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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    International and American Associations for Dental Research

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    - Jul 1, 2004Version of Record >>

    at Sidney Sussex College on October 7, 2014 For personal use only. No other uses without permission.cro.sagepub.comDownloaded from

    International and American Associations for Dental Research

    at Sidney Sussex College on October 7, 2014 For personal use only. No other uses without permission.cro.sagepub.comDownloaded from

    International and American Associations for Dental Research

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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.

    at Sidney Sussex College on October 7, 2014 For personal use only. No other uses without permission.cro.sagepub.comDownloaded from

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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 rela

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