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A Survey on the Dynamics of Bacterioplankton Assemblages Associated with an Estuarine System and the Stomodeum of Mnemiopsis Leidyi and Their Functional Potential

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A Survey on the Dynamics of Bacterioplankton Assemblages Associated with an Estuarine System and the Stomodeum of Mnemiopsis Leidyi and Their Functional Potential A survey on the dynamics of bacterioplankton assemblages associated with an estuarine system and the stomodeum of Mnemiopsis leidyi and their functional potential by Richard M. Mariita A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama December 10, 2016 Keywords: antibiotic resistance, ctenophore, genomics, metagenomics, chemotaxonomy Copyright 2016 by Richard M. Mariita Approved by Anthony G. Moss, Chair, Associate Professor of Biological Sciences Mark R. Liles, Professor of Biological Sciences Nanette Chadwick, Associate Professor of Biological Sciences Yucheng Feng, Professor of Crop, Soil and Environmental Sciences Abstract Estuaries are among the most biologically productive ecosystems. Eighty percent of our sea food is harvested from estuaries, which are popular recreation areas, yet vital to marine transportation. Unfortunately, estuaries also act as sinks for anthropogenic and natural pollutants. From the viewpoint of ecosystem health, it is important to monitor estuarine ecosystems and their resident organisms, especially those with invasive potential. Chapter 1 provides an introduction to estuarine ecosystems and discusses the major pollutants that affect the dynamics of bacterial assemblages and their functional potential. The impacts of anthropogenic and natural perturbations such as atmospheric deposition of gaseous pollutants, acidification, nutrient loads, bacteria and antibiotic resistance genes and invasive species and their effects are covered. The chapter concludes with an exploration of how to mitigate the impacts of pollution in estuarine ecosystems. Chapter 2 correlates changes in the abiotic, physicochemical parameters of Mobile Bay and changes in dominant bacterial assemblages between wet, cold (January and March) and dry, warm (August and September) months. The study also investigates the differences in the taxonomic, phylogenetic and functional potential of the bacterial assemblages between the two sampling periods, using a metagenomic approach. The study also performs a comparative analysis between Mobile Bay and four other coastal ecosystems. Chapter 3 provides a survey of bacterial assemblages in the stomodeum of the Mnemiopsis leidyi and predicts their functional potential. A comparative analysis between M. leidyi bacterial assemblages and those associated with hosts belonging to two sister phyla (a poriferan and a cnidarian). Chapter 4 examines ii previously uncharacterized bacterial isolates from the ctenophore M. leidyi that display antibiotic resistance, using genomic, chemotaxonomic and classical microbiology techniques. A new species, Staphylococcus mnemiopsis nov., isolated from the M. leidyi stomodeum, displays antibiotic resistance against the penicillins (Penicillin and Ampicillin), fluoroquinolones (Ciprofloxacin, Nalidixic acid), a polypeptide (Bacitracin) and an aminoglycoside (Kanamycin). The present study reveals aspects of the dynamics of bacterial assemblages in Mobile Bay, and the potential for the ctenophore M. leidyi to harbor bacteria with antibiotic resistance genes. This study could form the basis for future examination of the link between watershed management, estuarine systems and ecosystem health. iii Dedication This work is dedicated to my late mother, Nyanchama Mariita, who was the most committed person towards my progress. She taught me that no matter how many punches life throws at me, I must never quit. Her value for education was unmatched, such that regardless of her painful circumstances on her deathbed, she made me promise that I will stay in school and make the best out of my life. Without her, it is hard to imagine what I will have become. I also dedicate this to those who have supported me in the past and present, my elementary school head teacher, Chris Mabuta, who ensured that I stayed in school and my High School Principal, Mr. Fred Sunda, and his deputy, Mr. Casper Maina, I am extremely thankful for the bursaries they provided. To my mentor, role model and longtime friend, Prof. Paul Okemo, who has always stood by me since I was a sophomore in his laboratory through my master’s degree. He did not just teach me to work hard, but made me realize that the harder I work, the luckier I will get. And I have been so lucky. I say thank you. To Dr. John Maingi (Chair of Microbiology Dept., Kenyatta University) and Prof. Callistus Ogol (African Union) for always being there for me. Also, to all my family members, including Naliya Mariita for being the motivator in-chief and Courtney Mariita, my dear wife, for her patience during my intermittent vulgar moods. Her patience and support is a testament of unwavering devotion and enduring love. For that, I am forever grateful. iv Acknowledgments Many thanks to my major professor, Anthony G. Moss, for support, encouragement, and the immense understanding over the course of my education at Auburn University. I thank my dissertation committee Prof. Mark Liles, Prof. Nanette Chadwick and Prof. Yucheng Feng for their input in this work, and for their encouragement, criticism and advice. I am also grateful to Prof. Aharon Oren (The Hebrew University, Israel and IJSEM chief editor), Dr. Lee Zhang, Dr. Scott Miller, Dr. Stephen Kempf, Dr. Alice Ortmann (Bedford Institute of Oceanography, Canada), Mr. Grant Lockridge (DISL), Dr. Lei Hu (DISL), Dr. Jeffrey Krause (DISL), Dr. Mohammad Hossain (Johns Hopkins University) and Srijak Bhatnagar (UCDavis) for their helpful discussions and technical help. I am indebted to my fellow students at Auburn University (Makau Musila, Jessica Gilpin, Susan Rashid, Gen Dong, Ronny Yampolsky, Carlye Ann, Elizabeth McElwee, Rebecca Riggs and Abdul Sajib), and the many friends I made during my stay at the MBL in Woods Hole, MA, and elsewhere (Kessina Lee, Jodi Gronborg, Asha Nelly, Emma Kristine, Taity Changa, Andy Gibbs, Noelle Al-Musaifry, Jess Millar, Jake Cohen, Tino Carr, Britany Waites Josh and Ben Roller) for being supportive. Also to Bonface Nyaribo, Christine Hucke, Michael Hucke, Julie Hobbs-Hucke, Naomi Musila, Loett and Jack Pifher, Irene Momanyi, Judith and George Mason (UK), Murat Sirinoglu (Turkey), Hyrine Munga (Auckland, NZ) for their kind help and encouraging conversations. I acknowledge the Mobile Bay National Estuary Program and NASA’s Giovanni Time Series version 4 mission scientists v and associated NASA, personnel for the production of the physicochemical data that I used as part of this research effort. This work was supported in part by an NSF/EPSCoR PhD fellowship (NSF EPS-115886) and AU-Cell & Molecular Biosciences (CMB) Doctoral Graduate Research Fellowship. The study was also partly funded by USDA-Hatch 370225-310100 (AGM, MRL) and NSF-MCB 0348327 (AGM) grants. vi Table of Contents Abstract ........................................................................................................................................... ii Dedication ...................................................................................................................................... iv Acknowledgments........................................................................................................................... v List of Tables ................................................................................................................................ xii List of Figures .............................................................................................................................. xiv List of Abbreviations .................................................................................................................... xx Chapter 1: Sources of pollution in estuarine ecosystems, their impacts on the dynamics of bacterial assemblages, and mitigation strategies ............................................................................ 1 Abstract ....................................................................................................................................... 1 Introduction ................................................................................................................................. 2 What are estuaries? ................................................................................................................. 2 Types of estuaries ................................................................................................................... 2 Role of estuaries ...................................................................................................................... 3 Nutrients and other chemical pollutants ................................................................................. 5 Sediment and heavy metals ..................................................................................................... 7 Oil spills and related waste chemicals .................................................................................... 9 Gaseous pollutants ................................................................................................................ 10 Acidification ......................................................................................................................... 11 vii Invasive species .................................................................................................................... 12 Microorganisms and antibiotic resistance genes................................................................... 13 Assessment
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