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Siderophore Production by Marine Alpha-Proteobacterium UNIVERSITY OF CALIFORNIA Santa Barbara Siderophore production by marine α-proteobacterium Ochrobactrum sp. SP18 A Dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Chemistry by Jessica Elanor Martin Committee in charge: Professor Alison Butler, Chair Professor Peter Ford Professor Richard Watts Professor Stanley Parsons June 2006 UMI Number: 3218830 UMI Microform 3218830 Copyright 2006 by ProQuest Information and Learning Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. ProQuest Information and Learning Company 300 North Zeeb Road P.O. Box 1346 Ann Arbor, MI 48106-1346 The dissertation of Jessica Elanor Martin is approved. ____________________________________________ Alison Butler ____________________________________________ Peter Ford ____________________________________________ Richard Watts ____________________________________________ Stanley Parsons May 2006 Siderophore production by marine α-proteobacterium Ochrobactrum sp. SP18 Copyright © 2006 by Jessica Elanor Martin iii ACKNOWLEDGMENTS I would like to thank Prof. Alison Butler, Department of Chemistry and Biochemistry, University of California, Santa Barbara for her assistance, patience, and support throughout my graduate education. Prof. Butler’s ideas and suggestions were the foundation for the work in this dissertation. I thank my committee, Professors Peter Ford, Richard Watts, and Stanley Parsons for their time, commentary, and helpful advice. Sincere thanks go to Dr. James Pavlovich for his invaluable assistance with mass spectrometry and for many interesting conversations. I would also like to thank the Butler lab members, current and past, for their friendship, assistance, and support. I would especially like to thank my husband Chris Martin for his patience, care, and support. Without his help, this work would not have been possible. I would also like to thank my parents, Charles and Marilyn Dryden, and my sister, Amy Dryden, for their love and support throughout my education. It was because of their care and faith that I have been able to accomplish my goals. iv VITA OF JESSICA ELANOR MARTIN May 2006 Education May 1998 M.S. in Chemistry Thesis: Relationships between nutrient concentrations and fecal coliform levels at Pine Flats in Oak , Arizona Thesis advisor: Professor Richard Foust Northern Arizona University, Flagstaff, Arizona May 1996 B.S. in Chemistry Northern Arizona University, Flagstaff, Arizona Research Experience 2000 – 2006 Graduate Research Assistant Advisor: Professor Alison Butler Topic: Marine bacterial siderophores University of California, Santa Barbara, California 2004 – 2005 California Sea Grant Graduate Trainee Advisor: Professor Alison Butler Topic: Marine red algal vanadium-dependent bromoperoxidases University of California, Santa Barbara, California 1996 – 1998 Graduate Research Assistant/Associate Advisor: Professor Richard Foust Topic: Oak Creek Water Quality Monitoring Project, EPA Section 319(h) National Monitoring Program Northern Arizona University, Flagstaff, Arizona Publications Martin, J.D., Homann, V.V., Haygood, M.G., and Butler, A. Structure and membrane affinity of novel lipophilic siderophores produced by Ochrobactrum sp. SP18. Journal of Biological Inorganic Chemistry in press. Butler, A. and Martin, J.D. The marine biogeochemistry of iron. In Metal Ions in Biological Systems (A. Sigel, H. Sigel, and R.K.O. Sigel, Eds.). 2005, Vol. 44, 21 – 46, Marcel Dekker, New York. Martinez, J.S., Carter-Franklin, J.N., Mann, E.L., Martin, J.D., Haygood, M.G., and Butler, A. Structure and membrane affinity of a new suite of amhiphilic siderophores produced by a marine bacterium. Proceedings of the National Academy of Sciences USA 2003, 100, 3754 – 3759. v ABSTRACT Siderophore production by marine α-proteobacterium Ochrobactrum sp. SP18 by Jessica Elanor Martin Iron is required for growth of nearly all microorganisms. While iron is the fourth most abundant element on the earth’s surface, iron is only sparingly soluble in the aerobic, near neutral conditions under which most microorganisms grow. Therefore, microorganisms experience iron limitation in nearly every environment where they grow, from infection of a mammalian host (where iron is highly controlled by protein complexation) to aquatic and marine environments (where iron is relatively insoluble or is complexed by organic ligands). Bacteria, fungi, and other microbes have developed complex strategies to compete for iron under these conditions. Specifically, many microbes produce low molecular weight, iron binding compounds called siderophores to acquire iron from the environment. Siderophores are secreted by microorganisms and then are taken back into the cells as the ferric complex to promote microbial growth. The siderophores produced by marine α-proteobacterium Ochrobactrum sp. SP18 were structurally characterized. This marine bacterium produces a suite of three aerobactin-derived, amphiphilic siderophores composed of citrate, vi symmetrically derivatized with L-lysine which is N-hydroxylated and N-acylated to form two hydroxamate binding groups. Each siderophore contains one (E)-2- decenoic acid moiety and an (E)-2-octenoic, octanoic, or (E)-2-decenoic acid moiety. The photoreactivity and membrane affinity of these siderophores were investigated. In addition to isolation of the cell-associated ochrobactin siderophores from the marine α-proteobacterium Ochrobactrum sp. SP18, these amphiphilic siderophores were isolated from the marine γ-proteobacterium Vibrio sp. DS40M5. The isolation of these siderophores from two widely different strains, that are in distinct clades of bacteria suggests that these siderophores may be widely utilized in marine environments. vii TABLE OF CONTENTS I. Introduction...............................................................................................................1 A. Microbial iron acquisition.....................................................................1 1. Ferric-ion-specific chelators: siderophores......................................1 2. Siderophore structures......................................................................2 3. Ferric ion affinity .............................................................................4 4. Outer membrane transport proteins..................................................5 5. Siderophore transfer to the periplasm ..............................................7 6. Iron transport across the cytoplasmic membrane.............................8 7. Outer membrane transport proteins (OMPs) versus OMPNs ...........9 8. Apo- versus ferric-siderophore detection.......................................11 B. Iron in the oceans.................................................................................14 1. The iron hypothesis........................................................................14 2. Iron fertilization experiments.........................................................15 C. Iron speciation in the ocean.................................................................19 1. Iron binding ligands .......................................................................19 2. Photochemical iron cycling in marine waters ................................20 3. Dissolution of iron minerals...........................................................23 D. Marine siderophores............................................................................24 1. Amphiphilic character of marine siderophores..............................30 2. Photoreactivity of marine siderophores .........................................33 E. Siderophores in natural seawater environments ..................................34 viii F. Organization of this thesis ...................................................................37 G. References ...........................................................................................39 II. Isolation and structural characterization of siderophores produced by Ochrobactrum sp. SP18 .......................................................................................49 A. Introduction .........................................................................................49 1. Marine α-proteobacteria................................................................49 2. Citrate-derived siderophores ..........................................................51 B. Materials and methods.........................................................................53 1. Maintenance of Ochrobactrum sp. SP18 .......................................53 2. Siderophore production..................................................................53 3. Biofilm formation...........................................................................55 4. Siderophore isolation .....................................................................55 5. Structure determination..................................................................57 a. Amino acid analysis ...........................................................57 b. Fatty acid analysis..............................................................57 c. NMR...................................................................................58 d. Mass spectrometry .............................................................58 C. Results .................................................................................................59 1. Ochrobactrum sp. SP18 siderophores............................................59
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