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UNIVERSITY OF CALIFORNIA RIVERSIDE Selective Association Between the Free-Living Nematode Acrobeloides maximus and Soil Bacteria A Thesis submitted in partial satisfaction of the requirements for the degree of Master of Science in Genetics, Genomics and Bioinformatics by Sammy Farid Sedky June 2013 Thesis Committee: Dr. Paul De Ley, Chairperson Dr. Paul Orwin Dr. David Crowley Copyright by Sammy Farid Sedky 2013 The Thesis of Sammy Farid Sedky is approved: Committee Chairperson University of California, Riverside ACKNOWLEDGMENTS This master thesis would not have been possible without the help of several individuals who contributed their time, assistance, and expertise to the completion of this work: • To my advisor, Dr. Paul De Ley: Thank you for giving me a lab I could call home, where I was welcome and where I could grow as a researcher and scholar. Your assistance in navigating the labyrinth of challenges involved in the writing and completion of this document has been invaluable. Thank you for your guidance and support. • To Dr. Paul Orwin: I will always be grateful for the kind tutelage you provided during your sabbatical stay at UCR. This study could not have been completed without your vigilance. • To Dr. David Crowley: Thank you for allowing us to use Science Lab I 308 to perform most of the wet lab work and for your assistance as a committee member in the review and editing of this thesis. • To my colleagues, Dr. JP Baquiran and Brian Thater: It was a blast working with you both. Thanks for the laughs and good times. iv UCR DEDICATIONS • To my friend and protégé, Rosalynn Duong: I could not have chosen a better undergraduate assistant. Thank you for all your help, the late hours you put in taking care of the nematodes and bacterial cultures, your assistance with molecular work, and for most of all sticking with me on this journey. • To Dr. Irma Tandingan De Ley: Thank you for always being generous with your time and for your help and technical expertise in the lab. • To Dr. Cecilia Ritzinger: Thanks for showing me that sometimes we just need to step back and take a coffee break! Obrigado! • To the wonderful GGB graduate students: Amanda Hollowell, Yifan Lii, Stephanie Coffman, Keira Lucas, Hagop Atamian, Patrick Schacht, Meenakshi Kagda, Tusar Saha, Divya Sain, Ritu Chaudhary, Venkatesh Sivanandam: I wish you all nothing but the best in your future endeavors! It’s been a pleasure being your social committee chair these last two years. • To Dr. Michael Fugate, Dr. John Oross, Dr. Laura Abbot, Dr. Brian Brady, Dr. Gregory Filatov, Devon Duron Ehnes-Zepeda: Being a TA was one of the highlights of my graduate career. It was a pleasure to work alongside you while developing my pedagogical skills. • To Tiago Pereira and Ran Sun: I always enjoyed your visits to the lab. Thanks for taking time out of your busy schedules to chat with me. All the best! v DEDICATIONS TO FAMILY AND FRIENDS • To my loving parents, Soha and Mohamed: Thank you for your endless encouragement, love, and support. This one’s for you! • To my aunt and uncle, Siham and Fathy: Thanks for always believing in me and for your love, encouragement, and support. • To my sister, Sally: You are never far from my thoughts. Your strength and courage has always been a source of inspiration. • To the friends that cheered me on, encouraged me, and believed in me: Jorge Flores, Ryan Lee, Johnny Tang, Arif Mosavi, Samuel Koo, Deep Shah, Anand Panchal, Mrunal Patel, Jason Pico, Edgar Alvarado, David Benitez, Max Flores, Jasmine Flores, Dynasty Carfangnia, Jose Hernandez, Stephen Clawson: Thank you !!! vi TABLE OF CONTENTS GENERAL INTRODUCTION IMPORTANCE OF NEMATODE- BACTERIA SYMBIOSIS 1 RESEARCH RECENT STUDIES OF NEMATODE-BACTERIAL ASSOCIATIONS 4 IN SOIL MICROBIAL COMMUNITIES Radopholus similis and Wolbachia 4 Entomopathogenic nematodes and γ-Proteobacteria 5 Steinernema carpocapsae and Xenorhabdus 6 nematophila Heterorhabditis bacteriophora and Photorhabdus 6 luminescens Bacillus thuringiensis Cry5B crystal proteins and free living 7 nematodes Caenorhabditis elegans 7 Pristionchus pacificus 8 SYNOPSIS OF THIS THESIS 8 REFERENCES 10 CHAPTER ONE: Survey of the microbiota associated with A. maximus in soil microcosm ABSTRACT 15 INTRODUCTION 16 MATERIALS AND METHODS 18 Nematode cultivation and harvest 18 Rhizosphere soil collection and exposure 19 Long-term culture of A. maximus 20 Isolation of associated bacteria 20 DNA extraction and PCR analysis 21 16S rRNA gene library construction, sequencing and analysis 22 Preparation for Fluorescence In Situ Hybridization (FISH) 23 FISH Probes 24 FISH- Hybridization, Mounting, Microscopy 24 RESULTS 25 16S rDNA analysis of extracts 25 Co-cultures 26 Isolation and culture 26 Fluorescence In Situ Hybridization 27 DISCUSSION 27 REFERENCES 31 FIGURES AND TABLES 34 vii CHAPTER TWO: Phylogenetic Analysis of Bacterial Genera Detected At Significant Levels Within The Microbiota Associated With A. maximus ABSTRACT 41 INTRODUCTION 42 MATERIALS AND METHODS 43 Data Preparation 43 Multiple sequence alignments: T-Coffee, MAFFT, Kalign, and 44 WebPRANK Phylogenetic inference tools: Maximum Likelihood, PhyML, 45 Mr. Bayes LALIGN 45 RESULTS 46 Ochrobactrum sp. clones 46 Chitinophaga sp. clones 46 Pedobacter sp. clones 47 LALIGN plots 47 DISCUSSION 48 Comparison of multiple sequence alignment algorithms 48 Comparison of phylogenetic reconstruction methods 49 Ochrobactrum sp. clones 50 Chitinophaga sp. clones 51 Pedobacter sp. clones 53 LALIGN analysis 54 Requirements for describing a new bacterial species 55 Genotypic approaches 55 Phenotypic approaches 56 Chemotaxonomic approaches 56 FINAL THOUGHTS 57 REFERENCES 58 FIGURES AND TABLES 62 CONCLUDING COMMENTS BACTERIAL COMMUNITY IDENTIFICATION: 16S rRNA GENE 88 MARKER SURVEY VERSUS SHOTGUN METAGENOMICS 16S rRNA Gene Marker Surveys 88 Shotgun Metagenomics 90 PCR-amplified 16S rRNA and Pyrosequencing 91 Sequencing Technologies and Future Considerations 92 REFERENCES 95 viii LIST OF FIGURES CHAPTER ONE Figure 1. Soil exposed A. maximus populations were found to 34 be associated with a consistent bacterial population Figure 2A. Ochrobactrum is shown to be the predominate 35 alpha-proteobacteria within A. maximus Figure 2B. Pedobacter is shown to be the primary Spingobacteria 36 within A. maximus, along with a consistent representation of Chitinophaga at a lower level Figure 3A-C. Long term culture experiments appear to show stability 37 at the phylum level (A) but reveal shifts in population as the worm population ages at the genus level (B,C) Figure 4A-F. Fluorescence in situ hybridization was used to identify 38 the presence of both Ochrobactrum sp. (green) and Pedobacter sp. (red) in the gut of formaldehyde fixed A. maximus after recovery from soil microcosm CHAPTER TWO Figure 1. Ochrobactrum: T-Coffee-PhyML Phylogram 67-68 Figure 2. Ochrobactrum: MAFFT-ML Phylogram 69-70 Figure 3. Ochrobactrum: Kalign-MrBayes Phylogram 71-72 Figure 4. Chitinophaga: T-Coffee-ML Phylogram 73-74 Figure 5. Chitinophaga: MAFFT-ML Phylogram 75-76 Figure 6. Chitinophaga: Kalign-ML Phylogram 77-78 Figure 7. Pedobacter : T-Coffee-PhyML Phylogram 79-80 Figure 8. Pedobacter : MAFFT-PhyML Phylogram 81-82 Figure 9. Pedobacter : Kalign-PhyML Phylogram 83-84 Figure 10A. LALIGN Plot: Ochrobactrum sp. clone Acro231 85 compared against the consensus sequence of Ochrobactrum clones Figure 10B. LALIGN Plot: Chitinophaga sp. clone Acro210 compared 86 against the consensus sequence of Chitinophaga clones Figure 10C. LALIGN Plot: of Pedobacter sp. clone Acro279 compared 87 against the consensus sequence of Pedobacter clones ix LIST OF TABLES CHAPTER ONE Table 1. List Of Sequences Deposited Into GenBank 39 Table 2. Shannon-Wiener Population Statistics for Microcosm 39 Samples Table 3. Identified Isolates from association from A. maximus 40 microcosm and long term culture CHAPTER TWO Table 1A. Ochrobactrum Sequences Used In Phylogenetic 62 Analyses Table 1B. Pedobacter Sequences Used In Phylogenetic Analyses 62 Table 1C. Chitinophaga Sequences Used In Phylogenetic Analyses 63 Table 2. Pedobacter Settings For Phylogenetic Trees 64 Table 3. Ochrobactrum Settings For Phylogenetic Trees 65 Table 4. Chitinophaga Settings For Phylogenetic Trees 66 x GENERAL INTRODUCTION “The soils of our yards, gardens, and fields swarm with thousands of kinds of minute animals and plants of which we know little or nothing. We depend on the soil for our very existence, and it may seem that this fact should have caused us long ago to make ourselves thoroughly acquainted with it and all its inhabitants; yet the truth is otherwise. Here beneath our very feet are microbes, protozoa, fungi, and many other kinds of small organisms, thousands of species, of which we know hardly the first thing beyond the mere fact of their existence. Inhabiting the soil in myriads, hidden behind this veil of ignorance, there is a group of organisms known as nematodes.” (6) Nathan A. Cobb, 1914 IMPORTANCE OF NEMATODE-BACTERIA SYMBIOSIS RESEARCH Nematodes are among the most abundant metazoans on Earth, inhabiting terrestrial, marine, and freshwater ecosystems (7). They can be found in mountains, grasslands, forests, rivers, lakes, oceans and even in inhospitable environments such as arid deserts and icy tundras. Some parasitize animals and plants, making their homes within these unsuspecting organisms (25, 28, 44). Nematodes have evolved a myriad of fascinating survival strategies, allowing them to adapt to virtually all environments to increase their chances of survival, especially
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  • Variability in Snake Skin Microbial Assemblages Across Spatial Scales and Disease States

    Variability in Snake Skin Microbial Assemblages Across Spatial Scales and Disease States

    The ISME Journal (2019) 13:2209–2222 https://doi.org/10.1038/s41396-019-0416-x ARTICLE Variability in snake skin microbial assemblages across spatial scales and disease states 1 2 1 1 2 Donald M. Walker ● Jacob E. Leys ● Matthew Grisnik ● Alejandro Grajal-Puche ● Christopher M. Murray ● Matthew C. Allender3 Received: 24 August 2018 / Revised: 10 April 2019 / Accepted: 12 April 2019 / Published online: 7 May 2019 © The Author(s) 2019. This article is published with open access Abstract Understanding how biological patterns translate into functional processes across different scales is a central question in ecology. Within a spatial context, extent is used to describe the overall geographic area of a study, whereas grain describes the overall unit of observation. This study aimed to characterize the snake skin microbiota (grain) and to determine host–microbial assemblage–pathogen effects across spatial extents within the Southern United States. The causative agent of snake fungal disease, Ophidiomyces ophiodiicola, is a fungal pathogen threatening snake populations. We hypothesized that the skin microbial assemblage of snakes differs from its surrounding environment, by host species, spatial scale, season, and 1234567890();,: 1234567890();,: in the presence of O. ophiodiicola. We collected snake skin swabs, soil samples, and water samples across six states in the Southern United States (macroscale extent), four Tennessee ecoregions (mesoscale extent), and at multiple sites within each Tennessee ecoregion (microscale extent). These samples were subjected to DNA extraction and quantitative PCR to determine the presence/absence of O. ophiodiicola. High-throughput sequencing was also utilized to characterize the microbial communities. We concluded that the snake skin microbial assemblage was partially distinct from environmental microbial communities.