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Magnetospirillum Gryphiswaldense Mechanism and regulation of magnetosomal iron uptake and biomineralization in Magnetospirillum gryphiswaldense Dissertation der Fakultät für Biologie der Ludwig-Maximilians-Universität München vorgelegt von René Uebe aus Stralsund München 19.12.2011 II Gutachter: 1. Prof. Dr. Dirk Schüler 2. Prof. Dr. Heinrich Jung Tag der mündlichen Prüfung: 02.05.12 III IV Publications and manuscripts originating from this thesis CHAPTER 2 Uebe, R., Voigt, B., Schweder, T., Albrecht, D., Katzmann, E., Lang, C., Böttger, L., Matzanke, B. and Schüler, D. (2010). Deletion of a fur-like gene affects iron homeostasis and magnetosome formation in Magnetospirillum gryphiswaldense. J. Bacteriol. 192: 4192-4204. CHAPTER 3 Uebe, R., Junge, K., Henn, V., Poxleitner, G., Katzmann, E., Plitzko, J. M., Zarivach, R., Kasama, T., Wanner, G., Pósfai, M., Böttger, L., Matzanke, B. and Schüler, D. (2011). The cation diffusion facilitator proteins MamB and MamM of Magnetospirillum gryphiswaldense have distinct and complex functions, and are involved in magnetite biomineralization and magnetosome membrane assembly. Mol. Microbiol. 82: 818-835. CHAPTER 4 Uebe, R., Henn, V. and Schüler, D. (2012). The MagA protein of magnetospirilla is not involved in bacterial magnetite biomineralization. J. Bacteriol. 194: 1018-1023 V VI INDEX INDEX PUBLICATIONS AND MANUSCRIPTS ORIGINATING FROM THIS THESIS......................V INDEX.................................................................................................................................................VII ABBREVIATIONS ...............................................................................................................................X SUMMARY.............................................................................................................................................1 ZUSAMMENFASSUNG .......................................................................................................................3 CHAPTER 1 ...........................................................................................................................................5 INTRODUCTION..................................................................................................................................5 1.1 IMPORTANCE OF IRON IN ORGANISMS ............................................................................................5 1.2 ECOLOGY AND DIVERSITY OF MAGNETOTACTIC BACTERIA ..........................................................6 1.3 IRON METABOLISM OF MAGNETOTACTIC BACTERIA......................................................................8 1.4 MAGNETOSOMES AND BIOMINERALIZATION OF MAGNETITE ......................................................11 1.4.1 Biomineralization of magnetite ............................................................................................11 1.4.2 Structure and composition of the magnetosome membrane.................................................13 1.4.3 Genetics of magnetosome formation ....................................................................................14 1.4.4 Transport of iron into magnetosome vesicles.......................................................................18 1.5 REGULATION AND DYNAMICS OF MAGNETOSOME FORMATION ..................................................20 1.6 SCOPE OF THIS WORK ...................................................................................................................22 1.7 REFERENCES.................................................................................................................................23 CHAPTER 2 .........................................................................................................................................35 DELETION OF A FUR-LIKE GENE AFFECTS IRON HOMEOSTASIS AND MAGNETOSOME FORMATION IN MAGNETOSPIRILLUM GRYPHISWALDENSE ............35 2.1 ABSTRACT ....................................................................................................................................35 2.2 INTRODUCTION.............................................................................................................................36 2.3 MATERIALS AND METHODS .........................................................................................................39 2.3.1 Bacterial strains and growth conditions ..............................................................................39 2.3.2 Molecular and genetic techniques........................................................................................40 2.3.3 Isolation of total RNA and qualitative reverse transcriptase-PCR (RT-PCR).....................40 2.3.4 Fur Titration Assay (FURTA) ..............................................................................................41 2.3.5 Heterologous transcomplemention of an E. coli fur mutant ................................................41 2.3.6 Generation of a fur deletion strain.......................................................................................42 2.3.7 Analytical methods ...............................................................................................................42 2.3.8 Transmission Mössbauer Spectroscopy (TMS) ....................................................................43 2.3.9 Cell fractionation and preparation of protein extracts ........................................................43 2.3.10 2-D gel electrophoresis ......................................................................................................44 2.3.11 Protein digestion, mass spectrometry and data analysis ...................................................44 2.3.12 Bioinformatics ....................................................................................................................45 2.4 RESULTS .......................................................................................................................................46 2.4.1 Identification of a putative fur gene .....................................................................................46 2.4.2 MgFur transcomplements an E. coli fur mutation ...............................................................47 2.4.3 Generation and analysis of a M. gryphiswaldense fur mutant.............................................48 2.4.4 Mössbauer spectroscopic analysis of RU-1 reveals a large pool of iron bound to a ferritin- like component...............................................................................................................................53 2.4.5 Analyis of the putative Fur regulon......................................................................................55 2.4.6 Proteomic analysis of the Fur regulon.................................................................................56 2.5 DISCUSSION..................................................................................................................................59 2.6 ACKNOWLEGMENTS .....................................................................................................................61 2.7 REFERENCES.................................................................................................................................62 VII INDEX 2.8 SUPPLEMENTAL MATERIAL ..........................................................................................................69 2.9 REFERENCES.................................................................................................................................79 CHAPTER 3 .........................................................................................................................................80 THE CATION DIFFUSION FACILITATOR PROTEINS MAMB AND MAMM OF MAGNETOSPIRILLUM GRYPHISWALDENSE HAVE DISTINCT AND COMPLEX FUNCTIONS, AND ARE INVOLVED IN MAGNETITE BIOMINERALIZATION AND MAGNETOSOME MEMBRANE ASSEMBLY...............................................................................80 3.1 ABSTRACT ....................................................................................................................................80 3.2 INTRODUCTION.............................................................................................................................81 3.3 RESULTS .......................................................................................................................................83 3.3.1 MamM and MamB are highly conserved in all MTB...........................................................83 3.3.2 ∆mamM and ∆mamB mutants are non-magnetic but have distinct phenotypes ..................83 3.3.3 MamM is required for stability of MamB.............................................................................86 3.3.4 MamB participates in multiple protein-protein interactions................................................89 3.3.5 MamM and MamB are targeted to the magnetosome as well as to the cytoplasmic membrane ......................................................................................................................................92 3.3.6 Localization of MamC-GFP is altered in ∆mamM and ∆mamB..........................................95 3.3.7 MamM is involved in the control of magnetite nucleation and crystal growth....................95 3.4 DISCUSSION................................................................................................................................100 3.5 EXPERIMENTAL PROCEDURES ....................................................................................................105
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