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Red Acted Certified By. Signature Redacted Au1...6 Productivity, Metabolism and Physiology of Free-Living Chemoautotrophic Epsilonproteo bacteria by Jesse Christopher McNichol B.Sc., First Class Honours with Distinction, Mount Allison University (2008) Submitted to the Joint Program in Oceanography/Applied Ocean Science & Engineering in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the ASSACHUSETTS INSTITUTE MASSACHUSETTS INSTITUTE OF TECHNOLOGY OF TECHNOLOGY and the AUG 16 2016 WOODS HOLE OCEANOGRAPHIC INSTITUTION L A LIBRARIE September 2016 ARCHIVES @2016 Jesse C. McNichol. 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. A uthorAuho....Signature ........ red acted .............. .. Joint Program in Oceanography/Applied Ocean Science & Engineering Massachusetts Institute of Technology & Woods Hole Oceanographic Institution August 15th, 2016 Certified by. Signature redacted Au1............6 Dr. Stefan Sievert Associate Scientist with Tenure, Department of Biology Woods Hole Oceanographic Institution Thesis Supervisor AcceptedAcete by...y. SiSignature n t r redactede a t d......................... Dr. Ann M. Tarrant Chair, Joint Committee for Biological Oceanography Massachusetts Institute of Technology Woods Hole Oceanographic Institution 2 Productivity, Metabolism and Physiology of Free-Living Chemoautotrophic Epsilonproteo bacteria by Jesse Christopher McNichol Submitted to the Joint Program in Oceanography/Applied Ocean Science & Engineering Massachusetts Institute of Technology & Woods Hole Oceanographic Institution on August 15th, 2016, in partial fulfillment of the requirements for the degree of Doctor of Philosophy Abstract Chemoautotrophic ecosystems at deep-sea hydrothermal vents were discovered in 1977, but not until 1995 were free-living autotrophic Epsilonproteobacteriaidentified as important microbial community members. Because the deep-sea is food-starved, the autotrophic metabolism of hydrothermal vent Epsilonproteobacteriamay be very important for deep-sea consumers. However, quantifying their metabolic activities in situ has remained difficult, and biochemical mechanisms underlying their autotrophic physiology are poorly described. To gain insight into environmental processes, an ap- proach was developed for incubations of microbes at in situ pressure and temperature (25 MPa, 1 3 24'C) with various combinations of electron donors/acceptors (H 2 , 02 and N0 3 and HC03 ) as a tracer to track carbon fixation. During short (18-24 h) incubations of low-temperature vent fluids from Crab Spa (9'N East Pacific Rise), the concentration of electron donors/acceptors and cell numbers were monitored to quantify microbial processes. Measured rates were generally higher than previous studies, and the stoichiometry of microbially-catalyzed redox reactions revealed new insights into sulfur and nitrogen cycling. Single-cell, taxonomically-resolved tracer incorporation showed Epsilonproteobacteriadominated carbon fixation, and their growth efficiency was calculated based on electron acceptor consumption. Using these data, in situ primary productivity, micro- bial standing stock, and average biomass residence time of the deep-sea vent subseafloor biosphere were estimated. Finally, the population structures of the most abundant genera Sulfurimonas and Thioreductor were shown to be strongly influenced by P0 2 and temperature respectively, providing a mechanism for niche differentiation in situ. To gain insights into the core biochemical reactions underlying autotrophy in Epsilonprotebacteria,a theoretical metabolic model of Sulfurimonas deni- trificans was developed. Validated iteratively by comparing in silico yields with data from chemostat experiments, the model generated hypotheses explaining critical, yet so far unresolved reactions sup- porting chemoautotrophy in Epsilonproteobacteria. For example, it provides insight into how energy is conserved during sulfur oxidation coupled to denitrification, how reverse electron transport pro- duces ferredoxin for carbon fixation, and why aerobic growth yields are only slightly higher compared to denitrification. As a whole, this thesis provides important contributions towards understanding core mechanisms of chemoautrophy, as well as the in situ productivity, physiology and ecology of autotrophic Epsilonproteobacteria. Thesis Supervisor: Dr. Stefan Sievert Title: Associate Scientist with Tenure, Department of Biology Woods Hole Oceanographic Institution 3 4 Acknowledgments I owe a great debt of gratitude to the kind and supportive presence of my advisor, Stefan Sievert. When I entered graduate school, I only had a vague understanding of the complex project I was to be entrusted with. It is a testament to Stefan's belief in me that he was able to give me the freedom and encouragement to make this project my own. I have also come to realize how important the conceptual groundwork Stefan laid was for my success. Stefan's understanding of the important and unresolved questions about hydrothermal vent ecosystems meant that my thesis project was both challenging and meaningful. Stefan has always given thoughtful feedback on all of my scholarly writing, and has encouraged me to take pride in my accomplishments. I feel very grateful for the responsibility, resources, and guidance I was given to make my thesis successful and am excited to continue working with Stefan in the future. Many thanks also to Stefan's family - Christel, Lukas and Helen - for always making me feel welcome at their home and in Cape Cod. Another person key to my success at WHOI was Jeff Seewald. With Jeff's patience and can-do attitude, the IGT incubations became successful far beyond my expectations. When I expressed a desire to make oxygen measurements in hydrothermal fluids, Jeff found a way to make it happen. When there were challenges at sea, he faced them with a calm, optimistic and down-to-earth attitude. On land, we had many valuable discussions about writing papers and research where he brought a mature 'big picture' understanding of the hydrothermal vent environment to bear. I have learned much from Jeff that I will carry with me beyond WHOI and will always be grateful for his kindness towards me during my time in the joint program. I also owe many thanks to Craig Taylor, whose assistance and encouragement with designing equipment for the IGT incubations was greatly appreciated. Receiving practical help, kind words and encouragement from an eminent "veteran" of deep-sea research like Craig has meant an enormous amount to me. I'll also never forget all the laughs on cruises from Craig's many hilarious stories and anecdotes. While I was in Leipzig, Germany to analyze field samples, Niculina Musat was kind enough to take me under her wing and teach me the fundamentals of CARD-FISH. Under her careful tutelage, I was finally able to see the microbes that I was studying, which was an incredibly rewarding experience. She and others at UFZ Leipzig - Hryhoriy, Sabrina, Florin 5 and Matthias, were all kind and helpful, and made me feel very welcome while in a foreign country. Thanks are also due to members of my thesis committee: Costa Vetriani, Colleen Hansel, Roger Summons and Tanja Bosak. All of these experienced scientists took time from their busy schedules to give me constructive and encouraging feedback throughout the last three years of my degree. Thanks also to Roger and Mike Neubert for serving on my academic advisory committee and many thanks to Amy Apprill for her professionalism during both my proposal and thesis defense. Work in the lab and in the field would not have been nearly as productive or fun without the guidance and encouragement from and the sense of humour of many friends and colleagues. Big thanks to Frangois Thomas for being both a mentor and friend in the lab and at sea. Frangois never complained once despite the insane amount of work and odd hours we kept to monitor the "little boys" in the IGTs. Whether in the field or lab, Frangois is a calm and reassuring presence and has continued to give thoughtful advice to me even after leaving WHOI. Many thanks also go to Sean Sylva, a kind and encouraging gentleman who always lent a helping hand at sea or on shore no matter how demanding the request was from a troublesome "biologist" such as myself. Ying Zhang also deserves thanks for her guidance and introduction to genome-scale metabolic modeling, which has formed an important component of my thesis work. I am also grateful to Marc Mussmann and Stefan Dyksma for a productive collaboration and for the opportunity to learn from their expertise in CARD-FISH and marine microbiology in general. Thanks also to Fengping Wang and Xiang Xiao for hosting me in Shanghai during my academic exchange. Other members of the Sievert lab, both past and present, have also made my time at WHOI a fantastic experience. Lara Gulmann has always offered me a helping hand with sequence analysis and lab work, and I am also grateful for the kindness her family has shown me. Special thanks go to Ben and Eric for not only attending my thesis defense presentation but also kindly offering me their heartfelt congratulations afterwards! Big ups also to Emelia Deforce for being a high-energy, nurturing presence throughout much of my time at WHOI. Camila Signori has always been a great friend and colleague during my time at WHOI, and has shared with me many of the joys and frustrations of research in the lab and at sea. Florian G6tz has likewise been a great friend and colleague, who always shares what he has with others (including many delicious fish he caught himself) and has never hesitated to help 6 me out in times of need. Thanks also to Sayaka Mino, who I came to respect as a researcher and friend during her short time at WHOI. Finally, thanks are due to Dali Smolsky for her help with isolation and cultivation during her time in the Sievert lab. Life in the joint program was made so much richer by the friends I met while here. Many laughs and fun times were had with Peter Sullivan while living in Boston chez "quark quant".
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