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Bacterial Symbioses and the Innate Immune Response of the Model Host: Euprymna Scolopes Andrew J

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Bacterial Symbioses and the Innate Immune Response of the Model Host: Euprymna Scolopes Andrew J University of Connecticut OpenCommons@UConn Doctoral Dissertations University of Connecticut Graduate School 8-14-2014 Bacterial Symbioses and the Innate Immune Response of the Model Host: Euprymna scolopes Andrew J. Collins University of Connecticut - Storrs, [email protected] Follow this and additional works at: https://opencommons.uconn.edu/dissertations Recommended Citation Collins, Andrew J., "Bacterial Symbioses and the Innate Immune Response of the Model Host: Euprymna scolopes" (2014). Doctoral Dissertations. 516. https://opencommons.uconn.edu/dissertations/516 Bacterial Symbioses and the Innate Immune Response of the Model Host: Euprymna scolopes Andrew Collins University of Connecticut, 2014 All animals enter into beneficial relationships with bacteria. The light organ of the Hawaiian Bobtail squid, Euprymna scolopes, is a unique model for studying the establishment and maintenance of a symbiosis between a host and a single bacterial species, Vibrio fischeri. This bacterium inhabits a specialized structure known as the light organ and provides counter-illumination to mask the silhouette of the predator as it hunts for food during the night. Hemocytes, the primary innate immune cells, preferentially bind and phagocytose non-symbiotic at higher rates than their symbiont, but this can change with the colonization state of the animal. A goal of this work was to use high-throughput sequencing to identify genes expressed within hemocytes of adult animals. Of the many genes identified was a novel peptidoglycan recognition protein, EsPGRP5, which is one of the most abundant transcripts in circulating hemocytes. In addition to the light organ, female squid have an accessory nidamental gland (ANG) which contributes to making the jelly coat that covers the squid’s eggs. This gland is full of epithelium-lined tubules, most of which support a dense population of bacteria. Unlike the light organ however, the bacterial population in the ANG is a consortium of several species, not just one. This work characterized the bacterial symbionts within the ANG and showed that the population is partitioned, with certain tubules containing a single taxon. The dominant members of the ANG consortium are members of the ubiquitous Roseobacter clade, a group of marine bacteria within the Rhodobacterales. Several Andrew Jeffrey Collins – University of Connecticut, 2014 organisms were cultured from the ANGs of Euprymna scolopes. The genomes of these organisms were sequenced and analyzed for secondary metabolites. Among these were siderophores and homoserine lactones. The results of this work establish a database for future research into the molecular mechanisms of hemocytes. The presence of several genes can lead to the future characterization of many proteins and signaling pathways within hemocytes. This work also established the accessory nidamental gland as new model for consortial symbioses in E. scolopes. Comparisons between this new symbiosis and the light organ will shed light on how animals maintain many different bacterial communities. Bacterial Symbioses and the Innate Immune Response of the Model Host: Euprymna scolopes By Andrew Jeffrey Collins B.S. University of Puget Sound, 2007 A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy At the University of Connecticut 2014 Copyright by Andrew Jeffrey Collins 2014 i APPROVAL PAGE Doctor of Philosophy Dissertation Bacterial Symbioses and the Innate Immune Response of the Model Host: Euprymna scolopes Presented by Andrew Jeffrey Collins, B.S. Major Advisor Dr. Spencer Nyholm Associate Advisor Dr. Joerg Graf Associate Advisor Dr. Daniel Gage Examiner Dr. David Benson Examiner Dr. Steven Geary University of Connecticut 2014 ii Acknowledgements I would first like to thank my advisor, Dr. Spencer Nyholm for supervising my research for the past seven years. I am also grateful to the members of my committee, Dr. Joerg Graf, Dr. Daniel Gage, Dr. David Benson and Dr. Steven Geary, who asked held me to a high standard and asked really good questions. Past and present members of the Nyholm Lab profoundly affected my development as a scientist. I thank our former post-doctoral fellow Dr. Bethany Rader for our constructive discussions on science. I also acknowledge Tyler Schleicher who was a part of our lab for 6 out of my 7 years at UConn. He was an indispensable resource and partner in running the lab, tending to the animals and reviewing my research. I also mentored many students over the years and their inquisitive nature, work ethic and optimism helped me through many long days. I thank many people who helped me behind the scenes, including my parents who always supported me and encouraged me particularly when experiments were not working and I had seemingly reached my limit. My siblings, Courtney, Jon, Laura and Beth, for always making holidays and vacations fun and enjoyable. I especially thank my girlfriend Jess, who sacrificed many weekends to come into lab with me as I took care of the squid and finished up experiments. Finally, I acknowledge my fellow graduate students, who are the soul of research at UConn. It was the people I saw every day, working shoulder-to-shoulder in the lab that provided the greatest wisdom and guidance over the years. I especially need to thank my roommate and my truest friend, Reed Goodwin. Over the five years we lived together, we had many fruitful discussions of experiments, teaching, careers and football. iii I am indebted to him for so much advice, guidance and meaningful conversation over beers. Things would have turned out very differently without his support. iv Table of Contents Approval page ..................................................................................................................... ii Acknowledgements ............................................................................................................ iii Table of Contents ................................................................................................................ v List of Tables ................................................................................................................... viii List of Figures .................................................................................................................... ix Chapter 1. Introduction ...................................................................................................... 1 Beneficial microbes ......................................................................................................... 1 Innate immunity .............................................................................................................. 6 The Roseobacter clade and symbiosis ............................................................................ 8 Summary ....................................................................................................................... 11 Contributions of other researchers ................................................................................ 11 Chapter 2. Hemocyte Transcriptomics and EsPGRP5 ..................................................... 12 Introduction ................................................................................................................... 12 Materials and Methods .................................................................................................. 15 Hemocyte Collection ................................................................................................. 16 Curing Experiments ................................................................................................... 16 Transcriptome Sequencing ........................................................................................ 17 Bioinformatics ........................................................................................................... 17 Western Blot Analysis ............................................................................................... 18 Immunocytochemistry ............................................................................................... 18 Polymerase Chain Reaction ....................................................................................... 19 Results ........................................................................................................................... 20 Discussion ..................................................................................................................... 22 Chapter 3. The Accessory Nidamental Gland................................................................... 43 Introduction ................................................................................................................... 43 Materials and Methods .................................................................................................. 44 Animal maintenance ...................................................................................................... 44 Dissection and DNA extraction ................................................................................. 45 Culturing bacteria from the ANG .............................................................................. 46 Microscopy ................................................................................................................ 46 16S clone library construction and RFLP analysis .................................................... 47 454 Metagenomic Sequencing ..................................................................................
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