Bacterial Community Ecology of the Lone Star Tick (Amblyomma americanum) Open Access

Williams-Newkirk, Amanda Jo (2015)

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Vector-borne diseases dominate the list of emerging infections from the last century. Among arthropod vectors, ticks (Acari, Ixodida) transmit a greater diversity of disease causing organisms than any other known order. In the southeastern United States, the lone star tick (Amblyomma americanum) is the most abundant and aggressive human-biting tick and a vector of multiple known or suspected pathogens, including Rickettsia, Ehrlichia, Borrelia, and Heartland virus. The long life cycle of A. americanum and its broad host range complicate studies aimed at understanding the ecology of these diseases. Furthermore, abundant symbiotic bacteria, many of which are closely related to known pathogens, are a part of the tick's microbial community. Studies in this and other systems have robustly demonstrated that the non-pathogenic component of a vector's microbiome is capable of affecting the ability of the arthropod to acquire, maintain, and transmit pathogens to vertebrates. As a result, it is now recognized that pathogen ecology must be described in the context of the vector and the vector's microbiome. The aim of my dissertation was to provide the necessary context for further studies of A. americanum disease ecology. In my survey of A. americanum bacterial communities, I characterized the bacteria from 131 ticks collected from five sites in three states distributed throughout the species' eastern range. I then compared A. americanum's bacterial community to that of sympatric tick species of varying relatedness to determine if species with the opportunity to share hosts also shared similar microbiota and to look for evidence of the evolutionary history of the ticks in their bacterial communities. During these studies I detected multiple genotypes of a novel symbiont, Candidatus ‘Midichloria mitochondrii', in two Amblyomma species. In addition, I provided the first reference mitochondrial genome sequence for A. americanum, a tool that will be very important to future population genetics studies of this tick. My work provides a foundation for future studies in A. americanum by quantifying both intra and interspecific differences in bacterial communities, detecting new members of the bacterial community, and describing interactions between members which may now be targeted for characterization, metabolic evaluation, and functional studies.

Table of Contents

CHAPTER 1 pg. 1

Introduction: The evolution of tick microbiome research

1.1 Known effects of the tick microbiome on disease ecology pg. 2

1.2 Next generation sequencing as a tool for descriptive and

experimental microbiome studies pg. 6

1.3 Figures pg. 10

1.4 References pg. 11

CHAPTER 2 pg. 19

Presence, genetic variability, and potential significance of " Candidatus Midichloria mitochondrii" in the lone star tick Amblyomma americanum

2.1 Summary pg. 19

2.2 Introduction pg. 20

2.3 Materials and Methods pg. 22

2.4 Results pg. 25

2.5 Discussion pg. 26

2.6 Figures pg. 30

2.7 Tables pg. 33

2.8 References pg. 35

CHAPTER 3 pg. 40

Characterization of the bacterial communities of life stages of free living lone star ticks ( Amblyomma americanum)

3.1 Summary pg. 40

3.2 Introduction pg. 41

3.3 Materials and Methods pg. 44

3.4 Results pg. 52

3.5 Discussion pg. 57

3.6 Figures pg. 66

3.7 Tables pg. 84

3.8 References pg. 134

CHAPTER 4 pg. 151

Sex and species phylogenies influence the bacterial communities of four sympatric North American tick species

4.1 Summary pg. 151

4.2 Introduction pg. 152

4.3 Materials and Methods pg. 155

4.4 Results pg. 161

4.5 Discussion pg. 165

4.6 Figures pg. 176

4.7 Tables pg. 193

4.8 References pg. 231

CHAPTER 5 pg. 241

The mitochondrial genome of Amblyomma americanum

5.1 Summary pg. 241

5.2 Introduction pg. 241

5.3 Materials and Methods pg. 244

5.4 Results and Discussion pg. 250

5.5 Conclusions pg. 256

5.6 Figures pg. 257

5.7 Tables pg. 283

5.8 References pg. 285

CHAPTER 6 pg. 293

Strengths, limitations, and conclusions

6.1 Key Findings and Strengths pg. 293

6.2 Limitations pg. 298

6.3 Future Directions pg. 301

6.4 Figures pg. 303

6.5 References pg. 304

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