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Infection Strategies of Clade V Nematode Parasites by Way of Specific Effectors in Heterorhabditis Bacteriophora

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Infection Strategies of Clade V Nematode Parasites by Way of Specific Effectors in Heterorhabditis Bacteriophora Infection Strategies of Clade V Nematode Parasites by way of Specific Effectors in Heterorhabditis bacteriophora by Eric Kenney B.A. in Biology, May 2011, University of Maryland M.S. in Biological Sciences, August 2013, University of Maryland, Baltimore County A Dissertation submitted to The Faculty of The Columbian College of Arts and Sciences of The George Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy January 8, 2021 Dissertation directed by Ioannis Eleftherianos Associate Professor of Biology The Columbian College of Arts and Sciences of The George Washington University certifies that Eric Timothy Kenney has passed the final examination for the degree of Doctor of Philosophy as of September 11, 2020. This is the final and approved form of the dissertation. Infection Strategies of Clade V Nematode Parasites by way of Specific Effectors in Heterorhabditis bacteriophora Eric Kenney Dissertation Research Committee: Ioannis Eleftherianos, Associate Professor of Biology, Dissertation Director John Hawdon, Associate Professor of Microbiology, Immunology, and Tropical Medicine, Committee Member Damien O’Halloran, Associate Professor of Biology, Committee Member ii © Copyright 2021 by Eric Timothy Kenney All rights reserved iii Acknowledgments First and foremost, I would like to thank my research advisor, Dr. Ioannis Eleftherianos, for his continuous support and dedication to this project. His knowledge, work ethic, and professionalism have been a source of inspiration, and his mentorship has made the time I’ve spent in his lab deeply valuable to me. I have also long been grateful for the support of Dr. Damien O’Halloran and Dr. John Hawdon, not only for their invaluable input in shaping the experimental arc of this work, but also for their stalwart efforts in making this text more precise and effective. The depth and quality of their commentary on this project illustrate an uncommon level of care that is very much appreciated. In the same vein, I would also like to thank Dr. James Lok for agreeing to be a member of my dissertation committee and providing feedback on this thesis. A high level of gratitude is also owed to Dr. Leon Grayfer, Dr. L. Courtney Smith, and Dr. Mollie Manier for offering their expertise and material support. Their involvement has vastly improved this work, and I feel fortunate to have had the chance to learn from them and attempt to absorb a measure of their admirable research acumen. For contributing to a research community and support system that I could not have completed this project without, I thank past and present members of the Eleftherianos Lab as well as family and friends. Their kind words and actions have been a constant reminder to be a person as well as a scientist. iv Abstract Infection Strategies of Clade V Nematode Parasites by way of Specific Effectors in Heterorhabditis bacteriophora The entomopathogenic nematode Heterorhabditis bacteriophora is uniquely positioned to serve as a model for understanding the genetic basis of parasitism. Its close relationship to the model organism C. elegans provides a strong framework for interpreting genetic information and free-living nematode background. Additionally, H. bacteriophora has evolutionary proximity to a number of vertebrate-parasitic nematodes, so the information gleaned from the entomopathogen can be compared to these species to identify common virulence motifs. These aspects of the phylogenetic placement of H. bacteriophora have prompted a number of genomic and transcriptomic studies meant to highlight potential virulence factors, but the information gained from bioinformatic analyses is not always sufficient for understanding the contribution of a gene. The function of a given protein can often have equally plausible roles in regulating the parasite’s own physiology or interfering with that of the host, and this ambiguity calls for in vivo study of each candidate virulence factor’s ability to contribute to an infection. Before developing a system for characterizing virulence factors, the toxic or immunomodulatory effects of the parasite as a whole must first be examined. To this end, we injected concentrated H. bacteriophora excreted-secreted (ES) products from host- exposed nematodes into Drosophila melanogaster larvae and flies. We found that these products suppressed the expression of the antimicrobial peptide (AMP) Diptericin, and that the products were lethal to a subpopulation of flies. Notably, the finding that the nematode itself can produce lethal factors demonstrates that H. bacteriophora does not v rely entirely on the products of its bacterial symbiont, Photorhabdus luminescens, to kill the host. Following this foundational depiction of Heterorhabditis virulence, individual proteins that were predicted to be secreted were expressed in recombinant form and similarly injected into Drosophila to determine whether they might contribute to the observed effects. A putative UDP-glycosyltransferase (Hb-ugt-1), invertebrate-type lysozyme (Hb-ilys-1), and serine carboxypeptidase (Hb-sc-1) were examined in this manner, and each was shown to function as a virulence factor in vivo. Among other effects, Hb-ugt-1 and Hb-sc-1 were found to limit the upregulation of AMPs, Hb-ilys-1 suppressed the activity of phenoloxidase, and both Hb-sc-1 and Hb-ilys-1 contributed to the advancement of an infection by P. luminescens. These findings show that H. bacteriophora likely carries a rich and complex virulence arsenal, and understanding how individual effectors contribute to an infection could inform a variety of applications. Heterorhabditis nematodes are already commercially available as a means of biocontrol for insect pests, and enhanced trains could be developed by modulating the expression of known virulence factors. Additionally, information about H. bacteriophora effectors could be used to predict analogous roles for homologs in vertebrate-infective species, highlight those that are likely to be immunomodulatory, and guide the process of developing new treatments for helminth infections or inflammatory diseases. vi Table of Contents Acknowledgments ............................................................................................................ iv Abstract .............................................................................................................................. v List of Figures ................................................................................................................. viii List of Supplementary Material ...................................................................................... x Introduction ......................................................................................................................... 1 Chapter 1: Heterorhabditis bacteriophora excreted-secreted products enable infection by Photorhabdus luminescens through suppression of the Imd pathway ......................... 20 Chapter 2: A putative UDP-glycosyltransferase from Heterorhabditis bacteriophora suppresses antimicrobial peptide gene expression and factors related to ecdysone signaling. ........................................................................................................................... 60 Chapter 3: A putative lysozyme and serine carboxypeptidase from Heterorhabditis bacteriophora show differential virulence capacities in Drosophila melanogaster. ........ 93 Discussion ....................................................................................................................... 124 References ....................................................................................................................... 131 vii List of Figures Chapter 1 Figure 1. Exposure of Heterorhabditis bacteriophora infective juveniles (IJs) to host hemolymph induces the secretion of unique proteins ........................................... 51 Figure 2. Heterorhabditis bacteriophora nematode Excreted/Secreted (ES) products elicit differential Diptericin responses that are consistent across Drosophila melanogaster life stages ................................................................................................ 52 Figure 3. Differential Diptericin responses to ES products originate at or prior to transcriptional activation ............................................................................................... 53 Figure 4. Activated Heterorhabditis bacteriophora nematode Excreted/Secreted (ES) products are lethal to adult Drosophila melanogaster .......................................... 54 Figure 5. Triple-concentration of the Heterorhabditis bacteriophora nematode Excreted/Secreted (ES) products exacerbates Diptericin responses, but fails to elicit responses from other antimicrobial peptides ................................................................. 55 Figure 6. Co-injection of Escherichia coli with activated Heterorhabditis bacteriophora nematode Excreted/Secreted (ES) products results in fly mortality...... 56 Figure 7. The onset of mortality evoked by Photorhabdus luminescens infection is significantly advanced by Heterorhabditis bacteriophora nematode Excreted/Secreted activated products, but delayed by non-activated products ............ 57 Figure 8. Activated Heterorhabditis bacteriophora ES products enable the rapid proliferation of Photorhabdus luminescens during the early phase of an infection...... 58 Figure 9. Heterorhabditis bacteriophora nematode activated Excreted/Secreted (ES) products provoke
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