The microbial symbiont of an agricultural insect pest affects pathogen vectoring across scales Restricted; Files Only

Mendiola, Sandra (Fall 2023)

Permanent URL: https://etd.library.emory.edu/concern/etds/vh53ww99b?locale=en
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Abstract

Many insects form intimate associations, known as symbioses, with select microbes. Some symbioses can influence traits that contribute to vector competence—an insect vector’s ability to harbor and transmit a pathogen. Leveraging symbioses to mitigate the burden of agricultural vector-borne diseases has gained traction in recent years; however, implementation of these tactics requires a deeper understanding of the impact of symbionts on pathogen vectoring in individual insects and, more importantly, their implications for population-level pathogen transmission.

My dissertation uses the squash bug (Anasa tristis) to address how symbiotic microbes influence pathogen vectoring by an insect host. A. tristis is a pest of commercial cucurbit crops and the only confirmed vector of Serratia marcescens, causative agent of Cucurbit Yellow Vine Disease (CYVD). A. tristis forms symbiotic associations with bacteria in the genus Caballeronia, which colonizes specialized structures in their gut, known as crypts. Previous work has shown that Caballeronia accelerates host development and decreases mortality relative to symbiont-free (aposymbiotic) individuals.

My dissertation employs a multiscale approach to study the interactions between A. tristis, Caballeronia, and S. marcescens. Within individual insects, I demonstrated that Caballeronia has a marked effect on S. marcescens infection, with symbiotic individuals having shorter infections of lower intensity than their aposymbiotic counterparts. I also investigated how Caballeronia influences insect gene expression and its consequences for pathogen establishment. To see the impact of these findings on insect populations, I created a model of CYVD transmission that explicitly accounts for the presence of symbiotic and aposymbiotic bugs. I showed that aposymbiotic bugs contribute disproportionately to plant infections and high symbiont coverage in insects is needed for effective pathogen control.

To fully realize the potential of insect-microbe symbioses in combating vector borne disease, we must first understand how symbionts interact with pathogens within their insect hosts and ensure that patterns observed at the individual level have the desired effect when scaled to entire populations. My work investigating the influence of symbiotic microbes on A. tristis across scales provides a framework for the integration of vector biology and disease ecology to investigate the interactions between insects, pathogens, and symbionts.

Table of Contents

Table of Contents

Title page. ii

Abstract iv

Acknowledgments. vii

Table of Contents. xi

List of Figures and Tables. xiii

Chapter I: Introduction. 1

Summary of Dissertation Chapters. 4

References. 9

Chapter II: An integrative approach to symbiont-mediated vector control for agricultural pathogens. 15

Abstract 15

Introduction. 16

Overview of symbiont-mediated vector control 17

Integrative research to advance symbiont-mediated vector control 21

Conclusion. 24

Acknowledgments. 24

References. 26

Chapter III: Competitive Exclusion of phytopathogenic Serratia marcescens from squash bug vectors by the gut endosymbiont Caballeronia. 31

Abstract 31

Introduction. 32

Results. 34

Discussion. 39

Materials & Methods. 43

Acknowledgments. 47

Supplementary Material 48

References. 51

Chapter IV: Ecological modeling evaluates the potential impacts of symbionts on plant pathogen vectoring in field populations. 60

Abstract 60

Introduction. 61

Methods. 63

Results. 70

Discussion. 78

References. 85

Chapter V: Differential gene expression in the insect vector Anasa tristis in response to symbiont colonization but not infection with the phytopathogen Serratia marcescens. 92

Abstract 92

Introduction. 93

Methods. 95

Results. 101

Discussion. 110

Supplementary Material 116

References. 118

Chapter VI: Conclusion. 124

Summary and discussion of previous chapters. 124

Future directions. 128

References. 130

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