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Microbial Nitrogen Cycling Dynamics in Coastal Systems MICROBIAL NITROGEN CYCLING DYNAMICS IN COASTAL SYSTEMS A DISSERTATION SUBMITTED TO THE DEPARTMENT OF ENVIRONMENTAL EARTH SYSTEM SCIENCE AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Annika Carlene Mosier May 2011 © 2011 by Annika Carlene Mosier. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/wt558td2044 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Christopher Francis, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Kevin Arrigo I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Alexandria Boehm I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Craig Criddle I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Scott Fendorf Approved for the Stanford University Committee on Graduate Studies. Patricia J. Gumport, Vice Provost Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii Abstract Human influence on the global nitrogen cycle (e.g., through fertilizer and wastewater runoff) has caused a suite of environmental problems including acidification, loss of biodiversity, increased concentrations of greenhouse gases, and eutrophication. These environmental risks can be lessened by microbial transformations of nitrogen; nitrification converts ammonia to nitrite and nitrate, which can then be lost to the atmosphere as N2 gas via denitrification or anammox. Microbial processes thus determine the fate of excess nitrogen and yet recent discoveries suggest that our understanding of these organisms is deficient. This dissertation focuses on microbial transformations of nitrogen in marine and estuarine systems through laboratory and field studies, using cutting-edge techniques from molecular biology, genomics, microbial ecology, and microbiology. Recent studies revealed that many archaea can oxidize ammonia (AOA; ammonia-oxidizing archaea), in addition to the well-described ammonia-oxidizing bacteria (AOB). Considering that these archaea are among the most abundant organisms on Earth, these findings have necessitated a reevaluation of nitrification to determine the relative contribution of AOA and AOB to overall rates and to determine if previous models of global nitrogen cycling require adjustment to include the AOA. I examined the distribution, diversity, and abundance of AOA and AOB in the San Francisco Bay estuary and found that the region of the estuary with low-salinity and high C:N ratios contained a group of AOA that were both abundant and phylogenetically distinct. In most of the estuary where salinity was high and C:N ratios were low, AOB were more abundant than AOA—despite the fact that AOA iv outnumber AOB in soils and the ocean, the two end members of an estuary. This study suggested that a combination of environmental factors including carbon, nitrogen, and salinity determine the niche distribution of the two groups of ammonia- oxidizers. In order to gain insight into the genetic basis for ammonia oxidation by estuarine AOA, we sought to sequence the genome of AOA grown in an enrichment culture (84% pure) from San Francisco Bay; however, standard genome sequencing methods require large amounts of DNA from pure cultures. These genomic methods are severely limited because they can only be applied to the ~1% of microbes in nature that can be isolated in the lab. We overcame this deficiency using novel technology developed by Dr. Stephen Quake (Stanford University) that relies on microfluidics and laser tweezing to sequence the genome of a single microbial cell, thereby creating the potential for genomic sequencing of the ~99% of microbes found in nature that cannot be isolated. We demonstrated the feasibility of the method by sequencing the genome of single AOA cells, which proved to represent a new genus within the Archaea. The genome data revealed that the AOA have genes for both autotrophic and heterotrophic carbon metabolism, unlike the autotrophic AOB. These AOA may be chemotactic and motile based on numerous chemotaxis and motility-associated genes in the genome and electron microscopy evidence of flagella. Physiological studies showed that the AOA grow aerobically but they also oxidize ammonia at low oxygen concentrations and may produce the potent greenhouse gas N2O. Continued cultivation and genomic sequencing of AOA will allow for in-depth studies on the physiological and metabolic v potential of this novel group of organisms that will ultimately advance our understanding of the global carbon and nitrogen cycles. Denitrifying bacteria are widespread in coastal and estuarine environments and account for a significant reduction of external nitrogen inputs, thereby diminishing the amount of bioavailable nitrogen and curtailing the harmful effects of nitrogen pollution. I determined the abundance, community structure, biogeochemical activity, and ecology of denitrifiers over space and time in the San Francisco Bay estuary. Salinity, carbon, nitrogen and some metals were important factors for denitrification rates, abundance, and community structure. Overall, this study provided valuable new insights into the microbial ecology of estuarine denitrifying communities and suggested that denitrifiers likely play an important role in nitrogen removal in San Francisco Bay, particularly at high salinity sites. vi Acknowledgments My advisor, Chris Francis, has been the single most influential figure in the development and execution of my dissertation. He has provided continual guidance and encouragement, as well as the freedom to pursue my own research interests and financial support to participate in national and international conferences—an invaluable learning opportunity. I am extremely grateful to my dissertation committee members: Scott Fendorf, Alexandria Boehm, Kevin Arrigo, and Craig Criddle. I thank each of them for their time, constructive feedback on my research, and interest in my intellectual development and future success in academia. I also extend my appreciation to my mentors Mary Beth Mudgett and Karla Kirkegaard who have both provided valuable conversations about research and academic life. This research would not have been possible without Paul Salop, Sarah Lowe, Applied Marine Sciences, the San Francisco Estuary Institute, and the crew of the R.V. Endeavor. I thank them for allowing us to participate in the San Francisco Bay RMP sediment cruises, providing access to the RMP data, and assisting in sample collection. I thank all of my past and present labmates for their support, friendship, and assistance in the lab and field. In particular, I look to Alyson, George, Jason, and Kevan as colleagues and I am enriched from the countless scientific discussions we have shared over the years. Lastly, I thank all of my family. I thank my mom who taught me the value of education at a young age and has provided unwavering support of my academic vii pursuits ever since. Above all, to Jeremy, I could never thank you enough for all the ways that you made this process better, easier, happier. From your refreshing outside perspective to your exceptional editorial skills, you have been there every step of the way and I am so grateful to have you in my life. The work presented in this dissertation was funded by the Diversifying Academia, Recruiting Excellence Doctoral Fellowship (Stanford University), the Environmental Protection Agency STAR Graduate Fellowship, and National Science Foundation grants to Chris Francis. viii Table of Contents Abstract ........................................................................................................................iv Acknowledgments.......................................................................................................vii List of Tables................................................................................................................xi List of Figures .............................................................................................................xii Chapter 1. Introduction ..............................................................................................1 Importance of Nitrogen Cycling in Estuaries.............................................................2 Microbial Biogeochemistry of Ammonia Oxidation..................................................4 Microbial Biogeochemistry of Denitrification ...........................................................7 Dissertation Organization and Chapter Descriptions .................................................8 Figures ......................................................................................................................10
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