Summary Magnetotactic bacteria (MTB) use magnetosomes, membrane bound crystals of magnetite or greigite, for navigation along geomagnetic fields. In Magnetospirillum magneticum sp. AMB-1, and other MTB, a magnetosome gene island (MAI) is essential for every step of magnetosome formation. An 8-gene region of the MAI encodes several factors implicated in control of crystal size and morphology in previous genetic and proteomic studies. We show that these factors play a minor role in magnetite biomineralization in vivo. In contrast, MmsF, a previously uncharacterized magnetosome membrane protein encoded within the same region plays a dominant role in defining crystal size and morphology and is sufficient for restoring magnetite synthesis in the absence of the other major biomineralization candidates. In addition, we show that the 18 genes of the mamAB gene cluster of the MAI are sufficient for the formation of an immature magnetosome organelle. Addition of MmsF to these 18 genes leads to a significant enhancement of magnetite biomineralization and an increase in the cellular magnetic response. These results define a new biomineralization protein and lay down the foundation for the design of autonomous gene cassettes for the transfer of the magnetic phenotype in other bacteria.
One-dimensional magnetic nanostructures have magnetic properties superior to non-organized materials due to strong uniaxial shape anisotropy. Magnetosome chains in magnetotactic bacteria represent a biological paradigm of such magnet, where magnetite crystals synthesized in organelles called magnetosomes are arranged into linear chains. Two-dimensional synchrotron X-ray diffraction (XRD) is applied to cells of magnetotactic bacteria that are pre-aligned with a magnetic field to determine the crystallographic orientation of magnetosomes relative to the chain axis. The obtained pole figure patterns reveal a [111] fiber texture along the chain direction for magnetospirilla strains MSR-1 and AMB-1, whereas a [100] fiber texture is measured for Desulfovibrio magneticus strain RS-1. The [100] axis appears energetically unfavorable because it represents a magnetic hard axis in magnetite, but can be turned into an effective easy axis by particle elongation along [100] for aspect ratios higher than 1.25, consistent with aspect ratios in RS-1 magnetosomes determined earlier. The pronounced fiber textures can be explained either by a strain-specific biological control on crystal orientation at the chain level or by physical alignment effects due to intra-chain magnetic interactions. In this case, biological control of the axis of elongation would be sufficient to influence the crystallographic texture of the magnetosome chain.
The Cambrian explosion of life was a relatively short period approximately 540 Ma that marked a generalized acceleration in the evolution of most animal phyla, but the trigger of this key biological event remains elusive. Sponges are the oldest extant Precambrian metazoan phylum and thus a valid model to study factors that could have unleashed the rise of multicellular animals. One such factor is the advent of self-/non-self-recognition systems, which would be evolutionarily beneficial to organisms to prevent germ-cell parasitism or the introduction of deleterious mutations resulting from fusion with genetically different individuals. However, the molecules responsible for allorecognition probably evolved gradually before the Cambrian period, and some other (external) factor remains to be identified as the missing triggering event. Sponge cells associate through calcium-dependent, multivalent carbohydrate-carbohydrate interactions of the g200 glycan found on extracellular proteoglycans. Single molecule force spectroscopy analysis of g200-g200 binding indicates that calcium affects the lifetime (+Ca/-Ca: 680 s/3 s) and bond reaction length (+Ca/-Ca: 3.47 A/2.27 A). Calculation of mean g200 dissociation times in low and high calcium within the theoretical framework of a cooperative binding model indicates the nonlinear and divergent characteristics leading to either disaggregated cells or stable multicellular assemblies, respectively. This fundamental phenomenon can explain a switch from weak to strong adhesion between primitive metazoan cells caused by the well-documented rise in ocean calcium levels at the end of Precambrian time. We propose that stronger cell adhesion allowed the integrity of genetically uniform animals composed only of "self" cells, facilitating genetic constitutions to remain within the metazoan individual and be passed down inheritance lines. The Cambrian explosion might have been triggered by the coincidence in time of primitive animals endowed with self-/non-self-recognition and of a surge in seawater calcium that increased the binding forces between their calcium-dependent cell adhesion molecules.
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