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Microbial Community Composition, Extracellular

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Microbial Community Composition, Extracellular MICROBIAL COMMUNITY COMPOSITION, EXTRACELLULAR ENZYMATIC ACTIVITIES, AND STRUCTURE-FUNCTION RELATIONSHIPS IN THE CENTRAL ARCTIC OCEAN, A HIGH-LATITUDE FJORD, AND THE NORTH ATLANTIC OCEAN John Paul Piso Balmonte A dissertation submitted to the faculty at The University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Marine Sciences in the College of Arts and Sciences. Chapel Hill 2018 Approved by: Carol Arnosti Andreas Teske Ronnie Glud Barbara MacGregor John Bane © 2018 John Paul Piso Balmonte ALL RIGHTS RESERVED ii ABSTRACT John Paul Piso Balmonte: Microbial community composition, extracellular enzymatic activities, and structure-function relationships in the central Arctic Ocean, a high-latitude fjord, and the North Atlantic Ocean (Under the direction of Carol Arnosti and Andreas Teske) Due to their abundance, diversity, and capabilities to transform and metabolize diverse compounds, microbial communities regulate biogeochemical cycles on micro-, regional, and global scales. The activities of microbial communities affect the flow of matter, energy sources of other organisms, and human health, as well as other aspects of life. Yet, the composition, diversity, and ecological roles of microbes in parts of the global oceans— from the high latitudes to the deep water column—remain underexplored. Drawing from microbiological, oceanographic, and ecological concepts, this dissertation explores several fundamental topics: 1) the manner in which hydrographic conditions influence microbial community composition; 2) the ability of these microbial communities across environmental and depth gradients to hydrolyze organic compounds; and 3) microbial structure-function relationships in different habitats and under altered environmental conditions. In the central Arctic Ocean, the composition and enzymatic function of pelagic, particle associated, and benthic bacterial communities varied with depth and region, in parallel with specific hydrographic features. The microbial structure-function relationship in the pelagic realm indicated functional redundancy, suggesting that bacterial compositional shifts—in response to the changing Arctic—may have complex and less predictable functional consequences than previously anticipated. In Tyrolerfjord-Young Sound, northeast Greenland, microbial enzymatic activity patterns were investigated in rivers and within the fjord. Activity patterns correlated with the composition of bacterial communities and dissolved organic matter in the iii same waters, suggesting that factors extrinsic (organic matter supply) and intrinsic (composition) to microbial communities may, in concert, influence their heterotrophic activities. Finally, functional consequences of differences in community composition were further explored in the North Atlantic. Enriched with high molecular weight organic matter, compositionally-distinct microbial communities exhibited convergent and divergent successional patterns. While convergent features were driven by several initially rare taxa, overarching successional differences in microbial community composition and enzymatic profiles provide evidence for the functional significance of community structure. The integration of community compositional analyses and enzymatic activity measurements has provided valuable information on the identity, ecological roles, and environmental sensitivity of microbial communities in previously underexplored oceanic regions and depths. These insights can be used to evaluate the potential for environmental changes to alter marine microbial community structure and function. iv To my parents, Thelma and Leonardo, who taught me that there are no hardships too difficult to overcome. Maraming, maraming salamat, Ma at Pa. Para sa inyo ito. v ACKNOWLEDGEMENTS I am indebted to so many people for enabling me to carry out my research, be it through research advice, moral support, and/or camaraderie. First and foremost, I am grateful for my two incredibly intelligent and caring mentors, Dr. Carol Arnosti and Dr. Andreas Teske, who nurtured the potential that they saw in me as a prospective student, and provided me with the resources necessary to pursue questions I found most stimulating. Their dedication to helping a student develop into a scientist is unwavering, and their mentorship extended beyond the confines of science. Carol and Andreas, no words can express my deep appreciation for your guidance and generosity over the years. Thank you so much. Cheers! I thank my committee members, Dr. Ronnie Glud, Dr. Barbara MacGregor, and Dr. John Bane, for their insights and thoughtful feedback on my dissertation. I am grateful for Ronnie, whose invitation to join a field campaign in northeast Greenland 2015 enabled me to do fieldwork for one of my chapters. His commitment to being present at every committee meeting, despite the 6 hour time difference, is very much appreciated. I thank Barbara for constantly reminding me to adjust my interpretations in light of methodological limitations, teaching me to be a more thorough scientist. And I want to thank John for always bringing up physical processes when I became too focused on the [micro]biology. The graduate students in the department are among the brightest, friendliest, and most fun folks with whom I have had the pleasure of working. This cohort of scientists lifted up my spirit during the most challenging parts of graduate school. Several folks deserve special recognition. Dr. Natalie Cohen, the first in our cohort to receive her PhD, has celebrated and commiserated with me through graduate school’s ups and downs from day vi zero. Our conversations—on science, on the academy, and on inequalities—have inspired me to think critically about many pressing issues. Natalie, thank you for being a wonderful friend and role model. My predecessors in the Teske lab were among my earliest and closest mentors: Dr. Lisa Nigro, Dr. Verena Carvalho, Dr. Luke McKay, Dr. Tingting Yang, and NASA Astronaut, Zena Cardman. I appreciate everything that you all have taught me, as well as your efforts in mitigating the near-disasters that I may (or may not) have caused in the lab. I especially thank Sherif Ghobrial, the Arnosti lab manager, whose efforts in keeping the GPCs running ensured that I have a wealth of data to analyze. Dr. Anna Jalowska played several roles in my life: a deeply-caring friend, a trustworthy colleague and co- instructor, and my North Carolina mom. Anna, you have saved me from crippling stress, and potentially bank-breaking doggy-sitting bills—I am grateful for all with which you’ve helped. Many other students, in this department and in others, have enriched and elevated the graduate experience, for which I am incredibly grateful. Thank you to (in alphabetical order): Jill Arriola, Jesse Bikman, Sara Coleman, Serena Hackerott, Adrienne Hoarfrost, Andrew Hyde, Ji Hyuk Kim, Rob Lampe, Justin McNabb, Carly Moreno, Kathleen Onorevole, Sertanya Reddy, David Walters, and Barbara Zemskova. My family provided significant moral support and love. My parents, Thelma and Leonardo, listened to (read: suffered through) all of my explanations on what I had spent a fourth of my life researching. Their enthusiasm for understanding my projects—despite lacking in background—has motivated me to learn how to communicate my science to a broad audience. Their drive to improve their and their children’s lives has inspired me to better my own. My brothers—Johnard, Johnathan, Johnaefrey, and John Cris—have been role models in different ways since I entered this world. I will always appreciate their patience in teaching me how to be a better student and an even better person. Finally, to my future husband, Jake Reardon, and to my dogter, Hallie. Living with the two of you is one of the greatest joys of my life. Thank you for the love and happiness. vii TABLE OF CONTENTS LIST OF TABLES ................................................................................................................... xi LIST OF FIGURES ................................................................................................................. xii LIST OF ABBREVIATIONS ................................................................................................... xv CHAPTER 1: DISSERTATION INTRODUCTION .................................................................. 1 1.1 Background ........................................................................................................... 1 1.2 Main Questions ..................................................................................................... 5 1.3 Study Sites ............................................................................................................ 6 1.4 Methodological Approaches .................................................................................. 9 1.5 Chapter Divisions ................................................................................................ 11 References ................................................................................................................ 13 CHAPTER 2: STRUCTURE AND FUNCTION OF HIGH ARCTIC PELAGIC, PARTICLE- ASSOCIATED, AND BENTHIC BACTERIAL COMMUNITIES ........................................... 18 2.1 Introduction .......................................................................................................... 18 2.2 Methods and Materials .......................................................................................
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