hosts evolve to benefit these hosts, but host adaptation is not necessary since bacteria passaged in the absence of hosts also increase host fitness. Finally, because co-passaged bacteria do not improve ancestral host fitness to the same level as bacteria passaged through ancestral hosts, I further investigate co-passaging by examining the fitness of co-passaged hosts. Co-passaged bacteria reduce fitness of their co-passaged hosts but not hosts that evolved with ancestral B. subtilis, suggesting that coevolution may impede the establishment of novel symbioses. By leveraging experimental evolution and a tractable model system, this work illuminates how environmental and evolutionary contexts shape the evolution of host-microbe associations.

Table of Contents

I. INTRODUCTION

I.1. THE ORIGIN OF BENEFICIAL SYMBIOSES

I.2. THE ROLE OF EVOLUTIONARY INTERACTIONS IN BENEFICIAL HOST-MICROBE INTERACTIONS 

I.3. CAENORHABDITIS ELEGANS AND BACILLUS SUBTILIS AS A MODEL SYSTEM TO STUDY BENEFICIAL ASSOCIATIONS THROUGH EXPERIMENTAL EVOLUTION

I.4. SUMMARY OF DISSERTATION CHAPTERS

II. EXPERIMENTAL EVOLUTION AS AN UNDERUTILIZED TOOL FOR STUDYING BENEFICIAL HOST-MICROBE INTERACTIONS

II.1. INTRODUCTION

II.2. BENEFICIAL HOST-MICROBE INTERACTIONS: CURRENT QUESTIONS AND CHALLENGES

II.3. AN OVERVIEW OF EXPERIMENTAL EVOLUTION

II.4. UTILIZING EXPERIMENTAL EVOLUTION TO STUDY BENEFICIAL ANIMAL-MICROBE ASSOCIATIONS

III. THE EFFECTS OF BACILLUS SUBTILIS ON CAENORHABDITIS ELEGANS FITNESS AFTER HEAT STRESS 

III.1. INTRODUCTION

III.2. METHODS

III.3. RESULTS

III.4. DISCUSSION

IV. ASSOCIATION WITH A NOVEL BENEFICIAL MICROBE FACILITATES HOST ADAPTATION TO A STRESSFUL ENVIRONMENT

IV.1. INTRODUCTION

IV.2. METHODS

IV.3. RESULTS

IV.4. DISCUSSION

IV.5. SUPPLEMENTAL INFORMATION

V. THE EFFECTS OF MICROBIAL EVOLUTION AND COEVOLUTION ON HOST FITNESS

V.1. INTRODUCTION

V.2. METHODS

V.3. RESULTS

V.4. DISCUSSION

VI. CONCLUSION 

VI.1. SUMMARY AND DISCUSSION OF PREVIOUS CHAPTERS

VI.2. FUTURE DIRECTIONS 

REFERENCES 

About this Dissertation

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School	Laney Graduate School
Department	Biological and Biomedical Sciences
Subfield / Discipline	Population Biology, Ecology & Evolution
Degree	Ph.D.
Submission	Dissertation
Language	English
Research Field	Biology, Ecology Biology, Evolution and Development
Mot-clé	experimental evolution symbiosis Caenorhabditis elegans Bacillus subtilis
Committee Chair / Thesis Advisor	Nicole Gerardo, Emory University Levi Morran, Emory University
Committee Members	Timothy Read, Emory University William Ratcliff, Georgia Tech Daniel Weissman, Emory University

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