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Conservation, Acquisition, and Maturation of Gut and Bladder Symbioses in Hirudo Verbana

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Conservation, Acquisition, and Maturation of Gut and Bladder Symbioses in Hirudo Verbana Conservation, Acquisition, and Maturation of Gut and Bladder Symbioses in Hirudo verbana a dissertation presented by Emily Ann McClure to The Department of Cell and Molecular Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the subject of Microbiology University of Connecticut Storrs, Connecticut August 2019 ©2019 – Emily Ann McClure all rights reserved. Thesis advisor: Professor Joerg Graf Emily Ann McClure Conservation, Acquisition, and Maturation of Gut and Bladder Symbioses in H. verbana Abstract The medicinal leech is a developing experimental model of gut symbioses. Aeromonas veronii and Mucinivorans hirudinis are core members of the gut microbial community in H. verbana and may aid the leech in digesting the blood meal, preserving the blood meal, and keeping invading bacteria from coloniz- ing the gut. The bladders of H. verbana contain an entirely different microbial consortium. The scientific interest in this symbiosis is currently due to its simple nature and the extreme dietary habits of the leech. In order to increase the usefulness of this model, a more sophisticated understanding of processes by which the microbiome is acquired and develops is necessary. In my dissertation I have compared the gut and blad- der microbiomes of H. verbana to that of Macrobdella decora (the North American medicinal leech) in order to determine the conservation of symbionts. I have additionally examined the potential for horizontal and vertical transmission of gut and bladder symbionts to hatchling and juvenile H. verbana. With such information, future researchers will be able to draw parallels between processes occurring in the leech to those occurring in other organisms. A more detailed understanding of processes conserved or lost between symbiotic partners will lead to a better understanding of processes required for colonization and persis- tence across a wide range of animals. iii Contents 1 Introduction 1 1.1 Symbiosis . 1 1.2 Symbiont Transmission . 4 1.3 The Leech . 6 1.4 Reproduction in Hirudinids . 8 1.5 IntraCocoon Development . 12 1.6 Post Emergence . 14 1.7 Feeding . 15 1.8 Leech Symbionts . 18 1.9 Transmission . 19 2 Macrobdella decora: Old World Leech Gut Microbial Community Structure Con- served in a New World Leech 21 2.1 Abstract . 23 2.2 Importance . 24 2.3 Introduction . 24 2.4 Results . 27 2.5 Discussion . 48 2.6 Methods . 54 2.7 Acknowledgements . 62 2.8 Supplemental Figures & Tables . 63 3 Imperfect Vertical Transmission of Hirudo verbana Gut Symbionts is Horizontally Reinforced by Environmental Interactions 69 3.1 Introduction . 70 3.2 Results . 75 3.3 Discussion . 103 3.4 Methods . 109 3.5 Acknowledgments . 114 3.6 Supplemental Figures . 115 4 Horizontal Transmission Compensates for Insufficient Vertical Transmission 117 4.1 Introduction . 117 4.2 Results . 120 iv 4.3 Discussion . 135 4.4 Methods . 139 4.5 Acknowledgments . 145 4.6 Supplemental Figures & Tables . 145 5 Conclusions 184 5.1 The Conserved Symbiosis Model . 185 5.2 Symbionts have Different Modes of Transmission . 186 5.3 Symbionts Respond to Blood Meal and Provide a Nutrition Network . 187 5.4 The Fight to Colonize . 188 Appendix A Code for Defining M. decora Microbiome Conservation 190 Appendix B Code for Hatchling & Juvenile Microbiome Acquisition 214 Appendix C Code for Tracing Symbiont Transmission 247 References 278 v List of figures 1.1 Adult H. verbana on the side of a breeding tank . 9 1.2 Stages of Cocoon Deposition and Hatching . 11 2.1 Leech-associated microbiota is host species-specific at the genus level but not at higher tax- onomic levels. 30 2.2 The microbiome of M. decora ILF is more diverse than that of H. verbana but the opposite is true of the intestinum microbiomes. 34 2.3 False-color FISH micrographs of M. decora bladder samples. 40 2.4 Month of collection affects wild-caught M. decora - associated microbiota. 42 2.5 The prevalence of taxa in the ILF, but not intestinum, is greatly affected after a blood meal. 45 2.6 M. decora ILF diversity changes with time after feeding. 46 2.7 False-color FISH micrograph of M. decora ILF. 47 2.8 Unifrac-calculated NMDS plot of wild-caught M. decora - associated microbiota. 64 3.1 Microbiota present in H. verbana intraluminal fluid (ILF) is age-specific and affected by co- coon source . 78 3.2 Common genera in H. verbana juvenile and hatchling intraluminal fluid (ILF) are most sim- ilar to the genera found in adult bladder . 79 3.3 Hatchling ILF is most similar to adult bladder . 82 3.4 FISH imaging confirms the presence of adult bladder symbionts in hatchling ILF . 83 3.5 FISH imaging confirms a mature bladder symbiosis in hatchlings . 86 3.6 First blood meal reduces the OTUs in the ILF . 90 3.7 Time after hatching or first feeding has little effect on ILF alpha diversity . 91 3.8 Direct interaction with adult H. verbana or M. decora transmits Aeromonas and Bacteroidetes symbionts . 97 3.9 Indirect interaction with adult H. verbana transmits Aeromonas symbionts . 101 3.10 Variation between hatchling gut microbiomes is minimally affected by the parent source or lot................................................116 4.1 Cocoon albumin samples have the most ASVs . 122 4.2 Cocoon albumin is most similar to hatchling ILF . 123 4.3 Supplier significantly affects cocoon albumin microbiome . 125 4.4 Significant difference in ASVs present in cocoon albumin dependant on supplier . 126 4.5 Diversity and Abundance of Rikenellaceae and Aeromonas ASVs Change with Sample Site 130 4.6 Mucinivorans May Be Transmitted to Cocoons and Hatchlings at Extremely Low Abundance131 vi 4.7 Aeromonas is Transmitted to Cocoons and Hatchlings at Abundances Greater than Mucinivo- rans ...............................................132 4.8 Aeromonas and/or Mucinivorans are Irregularly Present in Cocoons and Hatchlings . 133 4.9 Deposition lot minimally affects cocoon albumin microbiome . 146 vii List of tables 2.1 Average percent of total 16S rRNA V4 sequences of core and common OTUs in ILF and in- testinum samples from H. verbana and M. decora ...................... 37 2.2 Presence of bladder OTUs in total 16S rRNA V4 sequences from M. decora and H. verbana bladder samples. 37 2.3 Number of samples collected of each sample type for this study. Only one sample of each sam- ple type was collected per animal, however multiple sample types were often collected from the same animal. A total of 36 H. verbana and 52 M. decora animals were used in this study. 65 2.4 OTU Smorgasbord . 66 2.5 OTU Smorgasbord cont. 67 2.6 FISH probes used in this study. 68 4.1 Prevalence and Abundance values for ASVs in Cocoon Albumin . 127 4.2 Identified Transmission Source of ASVs Identified in Cocoon Albumen and Hatchling ILF . 134 4.3 Sample Types in Grouped Samples . 145 4.4 ASVs Found in Sample Types . 147 4.5 ASVs Removed During Data Trimming . 147 4.6 ASVs Identified in Cocoon Albumen and Hatchling ILF . 174 viii I dedicate this thesis to anyone who has ever known me as Doodles. I like you a whole bunch. ix Acknowledgments My first thanks go to my advisor, Dr. Joerg Graf. Without his patience and generosity this work would not have been possible. I would also like to thank my committee members for all of their help, Dr. Ny- holm, Dr. Robinson, Dr. Gage, and Dr. Klassen. Dr. Linda McCollam-Guilani, although not part of my committee gave me support and helped me to develop as a college instructor. I could not do this without my family. I thank Hilary for loving me even when she has no idea what I am talking about. I thank Morgan for intellectual vacations and for being patient with my computer idiocy . I thank my father for always telling me everything that I do is ‘neat.’ And I thank my mother for being the kindest and most attentive ‘jailer’ anyone could ever ask for. I would not have made it this far without them and I am especially appreciative for everyone believing in me even when I could not believe in myself. Additional thanks also to my extended family: To the Tinsons for feeding me. To the Wexelblat(t)s - Dayenu. To Becca for ice time and book store time and french fry time and all the times in between. x 1 Introduction Symbiosis No animal exists in a completely sterile environment and successful animals are those functioning within a network of positive interactions. Animals continuously interact with their environment including other animals, plants, and microbes. In fact “all multicellular organisms contain abundant and diverse micro- biota”202. Interactions between members of a community in a biologically relevant space are termed “sym- 1 bioses” and may be composed of beneficial, neutral, or negative interactions. A beneficial interaction is one in which a participant derives a benefit, whether this be protection, nutrition, or reproduction based. A neutral interaction is one that persists despite a partner being neither positively or negatively affected. A negative interaction is one in which a participant is harmed. The simplest symbioses (involving only two species) may constitute different qualities of interaction depending on the partner’s perspective. Some ex- amples include: mutualistic interactions where both partners benefit, parasitic interactions where one partner benefits while another is harmed, commensal interactions where one partner benefits while the other is unaffected, and neutralistic interactions where neither partner is affected. Although symbioses are easiest to study in their simplest form (two partners with only one observed effect), we must eventually take into account that symbioses in fact are a network of interactions involving many species within any given environment.
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