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MICROBIAL CYCLING of MARINE HIGH MOLECULAR WEIGHT DISSOLVED ORGANIC MATTER By MICROBIAL CYCLING OF MARINE HIGH MOLECULAR WEIGHT DISSOLVED ORGANIC MATTER By Oscar Abraham Sosa B.S., University of Texas at Brownsville and Texas Southmost College, 2010 Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the MASSACHUSETTS INSTITUTE OF TECHNOLOGY and the WOODS HOLE OCEANOGRAPHIC INSTITUTION June 2016 © 2016 Oscar A. Sosa All rights reserved. The author hereby grants to MIT and WHOI permission to reproduce and to distribute publicly paper and electronic copies of this thesis document in whole or in part in any medium now known or hereafter created. Signature of Author Joint Program in Oceanography/Applied Ocean Sciences and Engineering Massachusetts Institute of Technology and Woods Hole Oceanographic Institution February 11, 2016 Certified by Dr. Edward F. DeLong Thesis Supervisor Accepted by Dr. Ann M. Tarrant Chair, Joint Committee for Biological Oceanography Woods Hole Oceanographic Institution Dr. Heidi Nepf Donald and Martha Harleman Professor of Civil and Environmental Engineering Chair, Graudate Program Committee 2 MICROBIAL CYCLING OF MARINE HIGH MOLECULAR WEIGHT DISSOLVED ORGANIC MATTER By Oscar Abraham Sosa Submitted to the MIT-WHOI Joint Program in Oceanography / Applied Ocean Science and Engineering on February 11, 2016 in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biological Oceanography Microorganisms play a central role mediating biogeochemical cycles in the ocean. Marine dissolved organic matter (DOM) – a reservoir of organic solutes and colloids derived from plankton is a major source of carbon, nutrients, and energy to microbial communities. The biological transformation and remineralization of DOM sustains marine productivity by linking the microbial food web to higher trophic levels (the microbial loop) and exerts important controls over the cycles of carbon and bio- essential elements, such as nitrogen and phosphorus, in the sea. Yet insight into the underlying metabolism and reactions driving the degradation of DOM is limited partly because its exact molecular composition is difficult to constrain and appropriate microbial model systems known to decompose marine DOM are lacking. This thesis identifies marine microorganisms that can serve as model systems to study the metabolic pathways and biochemical reactions that control an important ecosystem function, DOM turnover. To accomplish this goal, bacterial isolates were obtained by enriching seawater in dilution-to-extinction culturing experiments with a natural source of DOM, specifically, the high molecular weight (HMW) fraction (>1 kDa nominal molecular weight) obtained by ultrafiltration. Because it is relatively easy to concentrate and it is fairly uniform in its chemical composition across the global ocean and other aquatic environments, HMW DOM has the potential to serve as a model growth substrate to study the biological breakdown of DOM. The phylogeny, genomes, and growth characteristics of the organisms identified through this work indicate that HMW DOM contains bioavailable substrates that may support widespread microbial populations in coastal and open-ocean environments. The availability of ecologically relevant isolates in culture can now serve to test hypothesis emerging from cultivation-independent studies pertaining the potential role of microbial groups in the decomposition of organic matter in the sea. Detailed studies of the biochemical changes exerted on DOM by selected bacterial strains will provide new insight into the processes driving the aerobic microbial food chain in the upper ocean. Thesis Supervisor: Dr. Edward F. DeLong, Professor Department of Civil and Environmental Engineering and Biological Engineering, MIT 3 4 Acknowledgments I owe my deepest gratitude to those who mentored me in the lab. My advisers Ed DeLong and Dan Repeta really changed my life and career trajectory in a way I never imagined bringing me on as a JP student, giving me the opportunity to take part in research at sea and an important collaborative project as part of my dissertation. Thank you to my thesis committee members Martin Polz and Tracy Mincer who always provided constructive discussion and advice that helped me progress. Thank you to my friend and collegue Jamie Becker, my reference in the JP, who convinced my advisers Ed and Dan I should help him out with his research in Hawaii as he was finishing up his thesis, an experience that would be invaluable down the road as a continued my work there when our lab moved to C-MORE at the University of Hawaii. A big mahalo also to Scott Gifford; I was very fortunate to work with Scott, at the time a postdoc in the DeLong lab, a very skilled and thoughtful scientist with whom I learned and collaborated extensively. I also want to thank Asuncion “Chon” Martinez for offering a great deal of advice (almost on a daily basis) on science but also on the realm of academia and research. Having the guidance of these mentors was really important for my preparation and success in graduate school. Thanks to all. A special thanks to my lab mates at MIT and in Hawaii, Tsultrim Palden, Anna Romano, John Eppley, Mike Valliere, Jess Bryant, Daniel Mende, Frank Aylward, Torsten Nielsen and many others who were always willing to help me in lab simply by listening to my ideas and suggesting solutions to my day to day work. There are many other people who I met over the years, like WHOI professors, administrators, and graduate students from the JP, EAPS, and CEE, that made my experience and academic formation invaluable. Special thanks to my JP professors Sam Laney and Lauren Mullineaux who introduced me to BioOce, and my JP peers Rene Boiteau, Jesse McNichol, Winn Johnson, Alexis Fischer, Jordon Hemingway, Emily Estes, Emily Brownlee, Esther Shiu, Harriet Alexander, Katie Pitz, Nick McFarlane, Jannette Wheeler, and many, many others whose friendship was as important to my experience in the JP as the help of my mentors. I owe a big mahalo also to the C-MORE community, PIs, students, postdocs, and staff, for hosting me when my work moved over to Hawaii and showing me an enourmous deal of support. In Hawaii I found many new friendships but little did I know there awaited me the greatest discovery of all, my partner Maia. Meeting her and her family has been a wave of support and motivation to finish this work with much gratification. I dedicate this work to my family, especially to my parents Oscar and Mine, for whom I feel an enormous debt of gratitude for their relentless support towards my formation and education, and my brother and sister, Alex and Maria Jose, for their warmth every time I vistited home. They’ve truly been an inspiration and never cease to support with much enthusiasm my journey studying the natural world and the sea. 5 Financial support for this work was provided by the National Science Foundation Center for Microbial Oceanography: Research and Education (award #EF0424599) and the Gordon and Betty Moore Foundation (grant #492.01, #3777, and #3298). 6 WHEN YOU LOOK INTO THE ABYSS, THE ABYSS ALSO LOOKS INTO YOU. Friedrich Nietzsche 7 NVLLIAS IN VERBA “SEE FOR YOURSELF” (OR QUESTION AUTHORITY) Royal Society of London 8 TABLE OF CONTENTS Abstract.…...……………….………………………………..…...…………….….3 Acknowledgements.……………………………………………..…..................….5 Financial support…………………………………………………………………..6 Table of Contents.……………………………………………................................9 List of Tables.…………………………………………………...……………….12 List of Figures.…………………………………………………...………………14 Chapter 1. Introduction..…………………………………...…………………….17 The biogeochemical nature of DOM…………………………………….18 The role of bacterioplankton in the cycling of DOM in the sea…………22 Microbial model systems relevant to semi-labile DOM cycling………...27 Thesis goal and working hypotheses…………………………..………...29 Chapter summaries……………………………………………………….32 Figures………………………………………………………………...….34 References………………………………………………………………..38 Chapter 2. High-molecular-weight dissolved organic matter enrichment selects for methylotrophs in dilution-to-extinction cultures…….…..…...47 Abstract………………………………………………………………......48 Introduction………………………………………………………………49 Materials and methods………………………………………………...…52 Concentration of HMW DOM from seawater………………...…52 Molecular characterization of HMW DOM……………………...52 DOC measurements…………………………………………..….53 Preparation of seawater media………………………………...…53 Extinction culturing with HMW DOM additions……………..…54 Detection of culture growth………………………………..…….54 HMW-DOM dose response screen of the culture collection….…55 SSU rRNA sequencing…………………………………………..55 Whole genome sequencing………………………………………56 Bioinformatic and phylogenetic analysis……………………...…57 Results and discussion………………………………………………..….58 Molecular characterization of HMW DOM…………………...…58 Experimental overview………………………………………..…59 Growth screen……………………………………………...…….60 HMW DOM dose response……………………………………...60 Identification and purity screen………………………………….61 Isolate phylogeny…………………………………………...……63 Growth responses to differing media and C substrates…….……63 Conclusion……………………………………………………………….65 Acknowledgements…………………………………………………...….73 Tables…………………………………………………………………….74 Figures………………………………………………………………...….75 References………………………………………………..………………80 9 Supplemental material…………………………………...……...…….....86 Chapter 3. Assessment of the degradation capabilities of open-ocean bacterial isolates enriched with marine high-molecular-weight dissolved organic matter.………………………………………...……………………..…...93 Abstract………………………………………………………………......94
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