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Ecology of Cryptosporidium Parasites in Wild Rodent Populations

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Ecology of Cryptosporidium Parasites in Wild Rodent Populations ECOLOGY OF CRYPTOSPORIDIUM PARASITES IN WILD RODENT POPULATIONS A Dissertation Submitted to the Graduate Faculty of the North Dakota State University of Agriculture and Applied Science By Brianna Leigh Schneck Stenger In Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Major Program: Environmental and Conservation Sciences Option: Conservation Biology November 2014 Fargo, North Dakota North Dakota State University Graduate School Title ECOLOGY OF CRYPTOSPORIDIUM PARASITES IN WILD RODENT POPULATIONS By Brianna Leigh Schneck Stenger The Supervisory Committee certifies that this disquisition complies with North Dakota State University’s regulations and meets the accepted standards for the degree of DOCTOR OF PHILOSOPHY SUPERVISORY COMMITTEE: Dr. John McEvoy Co-Chair Dr. Mark Clark Co-Chair Dr. Wendy Reed Dr. Eakalak Khan Approved: 04/13/2015 Dr. Eakalak Khan Date Department Chair ABSTRACT Cryptosporidium is a genus of ubiquitous parasites that have been detected worldwide in nearly 500 species of amphibians, birds, fish, mammals, and reptiles. Most research has focused on the Cryptosporidium species and genotypes infecting humans and livestock, because of the public health significance and economic importance of the diarrheal disease cryptosporidiosis. Relatively little is known about Cryptosporidium-host dynamics in wildlife hosts, even though a wide range of wildlife species are susceptible to Cryptosporidium. Insights into ecology and host-parasite dynamics in wild populations are necessary to understand the biology and evolution of Cryptosporidium; to predict the emergence of human and livestock pathogens; and to clarify Cryptosporidium taxonomy and systematics. The focus of this research was to study the ecology of Cryptosporidium in populations of cricetid (voles, Peromyscus mice, muskrats) and sciurid (squirrels and chipmunks) rodents, and characterize Cryptosporidium taxa by sequencing multiple genetic loci (18S rRNA and actin genes). Paralogous copies of the 18S rRNA gene in Cryptosporidium genotypes from wild rodents were common and affected phylogenetic inferences. Eastern chipmunks (Tamias striatus) were infected with Cryptosporidium chipmunk genotype II, which had 18S rRNA gene paralogs that shared ~93% similarity. The degree of divergence has not been previously described in any Cryptosporidium taxa, but is similar to the divergence described in Plasmodium species, which have functionally distinct 18S rRNA gene copies. Marmotini squirrels were mainly host to novel Cryptosporidium genotypes, and to the best of our knowledge, we provide the first molecular characterization of Cryptosporidium in black-tailed prairie dogs (Cynomys ludovicianus). Cryptosporidium host adaptation and specificity was not evident in in Sciurini rodents and they were host to two zoonotic taxa, C. ubiquitum and Cryptosporidium skunk genotype. In conclusion, Cryptosporidium was prevalent in cricetid and sciurid rodents, and the extent of host adaptation varied among Cryptosporidium taxa as they are likely shaped by differences in host-parasite ecology and evolution. The rodents sampled are not significant reservoirs of zoonotic Cryptosporidium, with the exception of tree squirrels. Sequencing multiple genetic loci helped identify the presence of paralogs and resolve cryptic Cryptosporidium taxa, which strengthened phylogenetic inferences leading to a better understanding of Cryptosporidium systematics. iii ACKNOWLEDGEMENTS This dissertation would not have been possible without the assistance, encouragement, and support of many people. I’d sincerely like to thank my advisors, Drs. John McEvoy and Mark Clark, for their continued guidance and allowing me to work on this interdisciplinary project. Also, for providing me with opportunities to teach and work on various other projects. I also want to thank Dr. Wendy Reed, Dr. Margaret Khaitsa, and Dr. Eakalak Khan for serving on my committee and for their continued support, patience, and encouragement. I also sincerely thank Dr. Martin Kváč for being an amazing collaborator and his willingness to help. I cannot thank Cathy Giddings enough for all she has done for me (and other students) in and outside of the lab. I have learned so many things from her, which have helped me become a better scientist and person. She knew exactly when it was time for a Dairy Queen break or Redhawks game. Many thanks go out to all the McEvoy Lab grad students including Chris, Adam, and Tu for their friendship, willingness to help, and random brainstorming sessions. Also, thanks to the many undergraduate students that helped me both in the field and the lab, without them, I have no doubt I’d still be in the collection and PCR stage. Thank you to the staff and faculty of the Dept. of Veterinary and Microbiological Sciences, Dept. of Biological Sciences, the Environmental & Conservation Sciences Program, and the Graduate School for their general assistance throughout the years I have been at NDSU. Mainly, Dr. Craig Stockwell, Dr. Will Bleier, Dr. Donna Jacob, Dr. Marinus Otte, Madonna Fitzgerald, Jerie Little, Phyllis Murray, Sandy Erickson, and Suzy Schmoll, who have kept normal day-to-day things moving, paperwork flowing, or allowed me to invade their property in my search for small mammals with Cryptosporidium. Finally, I can’t thank my family enough for their unending support, encouragement, guidance, help, and love. My parents, Bob and Cyndi, and brother, Nathan, for helping me get to this point in many different ways. Lastly, my husband John, for his continued love and support. iv TABLE OF CONTENTS ABSTRACT ................................................................................................................................................. iii ACKNOWLEDGEMENTS ........................................................................................................................... iv LIST OF TABLES ........................................................................................................................................ ix LIST OF FIGURES ....................................................................................................................................... x GENERAL INTRODUCTION ........................................................................................................................ 1 Introduction ...................................................................................................................................... 1 Literature Review ............................................................................................................................. 1 Discovery and first description of Cryptosporidium ............................................................. 1 Cryptosporidium life cycle ................................................................................................... 3 Transmission ....................................................................................................................... 4 Cryptosporidium identification ............................................................................................. 5 Cryptosporidium taxonomy ................................................................................................. 5 18S rRNA gene ................................................................................................................. 10 Cryptosporidium in vertebrate animals ............................................................................. 11 Cryptosporidium in fish ........................................................................................ 11 Cryptosporidium in amphibians ............................................................................ 12 Cryptosporidium in reptiles .................................................................................. 12 Cryptosporidium in birds ...................................................................................... 13 Cryptosporidium in mammals .............................................................................. 14 Dissertation Objectives .................................................................................................................. 27 References ..................................................................................................................................... 27 PAPER 1. HIGHLY DIVERGENT 18S RRNA GENE PARALOGS IN A CRYPTOSPORIDIUM GENOTYPE FROM EASTERN CHIPMUNKS (TAMIAS STRIATUS) ........................................................ 44 Abstract .......................................................................................................................................... 44 Introduction .................................................................................................................................... 44 Materials and Methods ................................................................................................................... 46 Sample collection .............................................................................................................. 46 DNA isolation and PCR ..................................................................................................... 46 v Sequencing and phylogenetic analyses............................................................................ 48 Oocyst purification and morphometric analysis ................................................................ 49 Tissue sample collection and histology............................................................................
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