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We Hereby Approve the Dissertation Of MIAMI UNIVERSITY THE GRADUATE SCHOOL CERTIFICATE FOR APPROVING THE DISSERTATION We hereby approve the Dissertation of Christopher James Sedlacek Candidate for the Degree: Doctor of Philosophy ______________________________________ Dr. Annette Bollmann, Director ______________________________________ Dr. Rachael M. Morgan-Kiss, Reader ______________________________________ Dr. Donald J. Ferguson, Reader ______________________________________ Dr. Xiao-Wen Cheng ______________________________________ Dr. Melany C. Fisk Graduate School Representative ABSTRACT THE ECOPHYSIOLOGY OF NITROSOMONAS SP. IS79 by Christopher James Sedlacek Nitrification, the two-step microbially mediated process of transforming ammonia - (NH3) to nitrate (NO3 ) plays a large role in cycling nitrogenous compounds within and between both terrestrial and aquatic ecosystems. The first step in nitrification, ammonia oxidation, is carried out by ammonia-oxidizing microorganisms (AOM), both ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA). The study presented here focuses on the adaptation of AOB to different environmental conditions and their interactions with nitrite- oxidizing and heterotrophic bacterial community members. In order to investigate AOB species + adaptations to different environmental conditions, such as low ammonium (NH4 ) concentrations, cultivation dependent physiological growth experiments and whole genomic sequencing techniques were utilized. Comparison of whole and draft AOB genome sequences were used to correlate the presence or absence of genomic inventory with observed physiologic growth adaptations. The ability to identify and link genomic inventory with observed physiological adaptations allows for improved modeling of how changing environmental conditions will affect microbial community succession and overall ecosystem function. To investigate interactions between bacterial nitrifying community members, chemostat co-culture and community culture growth experiments were conducted with the AOB, Nitrosomonas sp. Is79; the nitrite-oxidizing bacteria (NOB), Nitrobacter winogradskyi and the enrichment culture G5-7. An isobaric tag for relative quantification (iTRAQ) proteomics approach was used to determine how the abundance of Nitrosomonas sp. Is79 proteins changed when grown in the presence of N. winogradskyi, heterotrophic bacteria or both in the enrichment culture G5-7. The growth rate of Nitrosomonas sp. Is79 increased when grown in co-culture with a N. winogradskyi or heterotrophic bacteria, but differential proteome shifts were observed. These differential proteome shifts produced a synergistic effect when Nitrosomonas sp. Is79 is grown in the presence of both N. winogradskyi and heterotrophic bacteria in G5-7. This synergistic effect involves abundance shifts in proteins involved in cellular pathways such as ammonia oxidation, the oxidative stress response and amino acid synthesis. Together these results highlight the importance of understanding species level adaptations within functional groups of microorganisms, such as ammonia oxidizers, and how co-culture or community level growth experiments can provide additional insights into microbial physiological characteristics. THE ECOPHYSIOLOGY OF NITROSOMONAS SP. IS79 A Dissertation Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Microbiology by Christopher James Sedlacek Miami University Oxford, OH 2015 Dissertation Director: Annette Bollmann, Ph.D. TABLE OF CONTENTS List of Tables iii List of Figures v Acknowledgements vi Introduction 1 Chapter 1. Physiological and Genomic Comparison of Ammonia-oxidizing Bacteria Adapted to Different Ammonium Concentrations 23 Chapter 2. The effect of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. Is79 53 Summary 100 References 110 ii" LIST OF TABLES Table Page 1. AOB isolation environment and Nitrosomonas cluster affiliation 28 2. General chracteristics of Nitrosomonas cluster 6a and 7 AOB genomes 37 3. tRNA genetic inventory of Nitrosomonas cluster 6a and 7 AOB genomes 38 4. Ammonia oxidation related genetic inventory of Nitrosomonas cluster 6a and 7 AOB genomes 40 5. Terminal oxidase genetic inventory of Nitrosomonas cluster 6a and 7 AOB genomes 42 6. Urea and hydrogen utilization related genetic inventory of Nitrosomonas cluster 6a and 7 AOB genomes 44 7. Nitrogen oxide metabolism related genetic inventory of Nitrosomonas cluster 6a and 7 AOB genomes 47 8. Carbon metabolism related genetic inventory of Nitrosomonas cluster 6a and 7 AOB genomes 50 9. 16S rRNA bacterial primers used for amplification and sequencing 61 10. Phylogenetic affiliation of the heterotrophic bacteria present in the enrichment culture G5-7 67 11. Phylogenetic affiliation of the bacterial isolates, isolated from the enrichment culture G5-7 68 12. Half saturation constant of ammonia-oxidizing activity and growth of Nitrosomonas sp. Is79 in pure culture, in the presence of N. winogradskyi and as part of the enrichment culture G5-7 71 + - - 13. Steady state NH4 , NO2 and NO3 concentrations in the continuous cultures: Nitrosomonas sp. Is79, Nitrosomonas sp. Is79 and N. winogradskyi and the enrichment culture G5-7 77 14. Nitrosomonas sp. Is79 proteins that were detected when in co-culture with N. winogradskyi compared to when grown as a pure culture 80 15. Nitrosomonas sp. Is79 proteins that were detected when grown as part of the enrichment culture G5-7 compared to when grown as a pure culture 85 iii" 16. Nitrosomonas sp. Is79 proteins that changed in abundance when in co-culture with N. winogradskyi or grown as part of G5-7 compared to when grown as a pure culture 90 iv" LIST OF FIGURES Figure Page 1. Simplified model of the nitrogen cycle 4 2. Simplified model of energy and reductant generation in AOB 11 3. Neighbor-joining tree of AOB based on 16S rRNA gene nucleotide sequences 33 + - 4. The influence of initial NH4 concentration, NO2 concentration, pH, headspace O2 concentration and urea on the growth rate of AOB 35 - - - 5. NO2 or NO2 /NO3 production by Nitrosomonas sp. Is79, Nitrosomonas sp. Is79 + N. winogradskyi, and G5-7 70 6. Growth rate of Nitrosomonas sp. Is79 in co-cultures and community cultures 73 + - - 7. NH4 , NO2 and NO3 concentration in continuous cultures of Nitrosomonas sp. Is79, Nitrosomonas sp. Is79 co-cultured with N. winogradskyi and the enrichment culture G5-7 76 8. SDS-PAGE of whole cell extracts from Nitrosomonas sp. Is79, Nitrosomonas sp. Is79 co-cultured with N. winogradskyi, and the enrichment culture G5-7 grown to steady state in continuous culture 79 9. Model of Nitrosomonas sp. Is79 proteome shifts in response to being grown in the presence of N. winogradskyi, heterotrophic bacteria or as part of the enrichment culture G5-7 106 v" ACKNOWLEDGEMENTS First and foremost I would like to thank my mentor Annette. Without her support, guidance and patience I never would have acquired the skills I have now or become the scientist I am today. When I joined the Bollmann lab, my only condition was that I would never work on the ammonia-oxidizers. Following these acknowledgements is my dissertation solely based on characterizing ammonia-oxidizing bacteria. As I look back now, I never could have imagined the relationships, mentorships and friendships that all started because “culturing the uncultureables” and uranium bioremediation sounded so fascinating. Secondly, I would like to acknowledge all the help I received along the way from my committee members: Rachael, Melany, DJ and Xiao-wen. They stayed with me through all the 4pm Friday committee meetings, listened when I would bank my whole dissertation on a single ill-fated idea and always kept me thinking critically with their advice. I would especially like to thank Rachael for giving me the unbelievable opportunity to join her Antarctic field research team; it was an experience and field season like no other (B-247). Without my family I never would have made it to graduate school. Never give up, work hard, and most importantly never lose yourself. That is what I learned from my family and that is what got me to where I am today. Thanks Mom, Dad, Jess and Jon for all your support. Throughout the years in the Bollmann lab, you probably couldn’t have assembled a weirder more eccentric group of people if you tried. There were lots of great undergrads I was able to work with, including Austin, Rhea and Britton but I would like to single out Brian McGowan. Brian is a great researcher and an even better person. I thank him for all his help in the lab and his continued friendship outside of the lab. Broomball champions, Cabrewing mates, Camping veterans, Team Steve, Plain blank tees; by the end of so many years we could call it by a lot of different names but it boils down to friends. I’ve made more than a few lifelong friends in the past six years and appreciate all the time we spent together both inside and outside of the Pearson Hall basement. As a founding member of OVUM, I hope the needle never stops spinning here in Oxford. -Cheers vi" INTRODUCTION Microorganisms in the environment are subjected to gradients of abiotic factors that are in constant flux. Environmental conditions such as substrate concentration, substrate availability, pH, temperature, light, and oxygen concentration play large roles in determining the diversity of microorganisms that can survive in a particular habitat. Freshwater lakes are an example of an environment with
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