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The Host-Pathogen Relationship in Rickettsia: Epidemiological Analysis of Rmsf in Ohio and a Comparative Molecular Analysis of Four Vir Genes

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THE HOST-PATHOGEN RELATIONSHIP IN RICKETTSIA: EPIDEMIOLOGICAL ANALYSIS OF RMSF IN OHIO AND A COMPARATIVE MOLECULAR ANALYSIS OF FOUR VIR GENES DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Jennifer R. Carmichael, B.S. ***** The Ohio State University 2008 Dissertation Committee: Approved by Paul A. Fuerst, Advisor Gustavo Leone _________________________________ Arthur Burghes Advisor Graduate Program in Molecular Genetics Glen Needham ABSTRACT Members of the vector-borne bacterial genus Rickettsia represent an emerging infectious disease threat and have continually been implicated in epidemics worldwide. It is of vital importance to understand the geographical distribution of disease and rickettsial-infected arthropods vectors. In addition, understanding the dynamics of the relationship between rickettsiae and their arthropod hosts will help aid in identifying important factors for virulence. Dermacentor variabilis dog ticks are the main vector in the eastern United States for Rickettsia rickettsii, the etiological agent of Rocky Mountain spotted fever. The frequency of rickettsial-infected ticks and their geographical location in Ohio over the last twenty years was analyzed. The frequency of rickettsial species was found to remain relatively constant (about 20%), but the incidence of R. rickettsii has increased from 6 to 16%. Also, the geographic distribution of rickettsial-positive ticks has expanded, corresponding to a rise of RMSF in these new areas. Type IV secretion system genes, like the vir group, are important for pathogenicity in many pathogens, but have not been analyzed in Rickettsia. Four vir genes, virB8, virB11, virB4, and virD4 were analyzed in Rickettsia amblyommii infected Amblyomma americanum Lone Star ticks from across the Northeast United States. Results showed that important protein motifs are mutated or absent. This evidence ii suggests the vir genes may not be functional in Rickettsia or they have evolved a novel role. In addition, analysis of virD4 showed that isolates were most similar to Rickettsia conorii and R. rickettsii, two highly pathogenic species. To determine if these genes are important for virulence, a novel qPCR approach was designed to compare the RNA expression in R. amblyommii-infected A. americanum tick and Vero cells. Here, expression of virB8 and virD4 was increased in Vero cells, while virB4 and virB11 had decreased expression. Since rickettsiae cause disease in humans, increases in expression levels in the mammalian Vero cells may be important for pathogenicity. Understanding all levels of disease, from basic biology and epidemiology, analysis of potential virulence genes, and functional analysis via RNA expression, contributes information that leads us closer to determining the process of rickettsial pathogenicity. iii Dedicated to my parents, Becky and John, and my sisters, Susie and Stephanie, without them none of this would have been possible Dedicated to Stephen Nye, who in death gave purpose to my work iv ACKNOWLEDGMENTS I would like to thank my advisor, Paul Fuerst, for giving me this opportunity and for his patience and advice. I would also like to thank all members of the Fuerst laboratory. This includes Greg Booton, Megan Shoff, Mike Sovic, and Daryl Kelly who I consider friends in addition to colleagues. I would also like to thank Megan for her helpful edits and suggestions. My Molecular Genetics classmates, Leena, Maria, Ryan, Stephen, and Casey have not only helped me through classes but have provided continued support and advice. Thanks to many members of the Gibbs lab, Chrissy, Kody, Jimmy, Tony, Liam and Jose, for invaluable advice, conversation, laughs, and friendship. These times have provided much needed stress relief and I looked forward to lunch every day. Also, I would like to thank Monica and Kaylan, whose friendships are highly valuable to me. There are many people outside the university that have also made all of this possible. I would like to thank my parents and my sisters, for always being there for me and giving me the motivation to succeed. Thanks to Beth Askue, Bela Bhatt, and Donna Winters who kept me in good health throughout these years; I can not express in words how much I am thankful for this. I would like to thank Joshua, without you there would be no figures in my thesis, and whose love and support I treasure close to my heart. v VITA March 8, 1979………………………………Born – Greensburg, PA 2001…………………………………………B.S., summa cum laude Lock Haven University of Pennsylvania 2001-2007…………………………………..Graduate Teaching Associate Graduate Research Associate Department of Molecular Genetics The Ohio State University 2007-2008………….……………………….Graduate Research Associate Department of Molecular Genetics The Ohio State University PUBLICATIONS 1. Carmichael, J. and P. Fuerst. 2006. A Rickettsial mixed infection in a Dermacentor variabilis tick from Ohio. Annals of the New York Academy of Sciences 1078: 334–337. 2. Kelly, D., J. Carmichael, G.C. Booton, K.F. Poetter and P.A. Fuerst. 2006. Novel Spotted Fever Group Rickettsiae (SFGR) infecting Amblyomma americanum ticks in Ohio, USA. Annals of the New York Academy of Sciences 1063: 352-355. 3. Booton, G.C., J.R. Carmichael, F.L. Schuster, P.A. Fuerst, T.J. Byers. 2003. Balamuthia mandrillaris: Identification of Clinical and Environmental Isolates Using Genus-Specific PCR. Journal of Eukaryotic Microbiology 50: 508-509. vi 4. Booton, G.C., J.R. Carmichael, G.S. Visvesvara, T.J. Byers and P.A. Fuerst. 2003. Genotyping of Balamuthia mandrillaris based on nuclear 18S and mitochondrial 16S rRNA genes. American Journal of Tropical Medicine and Hygiene 68: 65-69. 5. Booton, G.C., J.R. Carmichael, G.S. Visvesvara, T.J. Byers and P.A. Fuerst. 2003. PCR identification of Balamuthia mandrillaris using the mitochondrial 16S rRNA gene as a target. Journal of Clinical Microbiology 41: 453-455. FIELDS OF STUDY Major Field: Molecular Genetics vii TABLE OF CONTENTS Page Abstract……………………………………………………………………………... ii Dedication………………………………………………………………………...... iv Acknowledgements………………………………………………………………… v Vita…………………………………………………………………………………. vi List of Tables……………………………………………………………………….. x List of Figures……………………………………………………………………… xii List of Abbreviations……………………………………………………………….. xv Chapters: 1. Introduction…………………………………………………………………... 1 Aims………………………………………………………………………. 24 2. Trends in Dermacentor variabilis dog ticks infected with the agent of Rocky Mountain spotted fever, Rickettsia rickettsii, and cases of clinical disease in Ohio over a twenty year time period……………………..………………….. 37 Materials and methods……………………………………………………. 39 Results……………………………………………………………………. 44 Discussion………………………………………………………………… 49 Summary………………………………………………………………….. 56 3. Variability in the mitochondrial control region and 12S rDNA gene among Dermacentor variabilis ticks……...…………………………………………. 61 Materials and methods……………………………………………………. 63 Results……………………………………………………………………. 66 Discussion………………………………………………………………… 73 viii 4. Molecular and Phylogeograhpical analysis of the vir genes, virB8, virB11, virB4, and virD4, from Rickettsia amblyommii isolates from the northeast United States……………..………………………………………………….. 81 Materials and methods……………………………………………………. 86 Results…………………………………………………………………….. 90 Discussion………………………………………………………………… 100 5. Differential expression of vir genes between mammalian and arthropod cells infected with Rickettsia amblyommii……..………………………………….. 104 Materials and Methods...…………………………………………………. 107 Results..…………………………………………………………………... 117 Discussion…..……………………………………………………………. 140 6. Summary and Conclusions…………………………………………………... 147 Bibliography………………………………………………………………………... 151 Appendix A: Nucleotide Sequences………………………………………………... 166 ix LIST OF TABLES Table Page 1 Comparison of number of Dermacentor variabilis ticks positive for Rickettsia sp. by the 17kDa surface antigen gene and DFA methods….. 45 2 Number of rickettsial-infected Dermacentor variabilis submitted from Ohio counties in the years 1983-6 and 2003-4…………………………. 48 3 RMSF cases per county in Ohio for the years 1981-86 and 2003-4…… 53 4 Number of Dermacentor variabilis ticks analyzed for the 3’ 12S rDNA/D-loop gene region classified by geographical location................ 68 5 Number of Dermacentor variabilis ticks analyzed for the 5’12S rDNA gene region classified by geographical region………………………….. 71 6 Molecular analysis of the 17kDa surface antigen gene in Dermacentor variabilis ticks analyzed for the D-loop region and 12 rDNA…………. 78 7 vir genes PCR and sequencing primers and annealing temperatures…… 89 8 Geographical locations of Rickettsia amblyommii-infected Amblyomma americanum ticks analyzed for vir genes……………………………….. 91 9 Trypsin diluent ingredients per 2.5 L solution………………………….. 109 10 RNA concentrations and amounts used in RT-PCR of R. amblyommii- infected and uninfected Vero, 34oC, and 24oC Ambylomma americanum cell cultures……………………………………………………………… 111 11 Sequences of primers used in qPCR for virB8, virB11, virB4, virD4, and gltA………………………………………………………………….. 112 12 Sequences and annealing temperatures of PCR primers used to amplify vir genes…………………………………………………………………. 114 x 13 virD4 qPCR amplification and melt curve data………………………… 121 14 virB4 qPCR amplification and melt curve data…………………………. 126 15 virB8 qPCR amplification and melt curve data…………………………. 130 16 virB11 qPCR amplification and melt curve data………………………... 134 17 gltA qPCR amplification and melt
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    12.5 10.0 7.5 5.0 Distance, number of nodes 2.5 0.0 g1 g2 g3 g3.5 g4 g5 g6 g7 g8 g9 g10 g10.1 g11 g12 g13 g14 g15 (11) (3) (3) (10) (3) (3) (3) (3) (3) (3) (3) (4) (3) (3) (3) (2) (3) LC-locus alignment sites Supplementary Figure S1. Compatibility of the evolutionary histories of the LC-locus and of individual LC genes.The sites of the LC-locus alignment are arranged along the X-axis, with the dashed red lines demarcating the alignment boundaries of the individual RcGTA-like genes (labeled with RcGTA gene names, g1 through g15; see Supplementary Table S4). For each alignment site, the Y-axis shows the phylogenetic distance between the optimal placement of a taxon in a phylogeny reconstructed from a 100 amino-acid window that surrounds the site and in the LC-locus phylogeny, averaged across all sliding windows that contain the site. The Y-axis values averaged across all taxa and all sites within a gene is shown in parentheses on the X-axis. For 15 out of 17 genes, only 2-4 nodes separate the optimal taxon position in the LC-locus and gene phylogeny. The inflated distances for g1 and g3.5 are likely because only 15 and 21 of 95 LCs, respectively, have a homolog of these genes and the SSPB analysis is highly sensitive to missing data (Berger et al. 2011). a. Bacteria Unassigned Thermotogae Tenericutes Synergistetes Spirochaetes Proteobacteria ylum Planctomycetes h p Firmicutes Deferribacteres Cyanobacteria Chloroflexi Bacteroidetes Actinobacteria Acidobacteria 1(11,750) 2(1,750) 3(2,538) 4(168) 5(51) 6(54) 7(43) 8(32) 9(26) 10(40) 11(33) 12(198) 13(173) 14(101) 15(98) 16(43) 17(114) Number of rcc01682−rcc01698 homologs in a cluster b.
  • Health: Epidemiology Subchapter 41A

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