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Flagella and Swimming Behavior of Marine Magnetotactic Bacteria biomolecules Review Flagella and Swimming Behavior of Marine Magnetotactic Bacteria Wei-Jia Zhang 1,2 and Long-Fei Wu 2,3,* 1 Laboratory of Deep-Sea Microbial Cell Biology, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China; [email protected] 2 International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, F-13402 CNRS-Marseille, France/CAS-Sanya 572000, China 3 Aix Marseille Univ, CNRS, LCB, IMM, IM2B, CENTURI, F-13402 Marseille, France * Correspondence: [email protected]; Tel.: +33-4-9116-4157 Received: 25 February 2020; Accepted: 15 March 2020; Published: 16 March 2020 Abstract: 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. Keywords: flagellar number and position; north-seeking and south-seeking; magnetic and photo-response 1. Introduction Magnetotactic bacteria (MTB) are a group of phylogenetically, morphologically, and physiologically diverse Gram-negative bacteria [1,2]. They share the common capability of synthesizing unique intracellular organelles, the magnetosomes, i.e., single-domain magnetic crystals of magnetite or greigite, which are enveloped by membranes (Figure1). Cytoskeleton MamK filaments enable the magnetosomes to be organized into chains [3–5]. Magnetosome chains impart a net magnetic dipole moment to the cell, which allows cells to align and swim along geomagnetic field lines [6]. This behavior, referred to as magnetotaxis, is believed to facilitate microaerophilic or anaerobic MTB to locate at the preferable oxic–anoxic interface in chemically stratified sediments or water columns [1]. Biomolecules 2020, 10, 460; doi:10.3390/biom10030460 www.mdpi.com/journal/biomolecules Biomolecules 2020, 10, 460 2 of 14 Biomolecules 2020, 9, x 2 of 14 Figure 1. Magnetosomes and flagellaflagella of magnetotactic bacteria.bacteria. ((AA)) BilophotrichouslyBilophotrichously flagellated flagellated MO-1 MO- cells1 cells possess possess two two sheathed sheathed flagellar flagellar bundles bundles (green (green arrow) arrow) and one and magnetosome one magnetosome chain (yellowchain (yellow arrow). (arrow).B) Peritrichously (B) Peritrichously flagellated flagellated ellipsoidal magnetoglobuleellipsoidal magnetoglobule with flagella with (blue flagella arrows) and(blue magnetosomes arrows) and (yellowmagnetosomes arrows). (yellow Only the arrows). portion Only of flagellar the portion filaments of flagellar in the surfacefilaments matrix in the was surface preserved matrix during was samplepreserved preparation. during sample Scale bar preparation. is equal to 0.5Scaleµm. bar Courtesy is equal of the toelectron 0.5 µm. cryotomography Courtesy of the micrograph electron (cryotomographyA) from Dr. J. Ruan micrograph and Professor (A) from K. Namba,Dr. J. Ruan and and of the Professor Scan-TEM K. Namba, high-angle and annular of the Scan-TEM dark-field (STEM-HAADF)high-angle annular mode dark-field micrograph (STEM-HAADF) (B) of ultrathin mode sections micrograph of high-pressure (B) of freezingultrathin/freeze sections substitution of high- fixationpressure (HPF freezing/freeze/FS) fixed ellipsoidal substitution magnetoglobule fixation (HPF/FS) from Professor fixed ellipsoidal N. Menguy magnetoglobule and Dr. A. Kosta. from Professor N. Menguy and Dr. A. Kosta. Phylogenetically, magnetotactic bacteria are members of several classes of the Proteobacteria phylumPhylogenetically, including the Alpha-,magnetotactic Gamma-, bacteria Delta-, are Zeta-, membCandidatusers of severalLambda-, classesCandidatus of the Eta-classes,Proteobacteria the Nitrospiraephylum including phylum, the the Alpha-,Candidatus Gamma-,Omnitrophica Delta-, Zeta-, phylum, Candidatus the Candidatus Lambda-,Latescibacteria Candidatus Eta-classes, phylum, andthe Nitrospirae the Planctomycetes phylum, phylum the Candidatus [7]. They Omnitrophica present various phylum, morphotypes the Candidatus including Latescibacteria cocci, spirilla, rod-shaped,phylum, and vibrio, the Planctomycetes and more complex phylum multicellular [7]. They present magnetotactic various prokaryotes morphotypes that including are also calledcocci, magnetoglobulesspirilla, rod-shaped, (MMP) vibrio, [1, 8and]. more complex multicellular magnetotactic prokaryotes that are also calledMagnetotactic magnetoglobules bacteria (MMP) are found[1,8]. worldwide in aquatic environments from freshwater to marine ecosystems.Magnetotactic Here, we bacteria will discuss are found mainly worldwide three types in aq ofuatic marine environments magnetotactic from bacteria freshwater because to ofmarine their complexecosystems. flagellar Here, architecture we will discuss and peculiar mainly motilethree ty behavior.pes of marine The first magnetotactic is the spirillum bacteriaMagnetospira because sp.of straintheir QH-2complex isolated flagellar from thearchitecture intertidal sedimentsand peculiar of the motile China Seabehavior. [9]. Phylogenetically, The first is the QH-2 spirillum belongs toMagnetospira Rhodospirillaceae sp. strain and isQH-2 closely isolated related from to two the freshwater intertidal magnetotactic sediments spirilla,of the MagnetospirillumChina Sea [9]. magneticumPhylogenetically,AMB-1 QH-2 and Magnetospirillum belongs to Rhodospirillac gryphiswaldenseeaeMSR-1. and is Yet, closely certain related traits suchto two as the freshwater synthesis + + ofmagnetotactic osmoprotectant, spirilla, Na Magnetospirillum-dependent NADH-quinone magneticum oxidoreductase,AMB-1 and Magnetospirillum and Na -motive gryphiswaldense force driven flagellarMSR-1. Yet, motors, certain make traits QH-2 such betteras the suitedsynthesis to aof marine osmoprotectant, sedimentary Na+ lifestyle-dependent than NADH-quinone its freshwater counterpartsoxidoreductase, [10 ].and The Na second+-motive is theforce ovoid-coccoid driven flagellarMagnetococcus motors, make massalia QH-2strain better MO-1 suited isolated to a marine from sedimentssedimentary of thelifestyle Mediterranean than its freshwater Sea (Figure 1counteA) [ 11rparts]. MO-1 [10]. belongs The tosecond the newly is the established ovoid-coccoid class CandidatusMagnetococcusEtatproteobacteria massalia strain MO-1 and possesses isolated from the mostsediments exquisite of the flagellar Mediterranean apparatus Sea [12 (Figure]. The third1, A) group[11]. MO-1 is the belongs magnetoglobules to the newly that established have developed class Candidatus both multicellular Etatproteobacteria and magnetotactic and possesses properties the duringmost exquisite their evolution. flagellar apparatus To date, magnetotactic [12]. The third multicellular group is the prokaryotesmagnetoglobules are found that have only developed in marine environmentsboth multicellular [8]. They and exhibit magnetotactic peculiar patternsproperties of motility during by their coordinatively evolution. rotating To date, tens magnetotactic of thousands ofmulticellular peritrichous prokaryotes flagella (Figure are 1foundB), including only in bothmarine polar environments and axis magneto-aerotaxis, [8]. They exhibit ping-pong peculiar patterns motion, andof motility photophobic by coordinatively and photokinesis rotating swimming tens of patterns. thousands of peritrichous flagella (Figure 1, B), including both polar and axis magneto-aerotaxis, ping-pong motion, and photophobic and 2. Flagellar Apparatus of Marine Magnetotactic Bacteria photokinesis swimming patterns. Flagella provide one of the most highly efficient means of bacterial locomotion and play a pivotal role2. Flagellar in adhesion, Apparatus biofilm of formation, Marine Magnetotactic and host invasion Bacteria [13–16 ]. Bacterial flagella share a basic tripartite structure;Flagella the provide basal body, one theof the hook, most and highly the filamentefficient [means17]. The of bacterial basal body locomotion contains aand reversible play a pivotal rotary motorrole in madeadhesion, of a rotor,biofilm a driveformation, shaft, and a bushing, host invasion and about [13–16]. a dozen Bacterial stators. flagella The stator share forms a basic the tripartite proton orstructure; sodium the ion basal pathway body, and the converts hook, and ion the flow filament across [17]. the cytoplasmicThe basal body membrane contains into a reversible the mechanical rotary workmotor required made of fora rotor, flagellar a drive motor shaft, rotation. a bushing, The and basal about body a dozen also contains stators. theThe flagellarstator
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