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UNIVERSITY of CALIFORNIA, SAN DIEGO Indicators of Iron UNIVERSITY OF CALIFORNIA, SAN DIEGO Indicators of Iron Metabolism in Marine Microbial Genomes and Ecosystems A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Oceanography by Shane Lahman Hogle Committee in charge: Katherine Barbeau, Chair Eric Allen Bianca Brahamsha Christopher Dupont Brian Palenik Kit Pogliano 2016 Copyright Shane Lahman Hogle, 2016 All rights reserved . The Dissertation of Shane Lahman Hogle is approved, and it is acceptable in quality and form for publication on microfilm and electronically: Chair University of California, San Diego 2016 iii DEDICATION Mom, Dad, Joel, and Marie thank you for everything iv TABLE OF CONTENTS Signature Page ................................................................................................................... iii Dedication .......................................................................................................................... iv Table of Contents .................................................................................................................v List of Figures ................................................................................................................... vii List of Tables ..................................................................................................................... ix Acknowledgements ..............................................................................................................x Vita ................................................................................................................................... xiv Abstract of the Dissertation ............................................................................................. xvi Chapter 1 Introduction........................................................................................................1 1.1 References .............................................................................................................11 Chapter 2 Heme in the marine environment: From cells to the iron cycle ......................16 2.1 Abstract .................................................................................................................16 2.2 Intracellular roles for heme in marine microbes ...................................................16 2.3 Methods for heme acquisition in marine microbes ...............................................24 2.4 Heme in the marine environment ..........................................................................32 2.5 Conclusions and future directions .........................................................................41 2.6 Methods.................................................................................................................42 2.7 Acknowledgements ...............................................................................................43 2.8 References .............................................................................................................50 Chapter 3 Trace metal acquisition by marine heterotrophic bacterioplankton with contrasting trophic strategies .............................................................................................61 3.1 Abstract .................................................................................................................61 3.2 Introduction ...........................................................................................................62 3.3 Results ...................................................................................................................67 3.4 Discussion .............................................................................................................79 3.5 Conclusions ...........................................................................................................89 3.6 Materials and Methods ..........................................................................................90 3.7 Acknowledgements ...............................................................................................96 3.8 References ...........................................................................................................109 Chapter 4 Heme as a molecular intermediate in the microbial remineralization of marine biogenic Fe .......................................................................................................................118 4.1 Abstract ...............................................................................................................118 v 4.2 Introduction .........................................................................................................119 4.3 Results .................................................................................................................120 4.4 Discussion ...........................................................................................................127 4.5 Conclusions .........................................................................................................132 4.6 Materials and Methods ........................................................................................134 4.7 Acknowledgements .............................................................................................144 4.8 References ...........................................................................................................161 Chapter 5 Linking phytoplankton and bacterioplankton assemblage dynamics to iron- binding ligand production in a microcosm experiment ...................................................167 5.1 Abstract ...............................................................................................................167 5.2 Introduction .........................................................................................................168 5.3 Results .................................................................................................................171 5.4 Discussion ...........................................................................................................176 5.5 Materials and Methods ........................................................................................181 5.6 Acknowledgements .............................................................................................187 5.7 References ...........................................................................................................204 Chapter 6 Molecular and geochemical evidence for iron limitation in subsurface chlorophyll maxima of the eastern subtropical Pacific Ocean .........................................209 6.1 Abstract ...............................................................................................................209 6.2 Introduction .........................................................................................................210 6.3 Results and Discussion .......................................................................................213 6.4 Conclusions .........................................................................................................223 6.5 Materials and Methods ........................................................................................226 6.6 Acknowledgements .............................................................................................231 6.7 References ...........................................................................................................244 Chapter 7 Conclusion .....................................................................................................250 7.1 References ............................................................................................................252 vi LIST OF FIGURES Figure 2.1 Schematic showing the distribution of the major proteins containing heme- like cofactors in a hypothetical diatom ..............................................................................45 Figure 2.2 Biosynthetic pathway for heme and other tetrapyrroles in marine eukaryotic algae and bacteria ...............................................................................................................46 Figure 2.3 Representative schematic of encoding genes and protein machinery utilized in hemophore mediated heme uptake and direct heme uptake ..............................................47 Figure 2.4 Marine bacterial genomes containing heme uptake genes ..............................48 Figure 2.5 Structures of hemes a-c and siroheme .............................................................49 Figure 3.1 Maximum likelihood phylogenies of 42 Roseobacter genomes and 22 SAR11 genomes ...........................................................................................................................102 Figure 3.2 Examples of TRAP transporters in genome neighborhoods containing siderophore biosynthesis or siderophore-like uptake genes.............................................103 Figure 3.3 Boxplot showing trait depth (τD) of metal uptake genes with respect to Roseobacter and SAR11 phylogenies ..............................................................................104 Figure 3.4 Principal Component Analysis (PCA) based on the diversity and abundance of transporters in Roseobacter and SAR11 genomes ......................................................105 Figure 3.5 Network visualization of pairwise Spearman's rank correlation coefficients between metal uptake genes
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