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PHYSELLA ACUTA, COMPARATIVE IMMUNOLOGY and EVOLUTIONARY ASPECTS of GASTROPOD IMMUNE FUNCTION Jonathan H

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University of New Mexico UNM Digital Repository Biology ETDs Electronic Theses and Dissertations Fall 12-12-2018 PHYSELLA ACUTA, COMPARATIVE IMMUNOLOGY AND EVOLUTIONARY ASPECTS OF GASTROPOD IMMUNE FUNCTION Jonathan H. Schultz University of New Mexico - Main Campus Follow this and additional works at: https://digitalrepository.unm.edu/biol_etds Part of the Bioinformatics Commons, Biology Commons, Computational Biology Commons, Genomics Commons, Immunity Commons, and the Parasitology Commons Recommended Citation Schultz, Jonathan H.. "PHYSELLA ACUTA, COMPARATIVE IMMUNOLOGY AND EVOLUTIONARY ASPECTS OF GASTROPOD IMMUNE FUNCTION." (2018). https://digitalrepository.unm.edu/biol_etds/311 This Dissertation is brought to you for free and open access by the Electronic Theses and Dissertations at UNM Digital Repository. It has been accepted for inclusion in Biology ETDs by an authorized administrator of UNM Digital Repository. For more information, please contact [email protected]. Jonathan H. Schultz_______________________ candidate Biology_________________________________ Department This dissertation is approved, and is acceptable in quality and form for publication: Approved by the Dissertation Committee: Dr. Coenraad M. Adema, Chairperson_____________________________________________ Dr. Eric S. Loker_____________________________________________________ Dr. Irene Salinas_____________________________________________________ Dr. Patrick Hanington_________________________________________________ i PHYSELLA ACUTA, COMPARATIVE IMMUNOLOGY AND EVOLUTIONARY ASPECTS OF GASTROPOD IMMUNE FUNCTION By Jonathan H. Schultz B.A., Biology, State University of New York at Geneseo, 2012 DISSERTATION Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Ph.D. in Biology Center for Evolutionary and Theoretical Immunology (CETI) The University of New Mexico Albuquerque, New Mexico May, 2019 ii DEDICATION For my nephews Jackson Jonathan and Ian James. The next generation of critical thinkers. iii ACKNOWLEDGMENTS I’d like to especially thank my advisor, colleague, and friend Dr. Coen M. Adema. I knew very little about the scientific endeavor entering graduate school and I thank you for accepting me into your program and elevating my career in science. I look forward to continuing our impassioned discussions of comparative immunobiology. Thank you to my committee members Dr. Irene Salinas, Dr. Eric S. Loker, and Dr. Patrick Hanington. Irene, thank you for your continued support and guidance, especially the push to attend NACI in North Carolina, which set the course of direction for my postdoctoral studies. Sam, thank you for opening my eyes to the world of evolutionary immunology during my very first semester at UNM and thank you for the support from CETI throughout the years. Patrick, thank you for the enlightening discussions on snail immunity and for supporting me through the end of my PhD. Thank you to Dr. Susan Bandoni-Muench, my first mentor in science. The drive to pursue a career as a scientist started because of taking your parasitology course at SUNY Geneseo and led me on my path to UNM. I am forever grateful. Thank you to my lab and office mates near and far: Dr. Janeth Peña, Lijun Lu, Journey Nolan, and Erin Watson. We shared some of the highs and lows of graduate school together and there isn’t a better group of people to spend the time with. I wish you all continued success and happiness. The utmost gratitude to my closest friends Arthur Tackman, Ben Wheaton, Bishoy Kamel, Danielle Griegos, Erica and Dan Ebbs, and Nate Holscher. Thank you for all of the support and friendship that will last beyond my years in Albuquerque. A very special shout out to my roommate and confidant Joshua Lynn. I couldn’t ask for a better friend. iv Love and thanks to my family. My brother Justin, Nikki, and JJ, thank you for everything, especially the nightly vid chats. There just aren’t enough words. To my Mom, Dad, and Aunt Ronni, for your continued support and for travelling all those miles to see me defend. And lastly, thanks to my ride or die PhD pup and travel buddy, Bo (a.k.a. THE BEANZ), seeing me through it all. v PHYSELLA ACUTA, COMPARATIVE IMMUNOLOGY AND EVOLUTIONARY ASPECTS OF GASTROPOD IMMUNE FUNCTION By Jonathan H. Schultz B.A., Biology, State University of New York at Geneseo, 2012 Ph.D., Biology, University of New Mexico, 2019 ABSTRACT Gastropod immunobiology has benefitted from investigations focused on the planorbid snail Biomphalaria glabrata, intermediate host for the human parasite Schistosoma mansoni. Though such concentrated efforts have elucidated fascinating aspects of invertebrate immunity, they have not provided full knowledge regarding the evolution of immune function among other gastropod species. This dissertation presents the importance of making strategic choices regarding which organisms to select for comparative immunology. Herein, the choice was made to investigate the immunobiology of Physella acuta, a freshwater snail species of the Physidae, a sister family to Planorbidae to which B. glabrata belongs. Benefiting greatly from the use of next-generation sequencing (NGS), the immunobiology of P. acuta was studied using 454 pyrosequencing, Illumina RNA-seq, experimental infections with Echinostoma paraensei (trematode parasite), and other molecular techniques. These analyses revealed that many components of gastropod immunity have been conserved among physid and planorbid snails. Also, P. acuta displays differences in immune function, such as the use of fibrinogen-related proteins in response to trematode parasite exposure. Remarkably, P. acuta differentially expressed relatively large immune-relevant gene families (CD109/TEP, dermatopin, GTPase IMAP, among others) after exposure to E. paraenesi. Inspection of the individual members that represent these gene families vi demonstrated complex transcriptional profiles that suggest parasite influence on host immune function and the capacity of a host to maintain homeostasis while supporting parasite development, an extended phenotype of E. paraenesi. These lab-based studies represent the first large scale characterizations of P. acuta immune function. The immune factors described through NGS approaches enable investigations of the ecoimmunology of P. acuta snails collected from the field. This approach uncovered many sequences that are differentially expressed by P. acuta naturally in the field relative to the lab environment. There is variation in the expression of certain antimicrobial factors and genes governing biological processes. Overall, this dissertation has expanded the scope of gastropod immunity and provides resources and insights that are accessible for continued development and understanding of evolutionary and comparative immunology concepts. vii TABLE OF CONTENTS CHAPTER 1: ……………………….…………………………………………………………………1 INTRODUCTION……………………………………………………………………….1 COMPARATIVE IMMUNOLOGY………………………………………………………………1 GASTROPOD IMMUNOLOGY………………………………………………………………….3 PHYSELLA ACUTA………………………………………………………………………………..5 SIGNIFICANCE…………………………………………………………………………………...6 REFERENCES…………………………………………………………………………………...10 CHAPTER 2: …………………………………………………………………….………………15 COMPARATIVE IMMUNOGENOMICS OF MOLLUSCS………………………..15 ABSTRACT……………………………………………………………………………………..16 INTRODUCTION………………………………………………………………………………17 MOLLUSCAN IMMUNITY…………………………………………………………………..18 BEYOND “FACTOROLOGY”, IMMUNOGENOMICS PHASE 1……………………...22 GENOMES AND NEXT-GENERATION SEQUENCING, IMMUNOGENOMICS PHASE 2…………………………………………………………….28 LIMITATIONS AND POTENTIAL, FUTURE IMMUNOGENOMICS………………...34 ACKNOWLEDGEMENTS……………………………………………………………………38 FIGURES AND TABLES……………………………………………………………………..39 REFERENCES………………………………………………………………………………….42 CHAPTER 3 ………………………………………………………………………………………….63 COMPARATIVE IMMUNOLOGICAL STUDY OF THE SNAIL Physella acuta (HYGROPHILA,PULMONATA) REVEALS SHARED AND UNIQUE ASPECTS OF GASTROPOD IMMUNOBIOLOGY……..…………………………………………………..........................63 viii ABSTRACT……………………………………………………………………………………..64 INTRODUCTION………………………………………………………………………………65 MATERIALS AND METHODS……………………………………………………………...69 RESULTS………………………………………………………………………………………..77 DISCUSSION…………………………………………………………………………………...82 ACKNOWLEDGEMENTS……………………………………………………………………90 APPENDIX A…………………………………………………………………………………...90 FIGURES AND TABLES……………………………………………………………………..91 REFERENCES………………………………………………………………………………….97 CHAPTER 4…………………………………………………………………………………………...107 CHARACTERIZATION OF THE EARLY HOST RESPONSE OF Physella acuta TO THE DIGENETIC TREMATODE Echinostoma paraensei……………………………………………………………………………………….107 ABSTRACT……………………………………………………………………………………108 INTRODUCTION…………………………………………………………………………..…109 MATERIALS AND METHODS…………………………………………………………….112 RESULTS………………………………………………………………………………………115 DISCUSSION………………………………………………………………………………….119 ACKNOWLEDGEMENTS………………………………………………………………..…127 FIGURES AND TABLES……………………………………………………………………128 REFERENCES………………………………………………………………………………...134 ix CHAPTER 5: ………………………………………………………………………………………….145 FROM LAB TO FIELD: INITIAL INVESTIGATION OF THE ECOIMMUNOLOGY OF Physella acuta SNAILS………………………………………………………………………………………...145 ABSTRACT……………………………………………………………………………………146 INTRODUCTION…………………………………………………………………………..…147 MATERIALS AND METHODS ……………………………………………………………149 RESULTS…………………………………………………………………………………..…..152 DISCUSSION………………………………………………………………………………….155 ACKNOWLEDGEMENTS………………………………………………………………..…159 FIGURES AND TABLES.…………………………………………………………………...160 REFERENCES………………………………………………………………………………...171 CHAPTER 6:…………………………………………………………………………………………175
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    SNAIL PRODUCTION IN BAYELSA STATE, NIGERIA: TECHNOLOGIES, PRODUCTIVITY AND ENHANCEMENT MEASURES BY SUWARI, GOD’STIME SAMUEL PG/Ph.D/04/35563 DEPARTMENT OF VOCATIONAL TEACHER EDUCATION (AGRICULTURAL UNIT) UNIVERSITY OF NIGERIA, NSUKKA SUPERVISOR: DR. R.O. MAMA OCTOBER, 2010. 2 TITLE PAGE SNAIL PRODUCTION IN BAYELSA STATE, NIGERIA: TECHNOLOGIES, PRODUCTIVITY AND ENHANCEMENT MEASURES BY SUWARI, GOD’STIME SAMUEL PG/Ph.D/04/35563 A THESIS REPORT SUBMITTED TO THE DEPARTMENT OF VOCATIONAL TEACHER EDUCATION, UNIVERSITY OF NIGERIA, NSUKKA; IN PARTIAL FULFILLMENT OF THE REQUIREMENT FOR THE AWARD OF Ph.D DEGREE IN AGRICULTURAL EDUCATION SUPERVISOR: DR. R.O. MAMA OCTOBER, 2010. 2 3 APPROVAL PAGE This thesis has been approved for the Department of Vocational Teacher Education, University of Nigeria, Nsukka. By ………………………….. ………………………… Dr. R.O. Mama (Supervisor) Internal Examiner ………………………… ………………………. Prof. E.E. Agomuo External Examiner (Head of Department) …………………………… Prof. S.A. Ezeudu (Dean, Faculty of Education) 3 4 CERTIFICATION SUWARI, GOD’STIME SAMUEL, a postgraduate student in the Department of Vocational Teacher Education (Agriculture) with Registration Number PG/Ph.D/04/35563, has satisfactorily completed the requirements for the research work for the degree of Doctor of Philosophy in Agricultural Education. The work embodied in this thesis is original and has not been submitted in part or full for any Diploma or Degree of this University or any other University. ………………………………….. ……………………… SUWARI, GOD’STIME SAMUEL DR. R.O. MAMA Student Supervisor 4 5 DEDICATION To: Almighty God from whom mercy, knowledge, wisdom and understanding come and who has made me what I am today. 5 6 ACKNOWLEDGEMENTS The researcher wishes to express his profound gratitude to the project supervisor, Dr.
  • “Opisthobranchia”! a Review on the Contribution of Mesopsammic Sea Slugs to Euthyneuran Systematics

    “Opisthobranchia”! a Review on the Contribution of Mesopsammic Sea Slugs to Euthyneuran Systematics

    Thalassas, 27 (2): 101-112 An International Journal of Marine Sciences BYE BYE “OPISTHOBRANCHIA”! A REVIEW ON THE CONTRIBUTION OF MESOPSAMMIC SEA SLUGS TO EUTHYNEURAN SYSTEMATICS SCHRÖDL M(1), JÖRGER KM(1), KLUSSMANN-KOLB A(2) & WILSON NG(3) Key words: Mollusca, Heterobranchia, morphology, molecular phylogeny, classification, evolution. ABSTRACT of most mesopsammic “opisthobranchs” within a comprehensive euthyneuran taxon set. During the last decades, textbook concepts of “Opisthobranchia” have been challenged by The present study combines our published morphology-based and, more recently, molecular and unpublished topologies, and indicates that studies. It is no longer clear if any precise distinctions monophyletic Rhodopemorpha cluster outside of can be made between major opisthobranch and Euthyneura among shelled basal heterobranchs, acte- pulmonate clades. Worm-shaped, mesopsammic taxa onids are the sister to rissoellids, and Nudipleura such as Acochlidia, Platyhedylidae, Philinoglossidae are the basal offshoot of Euthyneura. Furthermore, and Rhodopemorpha were especially problematic in Pyramidellidae, Sacoglossa and Acochlidia cluster any morphology-based system. Previous molecular within paraphyletic Pulmonata, as sister to remaining phylogenetic studies contained a very limited sampling “opisthobranchs”. Worm-like mesopsammic hetero- of minute and elusive meiofaunal slugs. Our recent branch taxa have clear independent origins and thus multi-locus approaches of mitochondrial COI and 16S their similarities are the result of convergent evolu- rRNA genes and nuclear 18S and 28S rRNA genes tion. Classificatory and evolutionary implications (“standard markers”) thus included representatives from our tree hypothesis are quite dramatic, as shown by some examples, and need to be explored in more detail in future studies. (1) Bavarian State Collection of Zoology. Münchhausenstr.
  • Freshwater Snail Guide

    Freshwater Snail Guide

    A Beginner’s Guide to Freshwater Snails of Central Scotland Freshwater snails are a diverse and fascinating group of molluscs found in ponds, lochs, canals, rivers and watery ditches all across the globe. This guide is a simple introduction to some of the most commonly encountered and easily identifiable freshwater snail species in Central Scotland. How do I look for freshwater snails? 1) Choose your spot: anywhere with water – your garden pond, a nearby river, canal or loch – is likely to have snails. 2) Grab a pond net (buy online or make your own by attaching a sieve to the end of an old broom or mop), a white tray or tub and a hand-lens or magnifier. 3) Fill the tray with water from your chosen habitat. Sweep the net around in the water, making sure to get among any vegetation (don’t go too near the bottom or you’ll get a net full of mud), empty your net into the water-filled tray and identify what you have found! Snail shell features Spire Whorls Some snail species have a hard plate called an ‘operculum’ Height which they Mouth (Aperture) use to seal the mouth of the shell when they are inside Height Pointed shell Flat shell Width Width Pond Snails (Lymnaeidae) Variable in size. Mouth always on right-hand side, shells usually long and pointed. Great Pond Snail Common Pond Snail Lymnaea stagnalis Radix balthica Largest pond snail. Common in ponds Fairly rounded and ’fat’. Common in weedy lakes, canals and sometimes slow river still waters. pools.