No abstract

Magnetotactic bacteria are widespread aquatic microorganisms that use unique intracellular organelles to navigate along the Earth's magnetic field. These organelles, called magnetosomes, consist of membrane-enclosed magnetite crystals that are thought to help to direct bacterial swimming towards growth-favouring microoxic zones at the bottom of natural waters. Questions in the study of magnetosome formation include understanding the factors governing the size and redox-controlled synthesis of the nano-sized magnetosomes and their assembly into a regular chain in order to achieve the maximum possible magnetic moment, against the physical tendency of magnetosome agglomeration. A deeper understanding of these mechanisms is expected from studying the genes present in the identified chromosomal 'magnetosome island', for which the connection with magnetosome synthesis has become evident. Here we use gene deletion in Magnetospirillum gryphiswaldense to show that magnetosome alignment is coupled to the presence of the mamJ gene product. MamJ is an acidic protein associated with a novel filamentous structure, as revealed by fluorescence microscopy and cryo-electron tomography. We suggest a mechanism in which MamJ interacts with the magnetosome surface as well as with a cytoskeleton-like structure. According to our hypothesis, magnetosome architecture represents one of the highest structural levels achieved in prokaryotic cells.

Magnetotactic bacteria derive their magnetic orientation from magnetosomes, which are unique organelles that contain nanometre-sized crystals of magnetic iron minerals. Although these organelles have evident potential for exciting biotechnological applications, a lack of genetically tractable magnetotactic bacteria had hampered the development of such tools; however, in the past decade, genetic studies using two model Magnetospirillum species have revealed much about the mechanisms of magnetosome biogenesis. In this Review, we highlight these new insights and place the molecular mechanisms of magnetosome biogenesis in the context of the complex cell biology of Magnetospirillum spp. Furthermore, we discuss the diverse properties of magnetosome biogenesis in other species of magnetotactic bacteria and consider the value of genetically 'magnetizing' non-magnetotactic bacteria. Finally, we discuss future prospects for this highly interdisciplinary and rapidly advancing field.

We analyzed the biochemical composition of the magnetosome membrane (MM) in Magnetospirillum gryphiswaldense. Isolated magnetosomes were associated with phospholipids and fatty acids which were similar to phospholipids and fatty acids from other subcellular compartments (i.e., outer and cytoplasmic membranes) but were present in different proportions. The binding characteristics of MM-associated proteins were studied by selective solubilization and limited proteolysis. The MM-associated proteins were further analyzed by various proteomic approaches, including one-and two-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis followed by Edman and mass spectrometric (electrospray ionization-mass spectrometry-mass spectrometry) sequencing, as well as capillary liquid chromatography-mass spectrometry-mass spectrometry of total tryptic digests of the MM. At least 18 proteins were found to constitute the magnetosome subproteome, and most of these proteins are novel for M. gryphiswaldense. Except for MM22 and Mms16, all bona fide MM proteins (MMPs) were encoded by open reading frames in the mamAB, mamDC, and mms6 clusters in the previously identified putative magnetosome island. Eight of the MMPs display homology to known families, and some of them occur in the MM in multiple homologues. Ten of the MMPs have no known homologues in nonmagnetic organisms and thus represent novel, magnetotactic bacterium-specific protein families. Several MMPs display repetitive or highly acidic sequence patterns, which are known from other biomineralizing systems and thus may have relevance for magnetite formation.