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Marine environments are generally characterized by low bulk concentrations of nutrients that are susceptible to steady or intermittent motion driven by currents and local turbulence. Marine bacteria have therefore developed strategies, such as very fast-swimming and the exploitation of multiple directional sensing-response systems in order to efficiently migrate towards favorable places in nutrient gradients. The magnetotactic bacteria (MTB) even utilize Earth's magnetic field to facilitate downward swimming into the oxic-anoxic interface, which is the most favorable place for their persistence and proliferation, in chemically stratified sediments or water columns. To ensure the desired flagella-propelled motility, marine MTBs have evolved an exquisite flagellar apparatus, and an extremely high number (tens of thousands) of flagella can be found on a single entity, displaying a complex polar, axial, bounce, and photosensitive magnetotactic behavior. In this review, we describe gene clusters, the flagellar apparatus architecture, and the swimming behavior of marine unicellular and multicellular magnetotactic bacteria. The physiological significance and mechanisms that govern these motions are discussed., Competing Interests: The authors declare no conflicts of interest.

Magnetotactic multicellular prokaryotes (MMPs) consist of unique microorganisms formed by genetically identical Gram-negative bacterial that live as a single individual capable of producing magnetic nano-particles called magnetosomes. Two distinct morphotypes of MMPs are known: spherical MMPs (sMMPs) and ellipsoidal MMPs (eMMPs). sMMPs have been extensively characterized, but less information exists for eMMPs. Here, we report the ultrastructure and organization as well as gene clusters responsible for magnetosome and flagella biosynthesis in the magnetite magnetosome producer eMMP Candidatus Magnetananas rongchenensis. Transmission electron microscopy and focused ion beam scanning electron microscopy (FIB-SEM) 3D reconstruction reveal that cells with a conspicuous core-periphery polarity were organized around a central space. Magnetosomes were organized in multiple chains aligned along the periphery of each cell. In the partially sequenced genome, magnetite-related mamAB gene and mad gene clusters were identified. Two cell morphologies were detected: irregular elliptical conical 'frustum-like' (IECF) cells and H-shaped cells. IECF cells merge to form H-shaped cells indicating a more complex structure and possibly a distinct evolutionary position of eMMPs when compared with sMMPs considering multicellularity., (© 2017 Society for Applied Microbiology and John Wiley & Sons Ltd.)

The bacterial flagellum is a motility organelle that consists of a rotary motor and a helical propeller. The flagella usually work individually or by forming a loose bundle to produce thrust. However, the flagellar apparatus of marine bacterium MO-1 is a tight bundle of seven flagellar filaments enveloped in a sheath, and it has been a mystery as to how the flagella rotate smoothly in coordination. Here we have used electron cryotomography to visualize the 3D architecture of the sheathed flagella. The seven filaments are enveloped with 24 fibrils in the sheath, and their basal bodies are arranged in an intertwined hexagonal array similar to the thick and thin filaments of vertebrate skeletal muscles. This complex and exquisite architecture strongly suggests that the fibrils counter-rotate between flagella in direct contact to minimize the friction of high-speed rotation of individual flagella in the tight bundle within the sheath to enable MO-1 cells to swim at about 300 µm/s.

Marine magnetotactic ovoid bacterium MO-1 is capable of swimming along the geomagnetic field lines by means of its two sheathed flagellar bundles at a speed up to 300 μm/s. In this study, by using electron microscopy, we showed that, in each bundle, six individual flagella were organized in hexagon with a seventh in the middle. We identified 12 flagellin paralogs and 2 putative flagellins in the genome of MO-1. Among them, 13 were tandemly located on an ~ 17-kb segment while the 14th was on a separated locus. Using reverse transcription PCR and quantitative PCR, we found that all the 14 flagellin or putative flagellin genes were transcribed and that 2 of them were more abundantly expressed than others. A nLC (nanoliquid chromatography)-ESI (electrospray ionization)-MS/MS (mass spectrometry/mass spectrometry) mass spectrometry analysis identified all the 12 flagellin proteins in three glycosylated polypeptide bands resolved by one-dimensional denaturing polyacrylamide gel electrophoresis and 10 of them in 21 spots obtained by means of two-dimensional electrophoresis of flagellar extracts. Most spots contained more than one flagellin, and eight of the ten identified flagellins existed in multiple isoforms. Taken together, these results show unprecedented complexity in the spatial organization and flagellin composition of the flagellar propeller. Such architecture is observed only for ovoid-coccoid, bilophotrichously flagellated magnetotactic bacteria living in marine sediments, suggesting a species and environmental specificity., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

Flagella of some pathogens or marine microbes are sheathed by an apparent extension of the outer cell membrane. Although flagellar sheath has been reported for almost 60 years, little is known about its function and the mechanism of its assembly. Recently, we have observed a novel type of sheath that encloses a flagellar bundle, instead of a single flagellum, in a marine magnetotactic bacterium MO-1. Here, we reported isolation and characterization of the sheath which can be described as a six-start, right-handed helical tubular structure with a diameter of about 100 nm, and a pitch of helix of about 260 nm. By proteomic, microscopic and immunolabelling analyses, we showed that the sheath of MO-1 consists of glycoprotein with an apparent molecular mass > 350 kDa. This protein, named sheath-associated protein (Sap), shows homology with bacterial adhesins and eukaryotic calcium-dependent adherent proteins (cadherin). Most importantly, we showed that calcium ions mediate the assembly of the tubular-shaped sheath and disintegration of the sheath was deleterious for smooth swimming of MO-1 cells. The disintegrated sheath was efficiently reconstituted in vitro by adding calcium ions. Altogether, these results demonstrate a novel bacterial Ca(2+) -dependent surface architecture, which is essential for bacterial swimming., (© 2010 Blackwell Publishing Ltd.)