Review Special Issues

Bacterial autoaggregation

  • Received: 10 January 2018 Accepted: 22 February 2018 Published: 01 March 2018
  • Many bacteria, both environmental and pathogenic, exhibit the property of autoaggregation. In autoaggregation (sometimes also called autoagglutination or flocculation), bacteria of the same type form multicellular clumps that eventually settle at the bottom of culture tubes. Autoaggregation is generally mediated by self-recognising surface structures, such as proteins and exopolysaccharides, which we term collectively as autoagglutinins. Although a widespread phenomenon, in most cases the function of autoaggregation is poorly understood, though there is evidence to show that aggregating bacteria are protected from environmental stresses or host responses. Autoaggregation is also often among the first steps in forming biofilms. Here, we review the current knowledge on autoaggregation, the role of autoaggregation in biofilm formation and pathogenesis, and molecular mechanisms leading to aggregation using specific examples.

    Citation: Thomas Trunk, Hawzeen S. Khalil, Jack C. Leo. Bacterial autoaggregation[J]. AIMS Microbiology, 2018, 4(1): 140-164. doi: 10.3934/microbiol.2018.1.140

    Related Papers:

  • Many bacteria, both environmental and pathogenic, exhibit the property of autoaggregation. In autoaggregation (sometimes also called autoagglutination or flocculation), bacteria of the same type form multicellular clumps that eventually settle at the bottom of culture tubes. Autoaggregation is generally mediated by self-recognising surface structures, such as proteins and exopolysaccharides, which we term collectively as autoagglutinins. Although a widespread phenomenon, in most cases the function of autoaggregation is poorly understood, though there is evidence to show that aggregating bacteria are protected from environmental stresses or host responses. Autoaggregation is also often among the first steps in forming biofilms. Here, we review the current knowledge on autoaggregation, the role of autoaggregation in biofilm formation and pathogenesis, and molecular mechanisms leading to aggregation using specific examples.


    加载中
    [1] Sorroche FG, Spesia MB, Zorreguieta A, et al. (2012) A positive correlation between bacterial autoaggregation and biofilm formation in native Sinorhizobium meliloti isolates from Argentina. Appl Environ Microb 78: 4092–4101. doi: 10.1128/AEM.07826-11
    [2] Kragh KN, Hutchison JB, Melaugh G, et al. (2016) Role of multicellular aggregates in biofilm formation. MBio 7: e00237-16.
    [3] Corno G, Coci M, Giardina M, et al. (2014) Antibiotics promote aggregation within aquatic bacterial communities. Front Microbiol 5: 297.
    [4] Ochiai K, Kurita-Ochiai T, Kamino Y, et al. (1993) Effect of co-aggregation on the pathogenicity of oral bacteria. J Med Microbiol 39: 183–190. doi: 10.1099/00222615-39-3-183
    [5] Malik A, Sakamoto M, Hanazaki S, et al. (2003) Coaggregation among nonflocculating bacteria isolated from activated sludge. Appl Environ Microb 69: 6056–6063. doi: 10.1128/AEM.69.10.6056-6063.2003
    [6] Farrell A, Quilty B (2002) Substrate-dependent autoaggregation of Pseudomonas putida CP1 during the degradation of mono-chlorophenols and phenol. J Ind Microbiol Biot 28: 316–324. doi: 10.1038/sj.jim.7000249
    [7] McLean JS, Pinchuk GE, Geydebrekht OV, et al. (2008) Oxygen-dependent autoaggregation in Shewanella oneidensis MR-1. Environ Microbiol 10: 1861–1876. doi: 10.1111/j.1462-2920.2008.01608.x
    [8] Schembri MA, Hjerrild L, Gjermansen M, et al. (2003) Differential expression of the Escherichia coli autoaggregation factor antigen 43. J Bacteriol 185: 2236–2242. doi: 10.1128/JB.185.7.2236-2242.2003
    [9] Skurnik M, Bölin I, Heikkinen H, et al. (1984) Virulence plasmid-associated autoagglutination in Yersinia spp. J Bacteriol 158: 1033–1036.
    [10] Bossier P, Verstraete W (1996) Triggers for microbial aggregation in activated sludge? Appl Microbiol Biot 45: 1–6. doi: 10.1007/s002530050640
    [11] Haaber J, Cohn MT, Frees D, et al. (2012) Planktonic aggregates of Staphylococcus aureus protect against common antibiotics. PLoS One 7: e41075. doi: 10.1371/journal.pone.0041075
    [12] Tree JJ, Ulett GC, Hobman JL, et al. (2007) The multicopper oxidase (CueO) and cell aggregation in Escherichia coli. Environ Microbiol 9: 2110–2116. doi: 10.1111/j.1462-2920.2007.01320.x
    [13] Fexby S, Bjarnsholt T, Jensen PØ, et al. (2006) Biological Trojan horse: Antigen 43 provides specific bacterial uptake and survival in human neutrophils. Infect Immun 75: 30–34.
    [14] Galdiero F, Carratelli CR, Nuzzo I, et al. (1988) Phagocytosis of bacterial aggregates by granulocytes. Eur J Epidemiol 4: 456–460. doi: 10.1007/BF00146398
    [15] Meuskens I, Michalik M, Chauhan N, et al. (2017) A new strain collection for improved expression of outer membrane proteins. Front Cell Infect Microbiol 7: 464. doi: 10.3389/fcimb.2017.00464
    [16] Formosa-Dague C, Feuillie C, Beaussart A, et al. (2016) Sticky matrix: adhesion mechanism of the staphylococcal polysaccharide intercellular adhesin. ACS Nano 10: 3443–3452. doi: 10.1021/acsnano.5b07515
    [17] Guerry P (2007) Campylobacter flagella: not just for motility. Trends Microbiol 15: 456–461. doi: 10.1016/j.tim.2007.09.006
    [18] Das T, Sharma PK, Busscher HJ, et al. (2010) Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl Environ Microb 76: 3405–3408. doi: 10.1128/AEM.03119-09
    [19] Arenas J, Cano S, Nijland R, et al. (2014) The meningococcal autotransporter AutA is implicated in autoaggregation and biofilm formation. Environ Microbiol 17: 1321–1337.
    [20] Ishikawa M, Nakatani H, Hori K (2012) AtaA, a new member of the trimeric autotransporter adhesins from Acinetobacter sp. Tol 5 mediating high adhesiveness to various abiotic surfaces. PLoS One 7: e48830.
    [21] Xiao L, Zhou L, Sun C, et al. (2012) Apa is a trimeric autotransporter adhesin of Actinobacillus pleuropneumoniae responsible for autoagglutination and host cell adherence. J Basic Microb 52: 598–607. doi: 10.1002/jobm.201100365
    [22] Inoue T, Tanimoto I, Ohta H, et al. (1998) Molecular characterization of low-molecular-weight component protein, Flp, in Actinobacillus actinomycetemcomitans fimbriae. Microbiol Immunol 42: 253–258. doi: 10.1111/j.1348-0421.1998.tb02280.x
    [23] Riess T, Raddatz G, Linke D, et al. (2006) Analysis of Bartonella adhesin A expression reveals differences between various B. henselae strains. Infect Immun 75: 35–43.
    [24] Zhang P, Chomel BB, Schau MK, et al. (2004) A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana. Proc Natl Acad Sci USA 101: 13630–13635. doi: 10.1073/pnas.0405284101
    [25] Menozzi FD, Boucher PE, Riveau G, et al. (1994) Surface-associated filamentous hemagglutinin induces autoagglutination of Bordetella pertussis. Infect Immun 62: 4261–4269.
    [26] Tomich M, Mohr CD (2003) Adherence and autoaggregation phenotypes of a Burkholderia cenocepacia cable pilus mutant. FEMS Microbiol Lett 228: 287–297. doi: 10.1016/S0378-1097(03)00785-7
    [27] Boddey JA, Flegg CP, Day CJ, et al. (2006) Temperature-regulated microcolony formation by Burkholderia pseudomallei requires pilA and enhances association with cultured human cells. Infect Immun 74: 5374–5381. doi: 10.1128/IAI.00569-06
    [28] Guerry P, Ewing CP, Schirm M, et al. (2006) Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol Microbiol 60: 299–311. doi: 10.1111/j.1365-2958.2006.05100.x
    [29] Hoeflinger JL, Miller MJ (2017) Cronobacter sakazakii ATCC 29544 autoaggregation requires FliC flagellation, not motility. Front Microbiol 8: 301.
    [30] Nataro JP, Deng Y, Maneval DR, et al. (1992) Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun 60: 2297–2304.
    [31] Sherlock O, Schembri MA, Reisner A, et al. (2004) Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J Bacteriol 186: 8058–8065. doi: 10.1128/JB.186.23.8058-8065.2004
    [32] Henderson IR, Meehan M, Owen P (1997) Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. FEMS Microbiol Lett 149: 115–120. doi: 10.1111/j.1574-6968.1997.tb10317.x
    [33] Bieber D, Ramer SW, Wu CY, et al. (1998) Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280: 2114. doi: 10.1126/science.280.5372.2114
    [34] Leo JC, Lyskowski A, Hattula K, et al. (2011) The structure of E. coli IgG-binding protein D suggests a general model for bending and binding in trimeric autotransporter adhesins. Structure 19: 1021–1030.
    [35] Fagan RP, Smith SGJ (2007) The Hek outer membrane protein of Escherichia coli is an auto-aggregating adhesin and invasin. FEMS Microbiol Lett 269: 248–255. doi: 10.1111/j.1574-6968.2006.00628.x
    [36] Bhargava S, Johnson BB, Hwang J, et al. (2009) Heat-resistant agglutinin 1 is an accessory enteroaggregative Escherichia coli colonization factor. J Bacteriol 191: 4934–4942. doi: 10.1128/JB.01831-08
    [37] Sherlock O, Vejborg RM, Klemm P (2005) The TibA adhesin/invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect Immun 73: 1954–1963. doi: 10.1128/IAI.73.4.1954-1963.2005
    [38] Gao ZP, Nie P, Lu JF, et al. (2015) Type III secretion system translocon component EseB forms filaments on and mediates autoaggregation of and biofilm formation by Edwardsiella tarda. Appl Environ Microb 81: 6078–6087. doi: 10.1128/AEM.01254-15
    [39] Hendrixson DR, Geme JWS (1999) The Haemophilus influenzae Hap serine protease promotes adherence and microcolony formation, potentiated by a soluble host protein. Mol Cell 2: 841–850.
    [40] Pearson MM, Lafontaine ER, Wagner NJ, et al. (2002) A hag mutant of Moraxella catarrhalis strain O35E is deficient in hemagglutination, autoagglutination, and immunoglobulin D-binding activities. Infect Immun 70: 4523–4533. doi: 10.1128/IAI.70.8.4523-4533.2002
    [41] Hevia A, Martínez N, Ladero V, et al. (2013) An extracellular Serine/Threonine-rich protein from Lactobacillus plantarum NCIMB 8826 is a novel aggregation-promoting factor with affinity to mucin. Appl Environ Microb 79: 6059–6066. doi: 10.1128/AEM.01657-13
    [42] Abdel-Nour M, Duncan C, Prashar A, et al. (2013) The Legionella pneumophila collagen-like protein mediates sedimentation, autoaggregation, and pathogen-phagocyte interactions. Appl Environ Microb 80: 1441–1454.
    [43] Wu SS, Wu J, Kaiser D (1997) The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol Microbiol 23: 109–121. doi: 10.1046/j.1365-2958.1997.1791550.x
    [44] Park HS, Wolfgang M, van Putten JP, et al. (2001) Structural alterations in a type IV pilus subunit protein result in concurrent defects in multicellular behaviour and adherence to host tissue. Mol Microbiol 42: 293–307. doi: 10.1046/j.1365-2958.2001.02629.x
    [45] Carbonnelle E, Helaine S, Nassif X, et al. (2006) A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol 61: 1510–1522. doi: 10.1111/j.1365-2958.2006.05341.x
    [46] O'Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295–304. doi: 10.1046/j.1365-2958.1998.01062.x
    [47] Ausmees N, Jacobsson K, Lindberg M (2001) A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii. Microbiology 147: 549–559. doi: 10.1099/00221287-147-3-549
    [48] Collinson SK, Doig PC, Doran JL, et al. (1993) Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J Bacteriol 175: 12–18. doi: 10.1128/jb.175.1.12-18.1993
    [49] Kuroda M, Ito R, Tanaka Y, et al. (2008) Staphylococcus aureus surface protein SasG contributes to intercellular autoaggregation of Staphylococcus aureus. Biochem Bioph Res Co 377: 1102–1106. doi: 10.1016/j.bbrc.2008.10.134
    [50] Rohde H, Burdelski C, Bartscht K, et al. (2005) Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 55: 1883–1895. doi: 10.1111/j.1365-2958.2005.04515.x
    [51] Heilmann C, Schweitzer O, Gerke C, et al. (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20: 1083–1091. doi: 10.1111/j.1365-2958.1996.tb02548.x
    [52] Frick IM, Mörgelin M, Björck L (2000) Virulent aggregates of Streptococcus pyogenes are generated by homophilic protein-protein interactions. Mol Microbiol 37: 1232–1247. doi: 10.1046/j.1365-2958.2000.02084.x
    [53] Chiang SL, Taylor RK, Koomey M, et al. (1995) Single amino acid substitutions in the N-terminus of Vibrio cholerae TcpA affect colonization, autoagglutination, and serum resistance. Mol Microbiol 17: 1133–1142. doi: 10.1111/j.1365-2958.1995.mmi_17061133.x
    [54] Faris A, Lindahl M, Ljungh A, et al. (1983) Autoaggregating Yersinia enterocolitica express surface fimbriae with high surface hydrophobicity. J Appl Bacteriol 55: 97–100. doi: 10.1111/j.1365-2672.1983.tb02652.x
    [55] Mühlenkamp M, Oberhettinger P, Leo JC, et al. (2015) Yersinia adhesin A (YadA)-Beauty & beast. Int J Med Microbiol 305: 252–258. doi: 10.1016/j.ijmm.2014.12.008
    [56] Kolodziejek AM, Sinclair DJ, Seo KS, et al. (2007) Phenotypic characterization of OmpX, an Ail homologue of Yersinia pestis KIM. Microbiology 153: 2941–2951. doi: 10.1099/mic.0.2006/005694-0
    [57] Podladchikova O, Rykova V, Antonenka U, et al. (2012) Yersinia pestis autoagglutination is mediated by HCP-like protein and siderophore Yersiniachelin (Ych). Adv Exp Med Biol 954: 289–292. doi: 10.1007/978-1-4614-3561-7_36
    [58] Felek S, Lawrenz MB, Krukonis ES (2008) The Yersinia pestis autotransporter YapC mediates host cell binding, autoaggregation and biofilm formation. Microbiology 154: 1802–1812. doi: 10.1099/mic.0.2007/010918-0
    [59] Ojanen-Reuhs T, Kalkkinen N, Westerlund-Wikström B, et al. (1997) Characterization of the fimA gene encoding bundle-forming fimbriae of the plant pathogen Xanthomonas campestris pv. vesicatoria. J Bacteriol 179: 1280–1290. doi: 10.1128/jb.179.4.1280-1290.1997
    [60] Busch A, Waksman G (2012) Chaperone-usher pathways: diversity and pilus assembly mechanism. Phil Trans R Soc B 367: 1112–1122. doi: 10.1098/rstb.2011.0206
    [61] Van Gerven N, Klein RD, Hultgren SJ, et al. (2015) Bacterial amyloid formation: structural insights into curli biogensis. Trends Microbiol 23: 693–706. doi: 10.1016/j.tim.2015.07.010
    [62] Craig L, Pique ME, Tainer JA (2004) Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2: 363–378. doi: 10.1038/nrmicro885
    [63] Heilmann C (2011) Adhesion mechanisms of staphylococci. Adv Exp Med Biol 715: 105–123. doi: 10.1007/978-94-007-0940-9_7
    [64] Smeesters PR, McMillan DJ, Sriprakash KS (2010) The streptococcal M protein: a highly versatile molecule. Trends Microbiol 18: 275–282. doi: 10.1016/j.tim.2010.02.007
    [65] Glaubman J, Hofmann J, Bonney ME, et al. (2016) Self-association motifs in the enteroaggregative Escherichia coli heat-resistant agglutinin 1. Microbiology 162: 1091–1102. doi: 10.1099/mic.0.000303
    [66] Leo JC, Grin I, Linke D (2012) Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Phil Trans R Soc B 367: 1088–1101. doi: 10.1098/rstb.2011.0208
    [67] Fan E, Chauhan N, Udatha DB, et al. (2016) Type V Secretion Systems in Bacteria. Microbiol Spectrum 4.
    [68] Nesta B, Spraggon G, Alteri C, et al. (2012) FdeC, a novel broadly conserved Escherichia coli adhesin eliciting protection against urinary tract infections. MBio 3: 1–10. doi: 10.3391/mbi.2012.3.1.01
    [69] Klemm P, Vejborg RM, Sherlock O (2006) Self-associating autotransporters, SAATs: functional and structural similarities. Int J Med Microbiol 296: 187–195. doi: 10.1016/j.ijmm.2005.10.002
    [70] Balligand G, Laroche Y, Cornelis G (1985) Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination. Infect Immun 48: 782–786.
    [71] Misawa N, Blaser MJ (2000) Detection and characterization of autoagglutination activity by Campylobacter jejuni. Infect Immun 68: 6168–6175. doi: 10.1128/IAI.68.11.6168-6175.2000
    [72] Klemm P, Hjerrild L, Gjermansen M, et al. (2003) Structure-function analysis of the self-recognizing Antigen 43 autotransporter protein from Escherichia coli. Mol Microbiol 51: 283–296. doi: 10.1046/j.1365-2958.2003.03833.x
    [73] Montero DA, Velasco J, Del Canto F, et al. (2017) Locus of Adhesion and Autoaggregation (LAA), a pathogenicity island present in emerging Shiga Toxin-producing Escherichia coli strains. Sci Rep 7: 7011. doi: 10.1038/s41598-017-06999-y
    [74] Del Re B, Sgorbati B, Miglioli M, et al. (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31: 438–442. doi: 10.1046/j.1365-2672.2000.00845.x
    [75] Beloin C, Houry A, Froment M, et al. (2008) A short-time scale colloidal system reveals early bacterial adhesion dynamics. PLoS Biol 6: e167. doi: 10.1371/journal.pbio.0060167
    [76] Geng J, Henry N (2011) Short time-scale bacterial adhesion dynamics. Adv Exp Med Biol 715: 315–331. doi: 10.1007/978-94-007-0940-9_20
    [77] Heras B, Totsika M, Peters KM, et al. (2014) The antigen 43 structure reveals a molecular Velcro-like mechanism of autotransporter-mediated bacterial clumping. Proc Natl Acad Sci USA 111: 457–462. doi: 10.1073/pnas.1311592111
    [78] Hoiczyk E, Roggenkamp A, Reichenbecher M, et al. (2000) Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19: 5989–5999. doi: 10.1093/emboj/19.22.5989
    [79] Jonsson P, Wadström T (1984) Cell surface hydrophobicity of Staphylococcus aureus measured by the salt aggregation test (SAT). Curr Microbiol 10: 203–210. doi: 10.1007/BF01627256
    [80] Martinez R (1983) Plasmid-mediated and temperature-regulated surface properties of Yersinia enterocolitica. Infect Immun 41: 921–930.
    [81] Arenas J, Nijland R, Rodriguez FJ, et al. (2012) Involvement of three meningococcal surface-exposed proteins, the heparin-binding protein NhbA, the α-peptide of IgA protease and the autotransporter protease NalP, in initiation of biofilm formation. Mol Microbiol 87: 254–268.
    [82] Eboigbodin KE, Newton JRA, Routh AF, et al. (2005) Role of nonadsorbing polymers in bacterial aggregation. Langmuir 21: 12315–12319. doi: 10.1021/la051740u
    [83] Tsang TM, Wiese JS, Alhabeil JA, et al. (2017) Defining the Ail ligand-binding surface: hydrophobic residues in two extracellular loops mediate cell and extracellular matrix binding to facilitate Yop delivery. Infect Immun 85: e01047-15.
    [84] Kaiser PO, Riess T, Wagner CL, et al. (2008) The head of Bartonella adhesin A is crucial for host cell interaction of Bartonella henselae. Cell Microbiol 10: 2223–2234. doi: 10.1111/j.1462-5822.2008.01201.x
    [85] Meng G, Spahich N, Kenjale R, et al. (2011) Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation. EMBO J 30: 3864–3874. doi: 10.1038/emboj.2011.279
    [86] Fink DL, Buscher AZ, Green B, et al. (2003) The Haemophilus influenzae Hap autotransporter mediates microcolony formation and adherence to epithelial cells and extracellular matrix via binding regions in the C-terminal end of the passenger domain. Cell Microbiol 5: 175–186. doi: 10.1046/j.1462-5822.2003.00266.x
    [87] Fink DL, Geme JWS (2003) Chromosomal expression of the Haemophilus influenzae Hap autotransporter allows fine-tuned regulation of adhesive potential via inhibition of intermolecular autoproteolysis. J Bacteriol 185: 1608–1615. doi: 10.1128/JB.185.5.1608-1615.2003
    [88] Wolska KI, Grudniak AM, Rudnicka Z, et al. (2016) Genetic control of bacterial biofilms. J Appl Genet 57: 225–238. doi: 10.1007/s13353-015-0309-2
    [89] O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54: 49–79. doi: 10.1146/annurev.micro.54.1.49
    [90] Vaccari L, Molaei M, Niepa THR, et al. (2017) Films of bacteria at interfaces. Adv Colloid Interfac 247: 561–572. doi: 10.1016/j.cis.2017.07.016
    [91] Flemming HC, Wingender J, Szewzyk U, et al. (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14: 563–575. doi: 10.1038/nrmicro.2016.94
    [92] Gupta P, Sarkar S, Das B (2015) Biofilm, pathogenesis and prevention-a journey to break the wall: a review. Arch Microbiol 198: 1–15.
    [93] Anderson GG, O'Toole GA (2008) Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol 322: 85–105.
    [94] Dunne WM Jr (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15: 155–166. doi: 10.1128/CMR.15.2.155-166.2002
    [95] Bos R, Mei HCVD, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions-its mechanisms and methods for study. FEMS Microbiol Rev 23: 179–230. doi: 10.1111/j.1574-6976.1999.tb00396.x
    [96] Melaugh G, Hutchison J, Kragh KN, et al. (2016) Shaping the growth behaviour of biofilms initiated from bacterial aggregates. PLoS One 11: e0149683. doi: 10.1371/journal.pone.0149683
    [97] Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 14: 576–588. doi: 10.1038/nrmicro.2016.89
    [98] Laganenka L, Colin R, Sourjik V (2016) Chemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli. Nat Commun 7: 12984. doi: 10.1038/ncomms12984
    [99] Bible AN, Stephens BB, Ortega DR, et al. (2008) Function of a chemotaxis-like signal transduction pathway in modulating motility, cell clumping, and cell length in the alphaproteobacterium Azospirillum brasilense. J Bacteriol 190: 6365–6375. doi: 10.1128/JB.00734-08
    [100] Bible A, Russell MH, Alexandre G (2012) The Azospirillum brasilense Che1 chemotaxis pathway controls swimming velocity, which affects transient cell-to-cell clumping. J Bacteriol 194: 3343–3355. doi: 10.1128/JB.00310-12
    [101] Hiramatsu Y, Saito M, Otsuka N, et al. (2016) BipA is associated with preventing autoagglutination and promoting biofilm formation in Bordetella holmesii. PLoS One 11: e0159999. doi: 10.1371/journal.pone.0159999
    [102] Ramalingam B, Sekar R, Boxall JB (2013) Aggregation and biofilm formation of bacteria isolated from domestic drinking water. Water Sci Tech-W Sup 13: 1016–1023. doi: 10.2166/ws.2013.115
    [103] Blom JF, Zimmermann YS, Ammann T, et al. (2010) Scent of danger: floc formation by a freshwater bacterium is induced by supernatants from a predator-prey coculture. Appl Environ Microb 76: 6156–6163. doi: 10.1128/AEM.01455-10
    [104] Hahn MW, Moore ERB, Höfle MG (2000) Role of microcolony formation in the protistan grazing defense of the aquatic bacterium Pseudomonas sp. MWH1. Microb Ecol 39: 175–185.
    [105] Nikel PI, Martínez-García E, de Lorenzo V (2014) Biotechnological domestication of pseudomonads using synthetic biology. Nat Rev Microbiol 12: 368–379. doi: 10.1038/nrmicro3253
    [106] Klebensberger J, Rui O, Fritz E, et al. (2006) Cell aggregation of Pseudomonas aeruginosa strain PAO1 as an energy-dependent stress response during growth with sodium dodecyl sulfate. Arch Microbiol 185: 417–427. doi: 10.1007/s00203-006-0111-y
    [107] Klebensberger J, Lautenschlager K, Bressler D, et al. (2007) Detergent-induced cell aggregation in subpopulations of Pseudomonas aeruginosa as a preadaptive survival strategy. Environ Microbiol 9: 2247–2259. doi: 10.1111/j.1462-2920.2007.01339.x
    [108] Klebensberger J, Birkenmaier A, Geffers R, et al. (2009) SiaA and SiaD are essential for inducing autoaggregation as a specific response to detergent stress in Pseudomonas aeruginosa. Environ Microbiol 11: 3073–3086. doi: 10.1111/j.1462-2920.2009.02012.x
    [109] Hazelbauer GL, Falke JJ, Parkinson JS (2007) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33: 9–19.
    [110] Aravind L, Ponting CP (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176: 111–116. doi: 10.1111/j.1574-6968.1999.tb13650.x
    [111] Matz C, Bergfeld T, Rice SA, et al. (2004) Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ Microbiol 6: 218–226. doi: 10.1111/j.1462-2920.2004.00556.x
    [112] Zhou P, Liu J, Merritt J, et al. (2015) A YadA-like autotransporter, Hag1 in Veillonella atypica is a multivalent hemagglutinin involved in adherence to oral streptococci, Porphyromonas gingivalis, and human oral buccal cells. Mol Oral Microbiol 30: 269–279. doi: 10.1111/omi.12091
    [113] Corno G, Villiger J, Pernthaler J (2013) Coaggregation in a microbial predator-prey system affects competition and trophic transfer efficiency. Ecology 94: 870–881. doi: 10.1890/12-1652.1
    [114] Caceres SM, Malcolm KC, Taylor-Cousar JL, et al. (2014) Enhanced in vitro formation and antibiotic resistance of nonattached Pseudomonas aeruginosa aggregates through incorporation of neutrophil products. Antimicrob Agents Ch 58: 6851–6860. doi: 10.1128/AAC.03514-14
    [115] Owen P, Meehan M, de Loughry-Doherty H, et al. (1996) Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol Med Mic 16: 63–76. doi: 10.1111/j.1574-695X.1996.tb00124.x
    [116] Ulett GC, Valle J, Beloin C, et al. (2007) Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 75: 3233–3244. doi: 10.1128/IAI.01952-06
    [117] Zalewska-Piatek B, Zalewska-Piatek R, Olszewski M, et al. (2015) Identification of antigen Ag43 in uropathogenic Escherichia coli Dr+ strains and defining its role in the pathogenesis of urinary tract infections. Microbiology 161: 1034–1049. doi: 10.1099/mic.0.000072
    [118] Vo JL, Ortiz GCM, Subedi P, et al. (2017) Autotransporter adhesins in Escherichia coli pathogenesis. Proteomics: 1600431.
    [119] Valle J, Mabbett AN, Ulett GC, et al. (2008) UpaG, a new member of the trimeric autotransporter family of adhesins in uropathogenic Escherichia coli. J Bacteriol 190: 4147–4161. doi: 10.1128/JB.00122-08
    [120] Paton AW, Srimanote P, Woodrow MC, et al. (2001) Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect Immun 69: 6999–7009. doi: 10.1128/IAI.69.11.6999-7009.2001
    [121] Totsika M, Wells TJ, Beloin C, et al. (2012) Molecular characterization of the EhaG and UpaG trimeric autotransporter proteins from pathogenic Escherichia coli. Appl Environ Microb 78: 2179–2189. doi: 10.1128/AEM.06680-11
    [122] Lu Y, Iyoda S, Satou H, et al. (2006) A new immunoglobulin-binding protein, EibG, is responsible for the chain-like adhesion phenotype of locus of enterocyte effacement-negative, shiga toxin-producing Escherichia coli. Infect Immun 74: 5747–5755. doi: 10.1128/IAI.00724-06
    [123] Moreira CG, Palmer K, Whiteley M, et al. (2006) Bundle-forming pili and EspA are involved in biofilm formation by enteropathogenic Escherichia coli. J Bacteriol 188: 3952. doi: 10.1128/JB.00177-06
    [124] Personnic N, Striednig B, Hilbi H (2017) Legionella quorum sensing and its role in pathogen-host interactions. Curr Opin Microbiol 41: 29–35.
    [125] Yu VL, Plouffe JF, Pastoris MC, et al. (2002) Distribution of Legionella species and serogroups isolated by culture in patients with sporadic community-acquired legionellosis: an international collaborative survey. J Infect Dis 186: 127–128. doi: 10.1086/341087
    [126] Duncan C, Prashar A, So J, et al. (2011) Lcl of Legionella pneumophila is an immunogenic GAG binding adhesin that promotes interactions with lung epithelial cells and plays a crucial role in biofilm formation. Infect Immun 79: 2168–2181. doi: 10.1128/IAI.01304-10
    [127] Dehio C, Meyer M, Berger J, et al. (1997) Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalisation of the bacterial aggregate by a unique structure, the invasome. J Cell Sci 110: 2141–2154.
    [128] Moradali MF, Ghods S, Rehm BHA (2017) Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 7: 39.
    [129] Frederiksen B, Lanng S, Koch C, et al. (1996) Improved survival in the Danish center-treated cystic fibrosis patients: results of aggressive treatment. Pediatr Pulmonol 21: 153–158. doi: 10.1002/(SICI)1099-0496(199603)21:3<153::AID-PPUL1>3.0.CO;2-R
    [130] Khan TZ, Wagener JS, Bost T, et al. (1995) Early pulmonary inflammation in infants with cystic fibrosis. Am J Respir Crit Care Med 151: 1075–1082.
    [131] Walker TS, Tomlin KL, Worthen GS, et al. (2005) Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 73: 3693–3701. doi: 10.1128/IAI.73.6.3693-3701.2005
    [132] Häussler S (2004) Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Environ Microbiol 6: 546–551. doi: 10.1111/j.1462-2920.2004.00618.x
    [133] Drenkard E, Ausubel FM (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740–743. doi: 10.1038/416740a
    [134] Häussler S, Ziegler I, Löttel A, et al. (2003) Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol 52: 295–301. doi: 10.1099/jmm.0.05069-0
    [135] Goerke C, Wolz C (2010) Adaptation of Staphylococcus aureus to the cystic fibrosis lung. Int J Med Microbiol 300: 520–525. doi: 10.1016/j.ijmm.2010.08.003
    [136] Kaplan JB, Izano EA, Gopal P, et al. (2012) Low levels of β-lactam antibiotics induce extracellular DNA release and biofilm formation in Staphylococcus aureus. MBio 3: e00198-12.
    [137] Savin C, Martin L, Bouchier C, et al. (2014) The Yersinia pseudotuberculosis complex: characterization and delineation of a new species, Yersinia wautersii. Int J Med Microbiol 304: 452–463. doi: 10.1016/j.ijmm.2014.02.002
    [138] Reuter S, Connor TR, Barquist L, et al. (2014) Parallel independent evolution of pathogenicity within the genus Yersinia. Proc Natl Acad Sci USA 111: 6768–6773. doi: 10.1073/pnas.1317161111
    [139] Chauhan N, Wrobel A, Skurnik M, et al. (2016) Yersinia adhesins: An arsenal for infection. Proteom Clin Appl 10: 949–963. doi: 10.1002/prca.201600012
    [140] Laird WJ, Cavanaugh DC (1980) Correlation of autoagglutination and virulence of yersiniae. J Clin Microbiol 11: 430–432.
    [141] Kapperud G, Lassen J (1983) Relationship of virulence-associated autoagglutination to hemagglutinin production in Yersinia enterocolitica and Yersinia enterocolitica-like bacteria. Infect Immun 42: 163–169.
    [142] Nagano T, Kiyohara T, Suzuki K, et al. (1997) Identification of pathogenic strains within serogroups of Yersinia pseudotuberculosis and the presence of non-pathogenic strains isolated from animals and the environment. J Vet Med Sci 59: 153–158. doi: 10.1292/jvms.59.153
    [143] Falcão JP, Falcão DP, Pitondo-Silva A, et al. (2006) Molecular typing and virulence markers of Yersinia enterocolitica strains from human, animal and food origins isolated between 1968 and 2000 in Brazil. J Med Microbiol 55: 1539–1548. doi: 10.1099/jmm.0.46733-0
    [144] Fukushima H, Shimizu S, Inatsu Y (2011) Yersinia enterocolitica and Yersinia pseudotuberculosis detection in foods. J Pathog.
    [145] Freund S, Czech B, Trülzsch K, et al. (2008) Unusual, virulence plasmid-dependent growth behavior of Yersinia enterocolitica in three-dimensional collagen gels. J Bacteriol 190: 4111–4120. doi: 10.1128/JB.00156-08
    [146] Grosskinsky U, Schütz M, Fritz M, et al. (2007) A conserved glycine residue of trimeric autotransporter domains plays a key role in Yersinia adhesin A autotransport. J Bacteriol 189: 9011–9019. doi: 10.1128/JB.00985-07
    [147] Schütz M, Weiss EM, Schindler M, et al. (2010) Trimer stability of YadA is critical for virulence of Yersinia enterocolitica. Infect Immun 78: 2677–2690. doi: 10.1128/IAI.01350-09
    [148] Kapperud G, Namork E, Skurnik M, et al. (1987) Plasmid-mediated surface fibrillae of Yersinia pseudotuberculosis and Yersinia enterocolitica: relationship to the outer membrane protein YOP1 and possible importance for pathogenesis. Infect Immun 55: 2247–2254.
    [149] Felek S, Muszyński A, Carlson RW, et al. (2009) Phosphoglucomutase of Yersinia pestis is required for autoaggregation and polymyxin B resistance. Infect Immun 78: 1163–1175.
    [150] Bujnakova D, Kmet V (2002) Aggregation of animal lactobacilli with O157 enterohemorrhagic Escherichia coli. J Vet Med B Infect Dis Vet Public Health 49: 152–154. doi: 10.1046/j.1439-0450.2002.00526.x
    [151] Reid G, McGroarty JA, Angotti R, et al. (1988) Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Can J Microbiol 34: 344–351. doi: 10.1139/m88-063
  • Reader Comments
  • © 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(17948) PDF downloads(2032) Cited by(261)

Article outline

Figures and Tables

Figures(3)  /  Tables(1)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog