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Functional architecture of magnetotactic bacteria

Equipe Wu

Our research interest is to understand synthesis, function and ecological implication of bacterial motility apparatus.

Magnetotactic bacteria (MTB) are a phylogenetic, physiological and morphological divers group of Gram-negative bacteria. They display a myriad of cellular morphologies, including coccoid-ovoid, rod-shaped, vibrioid, spirilloid and, the most remarkable multicellular forms referred to as multicellular magnetotactic prokaryotes (MMP or magnetoglobules in short). They have the unique capacity of aligning and swimming along the geomagnetic field lines, a behavior referred to as magnetotaxis. To better understand the magnetotactic mechanism we have studied the synthesis and function of flagellar apparatus of magnetotactic bacteria.

Magnetospirillum magneticum strain AMB-1 has a flagellum at each pole of their spiral-shaped body (amphitrichously flagellated). Using fluorescence labeling, single-cell tracking and swimming pattern analysis we found that asymmetric rotation of the flagellum counter-clockwise (CCW) at the lagging end and clockwise (CW) at leading end propel the magnetospirillum AMB-1. Simultaneous change of the rotation directions leads to reversal of the swimming direction while symmetric rotation of the two flagella (either CCW or CW) results in tumble of the cell. By biochemical analysis, we showed that the flagellin of AMB-1 is glycosylated. Near the flagellin gene, several putative glycosyltransferases genes were found. Among these genes we have identified a gene encoding for a Maf (Motility Accessory Factor) homologue essentially found in pathogenic bacteria genera (like Campylobacter, Helicobacter, Legionella…) and we have studied its role and its structure. We have already showed that, in a Δmaf mutant, the flagellin is still produced but not glycosylated and the bacteria are unflagellated. The structure of Maf presents three different domains. The central domain displays close structural similarity with the structure of a sialyltransferase from C. jejuni.

Fig 1 : The structure of Maf is organized into three domains : a N-terminal domain of unknown function (blue), a central domain with a modified sialyltransferases fold (green and yellow) and a C-terminal exhibiting resemblance with flagellin export chaperones and flagellins (orange)

The magneto-ovoid strain MO-1 that has two flagellar bundles on one side of the cell (bilophitrichously flagellated). In collaboration with Prof. K. Namba’s laboratory at Osaka University we have discovered the most exquisite architecture of the MO-1 flagellar apparatus. Seven flagella filaments (composed of 12 kinds of glycosylated flagellins), and 24 fibrils are arranged in seven intertwined hexagonal arrays enveloped within a sheath (Fig. 2). Such a robust propeller probably allows chemo-litho-autotrophic bacterium MO-1 swimming across chemically stratified layers in marine sediments to obtain O2(electron acceptor, on surface), reduced inorganic sulfur compound (electron donors, in deep sediment) and bicarbonate for its growth.

Fig. 2 Locomotion apparatus of the strain MO-1. Panels A1 and A2 are two-tomograph slices showing side view of a shallow bowl-like platform with a diameter of 230 nm (d0) and a depth of 46 nm (d1) and flagella with yellow arrow heads. Panels B1 and B2 are cryo-eletron micrograph and re-constituted image of flagella array. Panels C1 and C2 show the extracted platform with 7 flagella (brown) and 24 fibrils (light green). Scale bar = 100 nm. Ruan et al (2012). Proc. Natl. Acad. Sci. USA. 109 : 20643-8..

The invention of multicellularity is one of the principal thresholds in evolutionary history. To shed light on the origin, evolution and function of multicellularity we perform ecological, microscopic, genomic and biophysical studies of magnetoglobules. This project is carried out in collaboration with Prof. T. Xiao’s laboratory at Institute of Oceanology of
Chinese Academy of Sciences,

Magnetoglobules were first discovered in the Rodrigo de Freitas lagoon in Brazil, and then observed worldwide. Typically 10–40 cells arrange in spherical or mulberry-like multicellular entity (Fig 3, A). Besides the mulberry-like, we have first observed at the Mediterranean Sea and then collected from both the Mediterranean Sea and the China Sea another group of magnetoglobules : the ellipsoid or pineapple-like MMPs (Fig. 3 up, Panel B). They are composed of about 40 phylogenetic-identical cells arranged in 4–6 interlaced circles. The spherical and ellipsoidal magnetoglobules belong to different genera of delta-Proteobacteria and co-occur in the sediments at the same sampling sites with one or the other as the dominant morphotype. They exhibit a specific ping-pong motility which involves a rapid backward movement and a slower forward movement along magnetic field lines. How these cells coordinate their surface flagellar rotation and what is the ecological implication of the ping-pong motion are enigmas.