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Magnetotactic Bacteria and Magnetosomes Chem. Rev. 2008, 108, 4875–4898 4875 Magnetotactic Bacteria and Magnetosomes Damien Faivre† and Dirk Schu¨ler*,‡ Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Science Park Golm, 14424 Potsdam, Germany, and Microbiology, Department of Biology I, Ludwig-Maximilians-Universita¨t Mu¨nchen, Biozentrum, Grohaderner Strasse 2, 82152 Planegg-Martinsried, Germany Received February 12, 2008 Contents 9. References 4895 1. Introduction 4875 1. Introduction 2. Magnetotactic Bacteria 4876 2.1. Morphologic and Phylogenetic Diversity 4876 Iron biominerals are formed by a broad host of organisms, 2.1.1. Physiology 4877 in which they serve various functions. For example, iron oxides formed by organisms serve for strengthening of 2.2. Ecology 4878 tissues1 and hardening of teeth.2 Iron biominerals are also 2.2.1. Freshwater Habitats 4878 associated with iron overload diseases and involved in 2.2.2. Marine Habitats 4879 intracellular iron storage and detoxification and sensing of 2.3. Geobiology 4879 magnetic fields,3-6 and crystals of magnetic iron minerals 2.3.1. Iron and Sulfur Cycling 4879 have been found even in the human brain.7-9 2.3.2. Fossil Record and Sediment Magnetization 4879 One of the most intriguing examples for the biological 3. Magnetosomes 4880 synthesis of iron minerals, and biomineral formation in 3.1. The Inorganic Core 4880 general, is represented by the biomineralization of magnetic 3.1.1. Structure of Magnetic Crystals 4880 minerals in bacterial magnetosomes. Magnetosomes are 3.1.2. Crystal Habits 4881 specialized organelles synthesized by magnetotactic bacteria 3.1.3. Composition 4882 (MTB) for geomagnetic navigation in their aquatic habitats. 3.2. The Organic Part: The Magnetosome 4882 The magnetosomes comprise membrane-enveloped, nano- Membrane sized crystals of either the magnetic iron oxide magnetite, 3.2.1. Structure and Biochemical Composition of 4882 Fe3O4 or, less commonly, the magnetic iron sulfide greigite, the Magnetosome Membrane (MM) Fe3S4. The magnetosomes are arranged in intracellular chains that enable the cell to align and swim along external magnetic 3.3. Genetics of Magnetosome Biomineralization 4883 10 3.3.1. Genomic Organization of Magnetosome 4883 fields, a behavior known as “magnetotaxis”. Magnetotaxis Genes is thought to facilitate the dwelling of bacteria within their 3.4. Pathway of Magnetosome Biomineralization 4884 growth-favoring microoxic zones on the bottom of chemi- cally stratified natural waters.11 3.4.1. Iron Reaction Pathway 4884 3.4.2. Systems for Iron Uptake and Transport 4885 The synthesis of bacterial magnetosomes is achieved by a high degree of control over the biomineralization of 3.5. Chemical Control: Influence of Organic 4886 Components and Solution Chemistry on perfectly shaped and sized magnetic crystals, and their Inorganic Crystal Properties assembly into a highly ordered chain structure to serve most 3.5.1. Nucleation and Growth of the Magnetic 4886 efficiently as a magnetic field sensor. The unique charac- Mineral teristics of magnetosome biomineralization have attracted a 3.5.2. Control of Particle Morphology 4886 broad interdisciplinary interest and might be exploited for a variety of applications in diverse disciplines from microbi- 3.5.3. Control of Magnetosome Dimensions 4887 ology, cell biology, and geobiology to biotechnology.12,13 4. Intracellular Organization of Magnetosome Chains 4888 The biomineralization of magnetosomes and their assembly 4.1. Cell Biology of Magnetosome Chain Formation 4888 into chains is of great interest for the generation of bioin- 4.2. Chain Assembly 4890 spired magnetic materials and has even been suggested as a 5. Magnetic Orientation of Cells 4890 biomarker to detect extraterrestrial life.14 In addition, the 5.1. Magnetic Properties of Magnetosome Chains 4890 formation of magnetosomes is a fascinating example of how 5.2. Magnetotaxis 4891 supposedly primitive organisms can translate genetic blue- 6. Application of MTB and Magnetosomes in Bio- 4892 print information into complex inorganic and cellular struc- and Nanotechnologies tures. As many of the fundamental mechanisms of biomin- 7. Perspectives and Directions for Future Research 4894 eralization are found in bacterial magnetosome biominerali- 8. Acknowledgments 4895 zation, magnetotactic bacteria may serve as an accessible and relatively simple model for studying and understanding * To whom correspondence should be addressed. Phone: +49-89-2180- biomineralization processes in general. 74502. Fax: +49-89-2180-74515. E-mail: [email protected]. Although several early reports by Salvatore Bellini (and † Department of Biomaterials, Max Planck Institute of Colloids and Interfaces. perhaps even earlier by J. Massart) described the observation ‡ Microbiology, Ludwig-Maximilians-Universita¨t Mu¨nchen. of bacteria, in which the swimming direction was apparently 10.1021/cr078258w CCC: $71.00 2008 American Chemical Society Published on Web 10/15/2008 4876 Chemical Reviews, 2008, Vol. 108, No. 11 Faivre and Schüler Damien Faivre studied physical chemistry at the University Claude Bernard Dirk Schu¨ler became fascinated by magnetotactic bacteria during his (Lyon, France), before joining Prof. G. Peshlerbe’s group in 1999 at undergraduate studies at the Ernst Moritz Arndt University Greifswald Concordia University (Montreal, Canada) to study theoretical nanochem- (Germany), where he started working on the isolation of these microorgan- istry. He returned to France in 2000, where his interests in magnetite isms in the group of Manfred Ko¨hler (1990). In 1991, he joined the started during his doctoral studies at the University Denis Diderot (Paris). laboratory of Edmund Ba¨uerlein at the Max Planck Institute of Biochemistry He studied the geochemical properties of abiogenic magnetite and their in Martinsried (Germany) to study biomineralization in Magnetospirillum implications on the definition of biogenicity criteria under the supervision gryphiswaldense, the bacterial strain he had isolated during his diploma of Prof. P. Zuddas. He was awarded an IPGP Fellowship to spend a thesis. In 1994, he finished his doctoral thesis, and in 1996, he joined research semester at the California Institute of Technology (Pasadena, the laboratory of Dennis Bazylinski at Iowa State University (USA). His USA) working in Prof. D. Newman’s group with Dr. A. Komeili, where he second postdoctoral position was at the Scripps Institute of Oceanography for the first time came into contact with the fascinating magnetotactic (University of California, San Diego, USA), in the laboratory of Brad Tebo, bacteria. In 2005, he left France again, this time with a Ph.D. and for where he started to do research on the molecular genetics of magneto- Germany, where he worked first as a Max Planck then as a Marie-Curie some formation. In 1999, he returned to Germany to join the Max Planck postdoctoral fellow in Prof. D. Schu¨ler’s group at the Max Planck Institute Institute for Marine Microbiology (Bremen) as the head of a research group. of Marine Microbiology (Bremen), where he got involved in various projects, He completed his habilitation at the University of Bremen in 2004 and specifically focusing on unraveling the biomineralization pathway of was appointed as an associate professor for microbiology at the Ludwig magnetosome formation. Since August 2007, he has been a research Maximilians University of Munich in October 2006. His research focus is group leader in the biomaterials department of the Max Planck Institute on physiology, cell biology, and genetics of magnetosome biomineralization of Colloids and Interfaces (Potsdam, Germany). His research interests by magnetotactic bacteria, and their potential application in nanobiotech- range from magnetic nanoparticles in biosystems, with a particular nology. emphasis on the physicochemical aspects of the magnetosome biomin- eralization by magnetotactic bacteria, to the development of molecular laboratory, their diversity can be studied by molecular biomimetics for the formation and assembly of hybrid magnetic nanomaterials. methods without prior cultivation.18 Based on 16S rRNA 15,16 sequence similarity, MTB are polyphyletic, but all known affected by magnetic fields (http://www.calpoly.edu/ 18 ∼rfrankel/SBellini1.pdf), it was Richard Blakemore’s ser- MTB belong to the domain Bacteria. Most of the cultured endipitous discovery of magnetotactic bacteria10 that initiated MTB and many of the so far uncultured phylotypes cluster and stimulated a wealth of research activities during the last within the Alphaproteobacteria, but MTB have also been affiliated to Deltaproteobacteria, to the phylum Nitrospira, few decades. Since Blakemore’s seminal paper in 1975, the 18 subject of magnetosome biomineralization has evolved into and, tentatively, also to Gammaproteobacteria. Within the an interdisciplinary and unique field of research. The aim of alphaproteobacteria, MTB are closely related to the non- this review is to give a broad overview over the current state magnetic, photosynthetic, nonsulfur purple bacteria, with of knowledge on the biology of magnetotactic bacteria and which they share the ability to form intracytoplasmic the structure of the biominerals formed by them. Emphasis membranes. In this respect, it is interesting to note that the is given on recent research studying the processes of formation of magnet-sensitive inclusions could be induced magnetosome biomineralization at the physicochemical, by incubation in iron rich medium in some species of
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