Experimental Observation of Magnetosome Chain Collapse in Magnetotactic Bacteria: Sedimentological, paleomagnetic, and evolutionary implications

Magnetotactic bacteria precipitate intracellular crystals of single-domain magnetite (Fe3O4) and/or greigite (Fe3S4), which have often been implicated in carrying the natural remanent magnetization (NRM) of freshwater and marine sediments. In vivo, the magnetic crystals are usually aligned in chains such that their moments add together, generating net cellular moments high enough to rotate the cells passively to align with the geomagnetic field. A magnetostatic/biophysical analysis demonstrates that this arrangement is out of dynamic equilibrium and would collapse spontaneously without a support mechanism. Past rock magnetic analyses of shallow water marine carbonates suggest that partial collapse does occur during diagenesis and dolomitization. To calibrate this effect we induced magnetosome chain collapse in Magnetospirillum magnetotacticum strain MS-1 by progressive sonification and treatment with detergents and monitored the changes with rock magnetic analysis and TEM. Although it has been speculated that the cell wall and associated membrane structures act to prevent magnetosome chain collapse, our data indicate that magnetosome linearity persists long after cells are disrupted. This is consistent with prior observations that in some magnetotcocci the magnetosome chains pass through the cell interior, precluding continuous contact with the cell wall and implying additional support structures exist in some species. Using TEM tomographic reconstructions prepared with a magnetic technique that prevents chain collapse, we examined the three dimensional ultrastructure of magnetosomes without the problem of post-mortem magnetosome motion. This method revealed the presence of an intracellular organic sheath beyond that of actin-like filaments reported recently that follows the chain of magnetosomes, which we postulate evolved to hold the crystals in place and enhances their ability to preserve NRM in sediments. As the genomes of two magnetotactic bacteria contain several apparent homologues of known eukaryotic cytoskeletal proteins, natural selection for magnetotaxis may have played a role in the evolution of precursors to the eukaryotic cytoskeleton. The presence of this sheath is also consistent with the observation of electron translucent material associated with putative magnetofossil chains in ALH84001.