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ABSTRACT JOHNSON, CONNIE RAE. Molecular Characterization of Host

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ABSTRACT JOHNSON, CONNIE RAE. Molecular Characterization of Host ABSTRACT JOHNSON, CONNIE RAE. Molecular Characterization of Host Feeding Patterns and Pathogen Infection Prevalence among Ixodid Tick Vectors in the Piedmont and Coastal Plain of North Carolina. (Under the direction of Dr. Charles S Apperson). Among tick-borne diseases reportable to the United States Centers for Disease Control and Prevention (CDC), Lyme disease (LD) is the most commonly reported while Spotted Fever Group (SFG) Rickettsioses cause the most severe and potentially fatal illness. North Carolina holds the distinction of being ranked among the states reporting the highest number of SFG Rickettsioses to the CDC. While Rocky Mountain Spotted Fever (RMSF), caused by Rickettsia rickettsii, is the cause of severe and potentially fatal disease, the majority of mild cases of SFG Rickettsioses are likely caused by other SFG Rickettsia. Rickettsia parkeri is known to be present in North Carolina ticks, transmitted by the Gulf Coast Tick, Amblyomma maculatum Koch. The competent vertebrate reservoir for R. parkeri is not yet known. One objective of this study was to identify the important vertebrate hosts of A. maculatum and determine if there was an association with R. parkeri pathogen prevalence. Ticks were collected from a reconstructed Piedmont prairie in Wake County, North Carolina. Molecular tools were employed to determine pathogen prevalence and identify the blood meal remnants from host seeking ticks. Pathogen prevalence was determined through PCR amplification and visualization of the R. parkeri outer membrane protein A. The reverse line blot hybridization (RLBH) assay was used to detect vertebrate blood meals through amplification of a 12S rDNA gene fragment and hybridization against 38 vertebrate probes. Rickettsia parkeri was detected among 36.9% (45/122) A. maculatum adults and 33.3% (2/6) nymphs as well as in a single male lone star tick, Amblyomma americanum Linneaus (2.3%; 1/43). Although no statistically significant association was observed between blood meal host and pathogen prevalence, the cotton rat, Sigmodon hispidus Say and Ord, was the most common blood meal host identified among 59.0% (36/61) of adult A. maculatum illustrating its importance as a maintenance host for this tick species. In the Coastal Plain region of the southeastern United States, two sympatric tick species, Ixodes affinis Neumann and I. scapularis Say are infected with the LD spirochete, Borrelia burgdorferi sensu lato (s.l.). Ixodes affinis is an enzootic vector of B. burgdorferi s.l., has a narrow feeding preference and is not thought to readily bite humans. Ixodes scapularis is a generalist feeder and is the primary bridge vector in the Eastern United States transmitting the LD pathogen to humans. This study investigated if an association occurred between B. burgdorferi s.l. infection prevalence and vertebrate hosts utilized by these two morphologically similar and sympatric tick species in the Coastal Plain of North Carolina. Pathogen prevalence was determined through amplification of the Borrelia burgdorferi s.l. flaB gene, rrfA-rrlB IGS, and a B. burgdorferi sensu stricto (s.s.)-specific rrs-rrlA ITS fragment. The RLBH assay was used to identify vertebrate hosts as well as molecularly confirm tick identifications. Statistically significant differences were observed in B. burgdorferi s.l. infection between I. affinis (80%; 68/85) and I. scapularis (46.8%; 44/94). Two B. burgdorferi s.l. genospecies were identified through Sanger sequencing of the flaB gene fragment, including the LD agent itself, B. burgdorferi sensu stricto (s.s.) which was detected among both I. affinis (52.9%; 55/85) and I. scapularis (35.1%; 33/94) and Borrelia bissettii, only known to cause human illness in Europe, was detected at a lower prevalence among I. affinis (11.8%; 10/85) and I. scapularis (4.3%; 4/94). While no statistically significant association between blood meal host and pathogen prevalence was observed among I. affinis or I. scapularis, cotton rat and Canis spp. were the most frequently detected blood meals among both tick species indicating that these vertebrates may play an important role in LD transmission among these sympatric ticks. © Copyright 2021 by Connie Rae Johnson All Rights Reserved Molecular Characterization of Host Feeding Patterns and Pathogen Infection Prevalence among Ixodid Tick Vectors in the Piedmont and Coastal Plain of North Carolina by Connie Rae Johnson A dissertation submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Entomology Raleigh, North Carolina 2021 APPROVED BY: _______________________________ _______________________________ Charles S. Apperson R. Michael Roe Committee Chair _______________________________ _______________________________ Edward Breitschwerdt Edward Vargo DEDICATION To my mother, Wanda Johnson, who was my greatest champion and best friend. ii BIOGRAPHY Connie Rae Johnson is a native of Texas. She attended Texas State University and earned a Bachelor of Science in General Biology in 1996 and a Master of Science in Aquatic Biology in 2001 under the direction of Dr. Alan Groeger; her thesis examined the longitudinal distribution of zooplankton and phytoplankton in a central Texas reservoir. She was then employed as an Aquatic Scientist by the Texas Commission on Environmental Quality where she worked in the Public Drinking Water Section’s Source Water Assessment and Protection team. In 2006, she earned a second, non-thesis Master of Agriculture in Economic Entomology from Texas A&M University under the direction of Dr. Jimmy Olsen where she completed a professional internship conducting West Nile virus surveillance for The Woodlands, Texas. Connie joined the United States Navy in 2005 as a medical entomologist in the Medical Service Corps. In 2009 she was selected for the Navy’s Duty Under Instruction program to pursue a PhD in Entomology and began her 3-year duty assignment as a graduate student at North Carolina State University under Dr. Charles Apperson. iii ACKNOWLEDGMENTS I am grateful to my friends, family and my Navy leadership who have supported and encouraged me along the way in conducting this research and completing this doctoral program. In particular, I express deep appreciation to my graduate advisor, Dr. Charles Apperson for his patience, support and mentorship. I also thank my committee members for their time and valuable direction, Dr. R. Michael Roe who served as my minor advisor, Dr. Edward Breitschwerdt who served as my graduate representative, and Dr. Edward Vargo. To Dr. Loganathan Ponnusamy for serving as special consultant on my committee, providing guidance and direction and for his mentorship in helping me build my molecular skill set. Dr. Allen Richards of the Navy Medical Research Command provided guidance and supplies for the Rickettsia parkeri project. Mr. Alden Estep of the United States Department of Agriculture’s Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL provided guidance and technical support in nanopore sequencing. Haley Thornton Sutton and Dr. Sangmi Lee, both formerly of the Dearstyne Laboratory, assisted in performing DNA extractions and troubleshooting the RLBH assay, respectively. To the North Carolina Museum of Natural Sciences (NCMNS) staff including Lisa Gatens who allowed me to volunteer in the Prairie Ridge Ecostation small mammal survey and Charles Yelton who provided historical knowledge of that site. Vertebrate tissues used in this research were obtained from the NCMNS tissue collection, Louisiana State University Museum of Natural Science Collection of Genetic Resources and the North Wildlife Resources Commission. Funding for this project was provided in part by a student grant from the Armed Forces Pest Management Board’s Deployed Warfighter Protection Fund. iv TABLE OF CONTENTS LIST OF TABLES ....................................................................................................................... vii LIST OF FIGURES .................................................................................................................... viii Chapter 1: Molecular Analyses of Blood Meal Hosts and Prevalence of Rickettsia parkeri in the Gulf Coast Tick Amblyomma maculatum (Acari: Ixodidae) from a Reconstructed Piedmont Prairie Ecosystem, North Carolina .......................................................................... 1 Abstract .............................................................................................................................. 2 Introduction ........................................................................................................................ 3 Materials and Methods ....................................................................................................... 7 Study Site and Field Tick Collection ..................................................................... 7 DNA Extraction from Ticks and Vertebrate Tissues ............................................. 8 Pathogen Detection ................................................................................................ 9 Identification of Host DNA ................................................................................. 11 Host Probe Development ......................................................................... 11 Reverse Line Blot Hybridization Assay .................................................. 12 Sensitivity and Specificity of Reverse Line Blot Hybridization
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