Abstract
The flagellum is a locomotive organelle that allows bacteria to respond to chemical gradients. This review summarizes the current knowledge regarding Escherichia coli flagellin variants and the role of flagella in bacterial functions other than motility, including the relationship between flagella and bacterial virulence.
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References
Allsopp LP, Beloin C, Ulett GC, Valle J, Totsika M, Sherlock O, Ghigo JM, Schembri MA (2012) Molecular characterization of UpaB and UpaC, two new autotransporter proteins of uropathogenic Escherichia coli CFT073. Infect Immun 80(1):321–332. doi:10.1128/IAI.05322-11
Barker CS, Meshcheryakova IV, Kostyukova AS, Samatey FA (2010) FliO regulation of FliP in the formation of the Salmonella enterica flagellum. PLoS Genet 6(9), e1001143. doi:10.1371/journal.pgen.1001143
Berger CN, Shaw RK, Ruiz-Perez F, Nataro JP, Henderson IR, Pallen MJ, Frankel G (2009) Interaction of enteroaggregative Escherichia coli with salad leaves. Environ Microbiol Rep 1(4):234–239. doi:10.1111/j.1758-2229.2009.00037.x
Beutin L, Strauch E (2007) Identification of sequence diversity in the Escherichia coli fliC genes encoding flagellar types H8 and H40 and its use in typing of Shiga toxin-producing E. coli O8, O22, O111, O174, and O179 strains. J Clin Microbiol 45(2):333–339. doi:10.1128/JCM.01627-06
Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB (2013) Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26(4):822–880. doi:10.1128/CMR.00022-13
Deane JE, Abrusci P, Johnson S, Lea SM (2010) Timing is everything: the regulation of type III secretion. Cell Mol Life Sci 67(7):1065–1075. doi:10.1007/s00018-009-0230-0
Donnenberg M (2013) Escherichia coli: pathotypes and principles of pathogenesis. Academic Press
Duan Q, Zhou M, Zhu X, Bao W, Wu S, Ruan X, Zhang W, Yang Y, Zhu J, Zhu G (2012) The flagella of F18ab Escherichia coli is a virulence factor that contributes to infection in a IPEC-J2 cell model in vitro. Vet Microbiol 160(1–2):132–140. doi:10.1016/j.vetmic.2012.05.015
Duan Q, Zhou M, Zhu X, Yang Y, Zhu J, Bao W, Wu S, Ruan X, Zhang W, Zhu G (2013a) Flagella from F18+Escherichia coli play a role in adhesion to pig epithelial cell lines. Microb Pathog 55:32–38. doi:10.1016/j.micpath.2012.09.010
Duan Q, Zhou M, Liang H, Zhu X, Guo Z, Li Y, Hardwidge PR, Zhu G (2013b) Contribution of flagellin subunit FliC to piglet epithelial cells invasion by F18ab E coli. Vet Microbiol 166(1–2):220–224. doi:10.1016/j.vetmic.2013.04.030
Evans LDB, Hughes C, Fraser GM (2014) Building a flagellum outside the bacterial cell. Trends Microbiol 22(10):566–572. doi:10.1016/j.tim.2014.05.009
Feng L, Liu B, Liu Y, Ratiner YA, Hu B, Li D, Zong X, Xiong W, Wang L (2008) A genomic islet mediates flagellar phase variation in Escherichia coli strains carrying the flagellin-specifying locus flk. J Bacteriol 190(13):4470–4477. doi:10.1128/JB.01937-07
Fleckenstein JM, Roy K, Fischer JF, Burkitt M (2006) Identification of a two-partner secretion locus of enterotoxigenic Escherichia coli. Infect Immun 74(4):2245–2258. doi:10.1128/IAI.74.4.2245-2258.2006
Fleckenstein JM, Hardwidge PR, Munson GP, Rasko DA, Sommerfelt H, Steinsland H (2010) Molecular mechanisms of enterotoxigenic Escherichia coli infection. Microbes Infect / Inst Pasteur 12(2):89–98. doi:10.1016/j.micinf.2009.10.002
Fraser GM, Bennett JC, Hughes C (1999) Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol Microbiol 32(3):569–580. doi:10.1046/j.1365-2958.1999.01372.x
Galan JE, Lara-Tejero M, Marlovits TC, Wagner S (2014) Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68(68):415–438. doi:10.1146/annurev-micro-092412-155725
Ghelardi E, Celandroni F, Salvetti S, Beecher DJ, Gominet M, Lereclus D, Wong AC, Senesi S (2002) Requirement of flhA for swarming differentiation, flagellin export, and secretion of virulence-associated proteins in Bacillus thuringiensis. J Bacteriol 184(23):6424–6433. doi:10.1128/JB.184.23.6424-6433.2002
Giron JA, Torres AG, Freer E, Kaper JB (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44(2):361–379. doi:10.1046/j.1365-2958.2002.02899.x
Guttenplan SB, Kearns DB (2013) Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev 37(6):849–871. doi:10.1111/1574-6976.12018
Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410(6832):1099–1103. doi:10.1038/35074106
He Y, Keen JE, Westerman RB, Littledike ET, Kwang J (1996) Monoclonal antibodies for detection of the H7 antigen of Escherichia coli. Appl Environ Microbiol 62(9):3325–3332
Hossain MM, Tsuyumu S (2006) Flagella-mediated motility is required for biofilm formation by Erwinia carotovora subsp. carotovora. J Gen Plant Pathol 72(1):34–39. doi:10.1007/s10327-005-0246-8
Hung C, Zhou Y, Pinkner JS, Dodson KW, Crowley JR, Heuser J, Chapman MR, Hadjifrangiskou M, Henderson JP, Hultgren SJ (2013) Escherichia coli biofilms have an organized and complex extracellular matrix structure. MBio 4(5):e00645–13. doi:10.1128/mBio.00645-13
Ikeda JS, Schmitt CK, Darnell SC, Watson PR, Bispham J, Wallis TS, Weinstein DL, Metcalf ES, Adams P, O’Connor CD, O’Brien AD (2001) Flagellar phase variation of Salmonella enterica serovar typhimurium contributes to virulence in the murine typhoid infection model but does not influence Salmonella-induced enteropathogenesis. Infect Immun 69(5):3021–3030. doi:10.1128/Iai.69.5.3021-3030.2001
Jarvis KG, Kaper JB (1996) Secretion of extracellular proteins by enterohemorrhagic Escherichia coli via a putative type III secretion system. Infect Immun 64(11):4826–4829
Kansal R, Rasko DA, Sahl JW, Munson GP, Roy K, Luo Q, Sheikh A, Kuhne KJ, Fleckenstein JM (2013) Transcriptional modulation of enterotoxigenic Escherichia coli virulence genes in response to epithelial cell interactions. Infect Immun 81(1):259–270. doi:10.1128/IAI.00919-12
Kazmierczak BI, Hendrixson DR (2013) Spatial and numerical regulation of flagellar biosynthesis in polarly flagellated bacteria. Mol Microbiol 88(4):655–663. doi:10.1111/mmi.12221
Kuwajima G, Asaka J, Fujiwara T, Fujiwara T, Node K, Kondo E (1986) Nucleotide sequence of the hag gene encoding flagellin of Escherichia coli. J Bacteriol 168(3):1479–1483
La Ragione RM, Sayers AR, Woodward MJ (2000) The role of fimbriae and flagella in the colonization, invasion and persistence of Escherichia coli O78:K80 in the day-old-chick model. Epidemiol Infect 124(3):351–363. doi:10.1017/S0950268899004045
Lane MC, Simms AN, Mobley HL (2007) Complex interplay between type 1 fimbrial expression and flagellum-mediated motility of uropathogenic Escherichia coli. J Bacteriol 189(15):5523–5533. doi:10.1128/JB.00434-07
Lawn AM (1977) Comparison of the flagellins from different flagellar morphotypes of Escherichia coli. J Gen Microbiol 101(1):112–130
Lawn AM, Orskov I, Orskov F (1977) Morphological distinction between different H serotypes of Escherichia coli. J Gen Microbiol 101(1):111–119
Lehti TA, Bauchart P, Dobrindt U, Korhonen TK, Westerlund-Wikstrom B (2012) The fimbriae activator MatA switches off motility in Escherichia coli by repression of the flagellar master operon flhDC. Microbiol SGM 158(Pt 6):1444–1455. doi:10.1099/mic.0.056499-0
Liu B, Hu B, Zhou Z, Guo D, Guo X, Ding P, Feng L, Wang L (2012) A novel non-homologous recombination-mediated mechanism for Escherichia coli unilateral flagellar phase variation. Nucleic Acids Res 40(10):4530–4538. doi:10.1093/nar/gks040
Luck SN, Badea L, Bennett-Wood V, Robins-Browne R, Hartland EL (2006) Contribution of FliC to epithelial cell invasion by enterohemorrhagic Escherichia coli O113:H21. Infect Immun 74(12):6999–7004. doi:10.1128/IAI.00435-06
Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57:77–100. doi:10.1146/annurev.micro.57.030502.090832
Mahajan A, Currie CG, Mackie S, Tree J, McAteer S, McKendrick I, McNeilly TN, Roe A, La Ragione RM, Woodward MJ, Gally DL, Smith DG (2009) An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157: H7 with bovine intestinal epithelium. Cell Microbiol 11(1):121–137. doi:10.1111/j.1462-5822.2008.01244.x
Majander K, Anton L, Antikainen J, Lang H, Brummer M, Korhonen TK, Westerlund-Wikstrom B (2005) Extracellular secretion of polypeptides using a modified Escherichia coli flagellar secretion apparatus. Nat Biotechnol 23(4):475–481. doi:10.1038/Nbt1077
Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7(6):569–575. doi:10.1038/ni1344
Minamino T (2014) Protein export through the bacterial flagellar type III export pathway. Bba-Mol Cell Res 1843(8):1642–1648. doi:10.1016/j.bbamcr.2013.09.005
Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11(1):142–201
Neal-McKinney JM, Konkel ME (2012) The Campylobacter jejuni CiaC virulence protein is secreted from the flagellum and delivered to the cytosol of host cells. Front Cell Infect Mi 2 doi 10.3389/Fcimb.2012.00031
O’Brien EJ, Bennett PM (1972) Structure of straight flagella from a mutant Salmonella. J Mol Biol 70(1):133–152
Orskov F, Orskov I (1984) Serotyping of Escherichia coli. Academic Press, London, United Kingdom
Parthasarathy G, Yao Y, Kim KS (2007) Flagella promote Escherichia coli K1 association with and invasion of human brain microvascular endothelial cells. Infect Immun 75(6):2937–2945. doi:10.1128/IAI.01543-06
Poly F, Ewing C, Goon S, Hickey TE, Rockabrand D, Majam G, Lee L, Phan J, Savarino NJ, Guerry P (2007) Heterogeneity of a Campylobacter jejuni protein that is secreted through the flagellar filament. Infect Immun 75(8):3859–3867. doi:10.1128/Iai.00159-07
Quinones B, Dulla G, Lindow SE (2005) Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact 18(7):682–693. doi:10.1094/MPMI-18-0682
Ratiner YA (1982) Phase variation of the H antigen in Escherichia coli strain Bi7327-41, the standard strain for Escherichia coli flagellar antigen H3. FEMS Microbiol Lett 15(1):33–36. doi:10.1111/j.1574-6968.1982.tb00032.x
Ratiner YA (1983) Presence of two structural genes determining antigenically different phase‐specific flagellins in some Escherichia coli strains. FEMS Microbiol Lett 19(1):37–41
Ratiner YA (1987) Different alleles of the flagellin gene hagB in Escherichia coli standard H test strains. FEMS Microbiol Lett 48(1–2):97–104
Ratiner YA (1998) New flagellin-specifying genes in some Escherichia coli strains. J Bacteriol 180(4):979–984
Ratiner YA, Sihvonen LM, Liu Y, Wang L, Siitonen A (2010) Alteration of flagellar phenotype of Escherichia coli strain P12b, the standard type strain for flagellar antigen H17, possessing a new non-fliC flagellin gene flnA, and possible loss of original flagellar phenotype and genotype in the course of subculturing through semisolid media. Arch Microbiol 192(4):267–278. doi:10.1007/s00203-010-0556-x
Reid SD, Selander RK, Whittam TS (1999) Sequence diversity of flagellin (fliC) alleles in pathogenic Escherichia coli. J Bacteriol 181(1):153–160
Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2(3), e18. doi:10.1371/journal.ppat.0020018
Rogers TJ, Thorpe CM, Paton AW, Paton JC (2012) Role of lipid rafts and flagellin in invasion of colonic epithelial cells by Shiga-toxigenic Escherichia coli O113:H21. Infect Immun 80(8):2858–2867. doi:10.1128/IAI.00336-12
Rossez Y, Holmes A, Wolfson EB, Gally DL, Mahajan A, Pedersen HL, Willats WG, Toth IK, Holden NJ (2014) Flagella interact with ionic plant lipids to mediate adherence of pathogenic Escherichia coli to fresh produce plants. Environ Microbiol 16(7):2181–2195. doi:10.1111/1462-2920.12315
Roy K, Hilliard GM, Hamilton DJ, Luo J, Ostmann MM, Fleckenstein JM (2009) Enterotoxigenic Escherichia coli EtpA mediates adhesion between flagella and host cells. Nature 457(7229):594–598. doi:10.1038/nature07568
Samatey FA, Imada K, Nagashima S, Vonderviszt F, Kumasaka T, Yamamoto M, Namba K (2001) Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410(6826):331–337. doi:10.1038/35066504
Seah JN, Kwang J (2000) Identification of H-specific determinants in flagellin of four Escherichia coli strains. Arch Microbiol 174(1–2):28–34. doi:10.1007/s002030000167
Shaw RK, Berger CN, Pallen MJ, Sjoling A, Frankel G (2011) Flagella mediate attachment of enterotoxigenic Escherichia coli to fresh salad leaves. Environ Microbiol Rep 3(1):112–117. doi:10.1111/j.1758-2229.2010.00195.x
Simms AN, Mobley HL (2008) PapX, a P fimbrial operon-encoded inhibitor of motility in uropathogenic Escherichia coli. Infect Immun 76(11):4833–4841. doi:10.1128/IAI.00630-08
Singer HM, Erhardt M, Steiner AM, Zhang MM, Yoshikami D, Bulaj G, Olivera BM, Hughes KT (2012) Selective purification of recombinant neuroactive peptides using the flagellar type III secretion system. mBio 3(3) doi: 10.1128/mBio.00115-12
Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, Barrett SL, Cookson BT, Aderem A (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4(12):1247–1253. doi:10.1038/ni1011
Song YC, Jin S, Louie H, Ng D, Lau R, Zhang Y, Weerasekera R, Al Rashid S, Ward LA, Der SD, Chan VL (2004) FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol Microbiol 53(2):541–553. doi:10.1111/j.1365-2958.2004.04175.x
Terashima H, Kojima S, Homma M (2008) Flagellar motility in bacteria structure and function of flagellar motor. Int Rev Cell Mol Biol 270:39–85. doi:10.1016/s1937-6448(08)01402-0
Tosi T, Pflug A, Discola KF, Neves D, Dessen A (2013) Structural basis of eukaryotic cell targeting by type III secretion system (T3SS) effectors. Res Microbiol 164(6):605–619. doi:10.1016/j.resmic.2013.03.019
Troge A, Scheppach W, Schroeder BO, Rund SA, Heuner K, Wehkamp J, Stange EF, Oelschlaeger TA (2012) More than a marine propeller—the flagellum of the probiotic Escherichia coli strain Nissle 1917 is the major adhesin mediating binding to human mucus. Int J Med Microbiol 302(7–8):304–314. doi:10.1016/j.ijmm.2012.09.004
Ulett GC, Mabbett AN, Fung KC, Webb RI, Schembri MA (2007) The role of F9 fimbriae of uropathogenic Escherichia coli in biofilm formation. Microbiol SGM 153(Pt 7):2321–2331. doi:10.1099/mic.0.2006/004648-0
Vijay-Kumar M, Gewirtz AT (2009) Flagellin: key target of mucosal innate immunity. Mucosal Immunol 2(3):197–205. doi:10.1038/mi.2009.9
Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5(12):1024–1037. doi:10.1038/Nrm1524
Wang L, Rothemund D, Curd H, Reeves PR (2003) Species-wide variation in the Escherichia coli flagellin (H-antigen) gene. J Bacteriol 185(9):2936–2943. doi:10.1128/jb.185.9.2936-2943.2003
Wood TK, Gonzalez Barrios AF, Herzberg M, Lee J (2006) Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol 72(2):361–367. doi:10.1007/s00253-005-0263-8
Xicohtencatl-Cortes J, Sanchez Chacon E, Saldana Z, Freer E, Giron JA (2009) Interaction of Escherichia coli O157:H7 with leafy green produce. J Food Prot 72(7):1531–1537
Yang L, Liu Y, Wu H, Song Z, Hoiby N, Molin S, Givskov M (2012) Combating biofilms. FEMS Immunol Med Microbiol 65(2):146–157. doi:10.1111/j.1574-695X.2011.00858.x
Yang Y, Yao F, Zhou M, Zhu J, Zhang X, Bao W, Wu S, Hardwidge PR, Zhu G (2013) F18ab Escherichia coli flagella expression is regulated by acyl-homoserine lactone and contributes to bacterial virulence. Vet Microbiol 165(3–4):378–383. doi:10.1016/j.vetmic.2013.04.020
Yokoseki T, Kutsukake K, Ohnishi K, Iino T (1995) Functional analysis of the flagellar genes in the fliD operon of Salmonella typhimurium. Microbiol SGM 141(Pt 7):1715–1722. doi:10.1099/13500872-141-7-1715
Yonekura K, Maki-Yonekura S, Namba K (2001) Structure analysis of the flagellar cap-filament complex by electron cryomicroscopy and single-particle image analysis. J Struct Biol 133(2–3):246–253. doi:10.1006/jsbi.2000.4345
Yonekura K, Maki-Yonekura S, Namba K (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424(6949):643–650. doi:10.1038/nature01830
Young GM, Schmiel DH, Miller VL (1999) A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci U S A 96(11):6456–6461. doi:10.1073/pnas.96.11.6456
Zhou M, Duan Q, Zhu X, Guo Z, Li Y, Hardwidge PR, Zhu G (2013) Both flagella and F4 fimbriae from F4ac+ enterotoxigenic Escherichia coli contribute to attachment to IPEC-J2 cells in vitro. Vet Res 44(1):30. doi:10.1186/1297-9716-44-30
Zhou M, Guo Z, Duan Q, Hardwidge PR, Zhu G (2014a) Escherichia coli type III secretion system 2: a new kind of T3SS? Vet Res 45:32. doi:10.1186/1297-9716-45-32
Zhou M, Guo Z, Yang Y, Duan Q, Zhang Q, Yao F, Zhu J, Zhang X, Hardwidge PR, Zhu G (2014b) Flagellin and F4 fimbriae have opposite effects on biofilm formation and quorum sensing in F4ac+ enterotoxigenic Escherichia coli. Vet Microbiol 168(1):148–153. doi:10.1016/j.vetmic.2013.10.014
Zieg J, Silverman M, Hilmen M, Simon M (1977) Recombinational switch for gene expression. Science 196(4286):170–172
Acknowledgments
This study was funded by the 948 programme grant no. 2011-G24 from the Ministry of Agriculture of the People’s Republic of China, the Genetically Modified Organisms Technology Major Project of China (2014ZX08006-001B), grants from the Chinese National Science Foundation Grant (no. 31270171, no. 31072136, and no. 30771603), a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, a project funded by China Scholarship Council (201500090062), and a fund of excellent doctorial dissertations from Yangzhou University.
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Zhou, M., Yang, Y., Chen, P. et al. More than a locomotive organelle: flagella in Escherichia coli . Appl Microbiol Biotechnol 99, 8883–8890 (2015). https://doi.org/10.1007/s00253-015-6946-x
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DOI: https://doi.org/10.1007/s00253-015-6946-x