CHEMOTAXIS-GUIDED MOVEMENTS IN BACTERIA

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  • http://cro.sagepub.com/Critical Reviews in Oral Biology & Medicine

    http://cro.sagepub.com/content/15/4/207The online version of this article can be found at:

    DOI: 10.1177/154411130401500404

    2004 15: 207CROBMRenate Lux and Wenyuan Shi

    Chemotaxis-guided Movements in Bacteria

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  • 15(4):207-220 (2004) Crit Rev Oral Biol Med 207

    (1) Preface

    The first observation of bacterial movement was made byAntony van Leeuwenkoek in 1683. While examining den-tal plaque from the mouth of an old man, Leeuwenhoek found"an unbelievably great company of living animalcules, a-swimming more nimbly than any I had ever seen up to thistime. The biggest sort...bent their body into curves in goingforwards.... Moreover, the other animalcules were in suchenormous numbers, that all the water...seemed to be alive ...."(Fig. 1). Some of the bacteria described by van Leeuwenhoekare now recognized as the highly motile oral spirocheteswhose corkscrew-like motility results in a very remarkableswimming behavior that will be addressed in more detail later.

    (2) Bacterial MovementSince van Leeuwenhoek's first report on bacterial motility, themajority of bacterial species were found to be motile during atleast a part of their life cycle (Fenchel, 2002). Bacterial motilitycan be categorized into flagellum-dependent motility and flagel-lum-independent motility. The flagellum is a bacterial motilityapparatus that, in most motile species, can be observed on thecell surface as long filamentous cellular appendices (Macnab,1996). The species variety within the bacterial kingdom is reflect-ed by an impressive diversity in flagellation patterns that com-monly serves as means of classification: Single or multiple fla-gella can be found at one cell pole (e.g., Helicobacter pylori,Pseudomonas sp., Vibrio sp., or Chromatium okenii), at both cellpoles (e.g., spirochetes or Spirillum sp.), in the middle of a cellbody (e.g., Rhodobacter spheroides or Selenomonas sp.), or all overthe cell body (Escherichia coli, Salmonella sp., or Bacillus subtilis).

    While, for the most part, bacterial motility is associatedwith the presence of at least one flagellum, some bacteria dotranslocate without the aid of flagella. The best-studied flagel-lum-independent types of motility include the gliding motilityof myxobacteria, cyanobacteria, mycobacteria and theCytophaga-Flavobacterium group, the twitching motility ofPseudomonas, Neisseria, and Synechocystis (McBride, 2001), and

    the swimming motility of Synechococcus (Ehlers et al., 1996).Flagellum-dependent motility, which generates bacterial

    movement via rotation of the flagellar filaments in aquatic envi-ronments, has been extensively studied, revealing remarkableamounts of detailed structural and functional information(Macnab, 1996, 1999; Aldridge and Hughes, 2002). Much less isknown about flagellum-independent motility, which is mainlyinvolved in surface translocation. Recent studies suggest thatseveral independent mechanisms are involved (McBride, 2001;Bardy et al., 2003). Substantial evidence has been generated sup-porting a model for twitching motility of Pseudomonas aeruginosaand Neisseria gonorrhoeae as well as for cell-group gliding motil-ity of Myxococcus xanthus. In these species, movement is medi-ated through the extension, adherence, and retraction of type IVpili (Merz et al., 2000; Sun et al., 2000; Skerker and Berg, 2001; Liet al., 2003). It appears that the single-cell gliding motility ofcyanobacteria and myxobacteria is associated with secretion ofcarbohydrate containing slimes (Hoiczyk and Baumeister, 1995,1998; Wolgemuth et al., 2002). Surface translocation of the bacte-ria in the Cytophaga-Flavobacterium group may involve adher-ence of moving outer membrane components to the surface(Lapidus and Berg, 1982). However, various other motility mod-elsincluding wave generation in the outer membrane andmuscle-like expansion/contraction mechanismshave beenproposed (Duxbury et al., 1980; Burchard, 1984). The glidingmotility of mycobacteria requires unique membrane proteinsthat modulate surface attachment/detachment by altering thehydrophobicity of the cell envelope (Recht et al., 2000), whereasthe swimming motility of Synechococcus appears to rely onstructures analogous to the cilia of eukaryotic organisms(Samuel et al., 2001).

    (3) Bacterial ChemotaxisMore than two centuries after the detection of motile micro-organisms, Theodor Engelmann and Wilhelm Pfeffer foundthat bacterial movement was not random and arbitrary(Engelmann, 1883; Pfeffer, 1884). Instead, bacterial cells exhibit-

    CHEMOTAXIS-GUIDED MOVEMENTS IN BACTERIA

    Renate LuxWenyuan Shi*

    School of Dentistry, Department of Microbiology, Immunology and Molecular Genetics, University of California-Los Angeles, Los Angeles, CA 90095; *corresponding author, wenyuan@ucla.edu

    ABSTRACT: Motile bacteria often use sophisticated chemotaxis signaling systems to direct their movements. In general, bac-terial chemotactic signal transduction pathways have three basic elements: (1) signal reception by bacterial chemoreceptorslocated on the membrane; (2) signal transduction to relay the signals from membrane receptors to the motor; and (3) signaladaptation to desensitize the initial signal input. The chemotaxis proteins involved in these signal transduction pathways havebeen identified and extensively studied, especially in the enterobacteria Escherichia coli and Salmonella enterica serovar typhimuri-um. Chemotaxis-guided bacterial movements enable bacteria to adapt better to their natural habitats via moving toward favor-able conditions and away from hostile surroundings. A variety of oral microbes exhibits motility and chemotaxis, behaviors thatmay play important roles in bacterial survival and pathogenesis in the oral cavity.

    Key words. Motility, chemotaxis, pathogenesis, oral bacteria.

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  • ed directed movement toward certain stimuli and away fromothers, a behavior they termed 'chemotaxis'. The discovery ofchemotaxis gave a completely new meaning to the ability ofbacteria to move within their environment. With the recogni-tion of chemotaxis-guided bacterial motility, it became appar-ent that bacteria can respond efficiently to environmentalchanges. Almost every motile bacterial species studied so farhas been found to possess chemotactic abilities which enablethem to adapt better to their natural habitats. For example, thetumor-inducing Agrobacterium tumefaciens enhances coloniza-tion by moving chemotactically toward injured plant rootsguided by specific phenolics released by the wound sites(Hawes and Smith, 1989; Shaw, 1991), Rhizobium sp. are attract-ed by substances exuded by plant roots during nodulation(Ames et al., 1980; Parke et al., 1985; Armitage et al., 1988;Pandya et al., 1999), Halobacterium sp. use phototaxis that is trig-gered by light of the wavelengths required for photosynthesis(Schimz and Hildebrand, 1979; Sundberg et al., 1990; Krohs,1994; Cercignani et al., 2000), and motile E. coli and Salmonellacells move toward optimal nutrients such as sugars, aminoacids, and oxygen (Stock and Surette, 1996). In addition toresponses to environmental signals, motility and chemotaxishave been found to be involved in virulence of many patho-genic bacteria (Freter, 1981; Ottemann and Miller, 1997; Lux etal., 2000; Josenhans and Suerbaum, 2002).

    (4) Understanding the Molecular Mechanism of Chemotaxis

    Since its discovery, chemotactic behavior has stimulated thecuriosity of numerous investigators. However, it wasn't untilthe groundbreaking work by Julius Adlerusing genetic, bio-chemical, and behavioral approaches to analyze the chemotac-

    tic behavior of E. colithat a detailed understanding of thisphenomenon became possible (Adler, 1965, 1969, 1973, 1975;Armstrong et al., 1967; Armstrong and Adler, 1969a,b). Theintensive research efforts by numerous laboratories in the ensu-ing 40 years have yielded a comprehensive understanding ofthe molecular mechanism of bacterial chemotaxis. In general,the bacterial chemotactic signal transduction pathway hasthree basic elements (Fig. 2): (1) signal reception by bacterialchemoreceptors located on the membrane; (2) signal transduc-tion to relay the signals from membrane receptors to the motor;and (3) signal adaptation to desensitize the initial signal input.

    (4.1) SIGNAL RECEPTION BY MEMBRANE RECEPTORSBacterial chemoreceptors are membrane proteins that can bemodified by methylation at specific glutamate and glutamineresidues, and are therefore also called methyl-accepting chemo-taxis proteins (MCPs) (Kort et al., 1975). MCPs are very sensi-tive detection devices that can perceive the extracellular con-centrations of specific ligands at low concentrations in the Mto nM range (Clarke and Koshland, 1979; Biemann andKoshland, 1994; Lin et al., 1994). Most chemoreceptors bindonly a small number of specific ligands but do not transportthem. The occupancy with ligand is constantly monitored bythe cell and transformed into appropriate motor responses.Lack of a specific MCP does not affect the cell's general abilityto perform chemotaxis but only abolishes the response to thechemo-effectors perceived by the missing MCP (Adler, 1969).

    Recently, it has become evident that bacterial chemorecep-tors are not isolated entities but rather function as 'signaling lat-tices' that facilitate 'teamworking' of various receptor types for

    208 Crit Rev Oral Biol Med 15(4):207-220 (2004)

    Figure 1. Original drawing from Antony van Leeuwenhoek's notes.Shown are some types of bacteria that he observed in a dentalplaque sample. Among them appear to be cocci (E), fusiforme bac-teria (F), and spirochetes (G)

    Figure 2. Schematic illustration of basic chemotactic signal transduc-tion pathway. The proteins involved in the basic chemotactic signaltransduction pathway are shown. The excitation response involvessignal reception by the chemoreceptors (MCP) and further signaltransduction via CheW, CheA, and CheY to the flagella motor.Adaptation is achieved via methylation/demethylation of the MCPsby CheR and CheB. See text for details.

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  • stronger signal amplification (Ames et al., 2002; Gestwicki andKiessling, 2002). The individual receptor types form very stablehomodimers that are organized in higher-order structures ingroups of three (trimers of dimers) (Kim et al., 1999). These'trimers of dimers' tend to cluster in large patches at the cellpoles in a variety of bacteria (Alley et al., 1992; Maddock andShapiro, 1993; Harrison et al., 1999; Gestwicki et al., 2000). Thishigher-order clustering is thought to have an important biolog-ical role in signal amplification, since the clustered chemore-ceptors can sense very small changes in stimulus concentration(1-10%) that would otherwise not be detected (Mesibov et al.,1973; Jasuja et al., 1999; Kim et al., 2001). The clustering andpolar localization of the chemoreceptor that facilitates sensitiveresponses to small environmental changes is highly conservedamong bacteria. Phylogenetically very distant species like E.coli, B. subtilis, or Spirocheta aurantia exhibit very similar pat-terns (Lamanna et al., 2002).

    A 'classic' chemoreceptor is a membrane-spanning proteinthat can be divided into three major parts: an 'extra-cytoplas-mic' ligand-binding domain and a transmembrane segmentthat connects to a cytoplasmic portion consisting of the signal-ing and methyl-accepting domains. The MCPs of E. coli and S.enterica serovar typhimurium have been intensively studied bygenetic, biochemical, and structural analysis techniques forseveral decades, and detailed structural and functional infor-mation has been revealed. Structural analysis uncovered amainly helical composition of the MCPs. X-ray crystallographyshowed that the periplasmic ligand-binding or sensory domainof the enteric chemoreceptors consists of a four-helix bundle(Fig. 3) (Milburn et al., 1991; Yeh et al., 1993). Two of thesehelices extend into the cytoplasmic membrane as the trans-membrane portion. Ligand-binding surfaces have been identi-fied via genetic mapping of the residues involved (Kossmann etal., 1988; Wolff and Parkinson, 1988; Mowbray and Koshland,1990; Gardina et al., 1992; Scott et al., 1993) and co-crystalizationof the ligand with the ligand-binding domain (Milburn et al.,1991). The structural changes that are induced upon ligand-binding to the sensory domain of the receptor and transmittedvia the transmembrane segment to the cytoplasmic domainhave been analyzed in great detail by solid-state nuclear mag-netic resonance (NMR) and spin-labeling electron paramagnet-ic resonance (EPR) techniques (Ottemann et al., 1998).

    Recently, deviations from the 'standard' ligand-bindingdomain have been discovered in a variety of bacterial species:Caulobacter crescentus, R. spheroides, the archeon Halobacteriumsalinarium, B. subtilis, and possibly others that contain 'soluble'receptors missing the transmembrane part (Harrison et al.,1999; Larsen et al., 1999; Hou et al., 2000, 2001; Potocka et al.,2002; Wadhams et al., 2002). These receptors are membrane-associated or found in the cytoplasm rather than integratedinto the membrane. Interestingly, similar to myoglobin, the sol-uble chemoreceptors of H. salinarium and B. subtilis carry heme-groups in their sen...

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