Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development

O'Toole, George A.; Kolter, Roberto

doi:10.1046/j.1365-2958.1998.01062.x

Cited by 2,697Bacterial biofilms and quorum sensingBiochemical and Structural CharacterizationBacterial Genetics and Biotechnology

Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development

O'Toole, George A., Kolter, Roberto·1998·Molecular Microbiology

DOI 10.1046/j.1365-2958.1998.01062.x

Open this paper in CoChat — free account

Abstract

The formation of complex bacterial communities known as biofilms begins with the interaction of planktonic cells with a surface in response to appropriate environmental signals. We report the isolation and characterization of mutants of Pseudomonas aeruginosa PA14 defective in the initiation of biofilm formation on an abiotic surface, polyvinylchloride (PVC) plastic. These mutants are designated surface attachment defective (sad ). Two classes of sad mutants were analysed: (i) mutants defective in flagellar-mediated motility and (ii) mutants defective in biogenesis of the polar-localized type IV pili. We followed the development of the biofilm formed by the wild type over 8 h using phase-contrast microscopy. The wild-type strain first formed a monolayer of cells on the abiotic surface, followed by the appearance of microcolonies that were dispersed throughout the monolayer of cells. Using time-lapse microscopy, we present evidence that microcolonies form by aggregation of cells present in the monolayer. As observed with the wild type, strains with mutations in genes required for the synthesis of type IV pili formed a monolayer of cells on the PVC plastic. However, in contrast to the wild-type strain, the type IV pili mutants did not develop microcolonies over the course of the experiments, suggesting that these structures play an important role in microcolony formation. Very few cells of a non-motile strain (carrying a mutation in flgK) attached to PVC even after 8 h of incubation, suggesting a role for flagella and/or motility in the initial cell-to-surface interactions. The phenotype of these mutants thus allows us to initiate the dissection of the developmental pathway leading to biofilm formation.

Integrity signals

Registry

Crossref · 10.1046/j.1365-2958.1998.01062.x

Cites

54 of 54 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Proteinaceous autoagglutinins include pili and fimbriae, flagella, large adhesin proteins such as M proteins and MSCRAMMs, and small β-barrel proteins.
“Proteinaceous autoagglutinins include pili and fimbriae [30],[46], flagella [28],[29], large adhesin proteins such as M proteins and MSCRAMMs (for microbial surface components recognising adhesive matrix molecules) [49],[52], and small β-barrel proteins [36],[56].”
From Bacterial autoaggregation (2018) · cites this paper as [46]
Autoaggregation can lead to microcolony formation and biofilm in two ways: single planktonic cells attach to the substrate and recruit other cells from suspension via autoagglutinins, or cells autoaggregate in solution and the aggregates settle on the substrate to initiate biofilm formation.
“Autoaggregation can lead to microcolony formation and biofilm in two ways (Figure 3). In the first, single planktonic cells attach to the substrate. This depends on expression of surface adhesins and possibly also motility factors [46]. Following this, these cells recruit other cells from suspension via autoagglutinins, leading to microcolony formation [75],[94].”
From Bacterial autoaggregation (2018) · cites this paper as [46]

Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
MICROBIAL BIOFILMS
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995) · Annual Review of Microbiology · doi:10.1146/annurev.mi.49.100195.003431 · Cited by 4,718 · see citing works
The Involvement of Cell-to-Cell Signals in the Development of a Bacterial Biofilm
Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., & Greenberg, E. P. (1998) · Science · doi:10.1126/science.280.5361.295 · Cited by 3,396 · see citing works
Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis
O'Toole, G. A., & Kolter, R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00797.x · Cited by 2,537 · see citing works
Self-citation
Rapid extraction of bacterial genomic DNA with guanidium thiocyanate
Pitcher, D. G., Saunders, N. A., & Owen, R. J. (1989) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.1989.tb00262.x · Cited by 2,148 · see citing works
Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia
Govan, J. R. W., & Deretic, V. P. (1996) · Microbiological Reviews · doi:10.1128/mr.60.3.539-574.1996 · Cited by 1,671 · see citing works
Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili
Pratt, L. A., & Kolter, R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.01061.x · Cited by 1,641 · see citing works
Self-citation
The genetic control and cytoplasmic expression of “Inducibility” in the synthesis of β-galactosidase by E. coli
Pardee, A. B., Jacob, F., & Monod, J. (1959) · Journal of Molecular Biology · doi:10.1016/s0022-2836(59)80045-0 · Cited by 1,125 · see citing works
Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material
Nickel, J. C., Ruseska, I., Wright, J. B., & Costerton, J. W. (1985) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.27.4.619 · Cited by 888 · see citing works
Infections Caused by Pseudomonas aeruginosa
Bodey, G. P., Bolivar, R., Fainstein, V., et al. (1983) · Clinical Infectious Diseases · doi:10.1093/clinids/5.2.279 · Cited by 868 · see citing works
Infections caused by Pseudomonas aeruginosa.
MUSSER, A. W., & Pr, B. (1961) · PubMed · Cited by 733 · see citing works
Type IV Pili, Transient Bacterial Aggregates, and Virulence of Enteropathogenic Escherichia coli
Bieber, D., Ramer, S. W., Wu, C.-Y., Murray, W. J., Tobe, T., Fernandez, R., & Schoolnik, G. K. (1998) · Science · doi:10.1126/science.280.5372.2114 · Cited by 465 · see citing works
Bacterial resistance to antibiotics: The role of biofilms
Hoyle, B. D., & Costerton, J. W. (1991) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-7139-6_2 · Cited by 451 · see citing works
Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa
Davies, D. G., Chakrabarty, A. M., & Geesey, G. G. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.4.1181-1186.1993 · Cited by 427 · see citing works
Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture
Davies, D. G., & Geesey, G. G. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.3.860-867.1995 · Cited by 400 · see citing works
A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models
WIMPENNY, J. W. T., & Colasanti, R. L. (2006) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.1997.tb00351.x · Cited by 362 · see citing works
New derivatives of transposon tn5 suitable for mobilization of replicons, generation of operon fusions and induction of genes in Gram-negative bacteria
Simon, R., Quandt, J., & Klipp, W. (1989) · Gene · doi:10.1016/0378-1119(89)90262-x · Cited by 346 · see citing works
Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili
Nunn, D., Bergman, S., & Lory, S. J. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.6.2911-2919.1990 · Cited by 342 · see citing works
Role of pili in adherence of Pseudomonas aeruginosa to mammalian buccal epithelial cells
Woods, D. E., Straus, D. C., JOHANSON, W. G., Berry, V. K., & Bass, J. A. (1980) · Infection and Immunity · doi:10.1128/iai.29.3.1146-1151.1980 · Cited by 339 · see citing works
Neisseria PilC protein identified as type-4 pilus tip-located adhesin
Rudel, T., Scheuerpflug, I., & Meyer, T. F. (1995) · Nature · doi:10.1038/373357a0 · Cited by 333 · see citing works
Green fluorescent protein as a marker for Pseudomonas spp
Bloemberg, G. V., O’Toole, G. A., Lugtenberg, B. J. J., et al. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.11.4543-4551.1997 · Cited by 324 · see citing works
Self-citation
Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots
de Weger, L. A., van der Vlugt, C. I., Wijfjes, A. H. M., Bakker, P. A. H. M., Schippers, B., & Lugtenberg, B. J. J. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.6.2769-2773.1987 · Cited by 322 · see citing works
A function of Pseudomonas aeruginosa PAO polar pili: twitching motility
Bradley, D. E. (1980) · Canadian Journal of Microbiology · doi:10.1139/m80-022 · Cited by 322 · see citing works
Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly.
Jonsson, A., Nyberg, G., & Normark, S. J. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07970.x · Cited by 300 · see citing works
Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus
Wu, S., & Kaiser, D. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_18030547.x · Cited by 283 · see citing works
Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria
Whitchurch, C. B., Hobbs, M., Livingston, S. P., et al. (1991) · Gene · doi:10.1016/0378-1119(91)90221-v · Cited by 276 · see citing works
Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures
Grant, C. C., Konkel, M. E., Cieplak, W., & Tompkins, L. S. (1993) · Infection and Immunity · doi:10.1128/iai.61.5.1764-1771.1993 · Cited by 275 · see citing works
Prevalence of Broad-Host-Range Lytic Bacteriophages of Sphaerotilus natans , Escherichia coli , and Pseudomonas aeruginosa
Jensen, E. C., Schrader, H. S., Rieland, B., et al. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.2.575-580.1998 · Cited by 270 · see citing works
Amplifying DNA with arbitrary oligonucleotide primers.Preprint
Caetano‐Anollés, G. (1993) · Genome Research · doi:10.1101/gr.3.2.85 · Cited by 261 · see citing works
Roles of Pseudomonas aeruginosa las and rhl Quorum-Sensing Systems in Control of Twitching Motility
Glessner, A. L., Smith, R. S., Iglewski, B. H., et al. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.5.1623-1629.1999 · Cited by 205 · see citing works
Interaction of two variable proteins (PilE and PilC) required for pilus‐mediated adherence of Neisseria gonorrhoeae to human epithelial cells
Rudel, T., van Putten, J. P. M., Gibbs, C. P., et al. (1992) · Molecular Microbiology · doi:10.1111/j.1365-2958.1992.tb02211.x · Cited by 202 · see citing works
Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus
Darzins, A. (1994) · Molecular Microbiology · doi:10.1111/j.1365-2958.1994.tb00296.x · Cited by 199 · see citing works
Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells
Doig, P. C., Todd, T., Sastry, P. A., Lee, K. K., Hodges, R. S., PARANCHYCH, W., & Irvin, R. T. (1988) · Infection and Immunity · doi:10.1128/iai.56.6.1641-1646.1988 · Cited by 184 · see citing works
Role of pili in the adherence of Pseudomonas aeruginosa to injured tracheal epithelium
Ramphal, R., SADOFF, J. C., Pyle, M., et al. (1984) · Infection and Immunity · doi:10.1128/iai.44.1.38-40.1984 · Cited by 176 · see citing works
Behavior ofPseudomonas fluorescens within the hydrodynamic boundary layers of surface microenvironments
Lawrence, J. R., DELAQUIS, P. J., Korber, D. R., et al. (1987) · Microbial Ecology · doi:10.1007/bf02011566 · Cited by 172 · see citing works
Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum
Homma, M., DeRosier, D. J., & Macnab, R. M. (1990) · Journal of Molecular Biology · doi:10.1016/s0022-2836(05)80266-9 · Cited by 168 · see citing works
Role of Pseudomonas aeruginosa pili in acute pulmonary infection
Tang, H. B., Kays, M., & Prince, A. S. (1995) · Infection and Immunity · doi:10.1128/iai.63.4.1278-1285.1995 · Cited by 168 · see citing works
Loss of virulence associated with absence of flagellum in an isogenic mutant of Pseudomonas aeruginosa in the burned-mouse model
Montie, T. C., Doyle-Huntzinger, D., Craven, R. C., et al. (1982) · Infection and Immunity · doi:10.1128/iai.38.3.1296-1298.1982 · Cited by 162 · see citing works
The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa - a review
Mattick, J. S., Whitchurch, C. B., & Alm, R. A. (1996) · Gene · doi:10.1016/s0378-1119(96)00441-6 · Cited by 152 · see citing works
Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre‐pilin‐like leader sequence
Alm, R. A., & Mattick, J. S. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02413.x · Cited by 150 · see citing works
Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein‐secretion systems and pilY1 encodes a gonococcal PilC homologue
Aim, R. A., Hallinan, J. P., Watson, A. A., & Mattick, J. S. (1996) · Molecular Microbiology · doi:10.1111/j.1365-2958.1996.tb02665.x · Cited by 138 · see citing works
Adherence of Pseudomonas aeruginosa to hydrophilic contact lenses and other substrata
Miller, M. J., & Ahearn, D. G. (1987) · Journal of Clinical Microbiology · doi:10.1128/jcm.25.8.1392-1397.1987 · Cited by 123 · see citing works
PilC of pathogenic Neisseria is associated with the bacterial cell surface
Rahman, M., Källström, H., Normark, S. J., & Jonsson, A. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.4601823.x · Cited by 115 · see citing works
Adhesion of Pseudomonas aeruginosa pilin-deficient mutants to mucin
Ramphal, R., Koo, L., Ishimoto, K. S., et al. (1991) · Infection and Immunity · doi:10.1128/iai.59.4.1307-1311.1991 · Cited by 112 · see citing works
Effect of Motility on Surface Colonization and Reproductive Success of Pseudomonas fluorescens in Dual-Dilution Continuous Culture and Batch Culture Systems
Korber, D. R., Lawrence, J. R., & Caldwell, D. E. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.5.1421-1429.1994 · Cited by 107 · see citing works
Molecular genetic analysis of type-4 pilus biogenesis and twitching motility using Pseudomonas aeruginosa as a model system – areview
Darzins, A., & Russell, M. A. (1997) · Gene · doi:10.1016/s0378-1119(97)00037-1 · Cited by 93 · see citing works
Roles of flagella, lipopolysaccharide, and a Ca2+-dependent cell surface protein in attachment of Rhizobium leguminosarum biovar viciae to pea root hair tips
Smit, G., Kijne, J., & Lugtenberg, B. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.1.569-572.1989 · Cited by 83 · see citing works
Role of Pili in the Pathogenesis of Pseudomonas aeruginosa Burn Infection
Sato, H., Okinaga, K., & Saito, H. (1988) · Microbiology and Immunology · doi:10.1111/j.1348-0421.1988.tb01372.x · Cited by 80 · see citing works
The pilE gene product of Pseudomonas aeruginosa, required for pilus biogenesis, shares amino acid sequence identity with the N‐termini of type 4 prepilin proteins
Russell, M. A., & Darztns, A. (1994) · Molecular Microbiology · doi:10.1111/j.1365-2958.1994.tb00489.x · Cited by 69 · see citing works
Ultrastructural study of microbiologic colonization of urinary catheters
Nickel, J. C., Downey, J. A., & Costerton, J. W. (1989) · Urology · doi:10.1016/0090-4295(89)90327-0 · Cited by 65 · see citing works
F116: A DNA bacteriophage specific for the pili of Pseudomonas aeruginosa strain PAO
Pemberton, J. M. (1973) · Virology · doi:10.1016/0042-6822(73)90203-1 · Cited by 43 · see citing works
Characterization of Pseudomonas aeruginosa fliO, a gene involved in flagellar biosynthesis and adherence
Simpson, D. A. C., Ramphal, R., & Lory, S. (1995) · Infection and Immunity · doi:10.1128/iai.63.8.2950-2957.1995 · Cited by 42 · see citing works
The role of pili in the attachment ofPseudomonas aeruginosato unworn hydrogel contact lenses
Fletcher, E. L., Weissman, B. A., Efron, N., et al. (1993) · Current Eye Research · doi:10.3109/02713689309033504 · Cited by 33 · see citing works
Regulation of Multicellular Development in MyxobacteriaPreprint
Kaiser, D. (1984) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969172.16.197 · Cited by 17 · see citing works

Flagged first, then by citations

Sorted by citations

Bacterial Biofilms: A Common Cause of Persistent Infections
Costerton, J. W., Stewart, P. S., & Greenberg, E. P. (1999) · Science · doi:10.1126/science.284.5418.1318 · Cited by 12,167 · see citing works
Biofilm formation as microbial development
O'Toole, G., Kaplan, H. B., & Kolter, R. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.49 · Cited by 3,571 · see citing works
Self-citation
Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm
Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., & Davies, D. G. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.4.1140-1154.2002 · Cited by 1,691 · see citing works
Bacterial adhesion: seen any good biofilms lately
Dunne, W. M. (2002) · Clinical Microbiology Reviews · doi:10.1128/cmr.15.2.155-166.2002 · Cited by 1,516 · see citing works
A component of innate immunity prevents bacterial biofilm development
Singh, P. K., Parsek, M. R., Greenberg, E. P., & Welsh, M. J. (2002) · Nature · doi:10.1038/417552a · Cited by 1,026 · see citing works
Biofilm Dispersal: Mechanisms, Clinical Implications, and Potential Therapeutic Uses
Kaplan, J. B. (2010) · Journal of Dental Research · doi:10.1177/0022034509359403 · Cited by 949 · see citing works
Bacterial autoaggregation
Trunk, T., Bacterial Cell Surface Group, S. F. G. A. E. B., S. Khalil, H., & C. Leo, J. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.1.140 · Cited by 444 · see citing works
“using type IV pili, and aggregate together [46,94].”
BackgroundMethod
Environmental factors that shape biofilm formation
Toyofuku, M., Inaba, T., Kiyokawa, T., Obana, N., Yawata, Y., & Nomura, N. (2016) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2015.1058701 · Cited by 429 · see citing works
The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum
Pukatzki, S., Kessin, R. H., & Mekalanos, J. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052704399 · Cited by 289 · see citing works
Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection
Häußler, S., Ziegler, I., Löttel, A., Götz, F. V., Rohde, M., Wehmhöhner, D., Saravanamuthu, S., Tümmler, B., & Steinmetz, I. (2003) · Journal of Medical Microbiology · doi:10.1099/jmm.0.05069-0 · Cited by 228 · see citing works
Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa
Schaber, J. A., Carty, N. L., McDonald, N. A., Graham, E. D., Cheluvappa, R., Griswold, J. A., & Hamood, A. N. (2004) · Journal of Medical Microbiology · doi:10.1099/jmm.0.45617-0 · Cited by 224 · see citing works
Anaerobic killing of mucoid Pseudomonas aeruginosa by acidified nitrite derivatives under cystic fibrosis airway conditions
Yoon, S. S. (2006) · Journal of Clinical Investigation · doi:10.1172/jci24684 · Cited by 212 · see citing works
Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing
Matz, C., Bergfeld, T., Rice, S. A., & Kjelleberg, S. (2004) · Environmental Microbiology · doi:10.1111/j.1462-2920.2004.00556.x · Cited by 200 · see citing works
S <scp>upragingival</scp> C <scp>alculus:</scp> F <scp>ormation and</scp> C <scp>ontrol</scp>
Jin, Y., & Yip, H.-K. (2002) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/154411130201300506 · Cited by 181 · see citing works
A mechanical signal transmitted by the flagellum controls signalling in <scp>B</scp> acillus subtilis 
Cairns, L. S., Marlow, V. L., Bissett, E., Ostrowski, A., & Stanley‐Wall, N. R. (2013) · Molecular Microbiology · doi:10.1111/mmi.12342 · Cited by 143 · see citing works
Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa
Häußler, S. (2004) · Environmental Microbiology · doi:10.1111/j.1462-2920.2004.00618.x · Cited by 143 · see citing works
Studies of Pseudomonas aeruginosa Mutants Indicate Pyoverdine as the Central Factor in Inhibition of Aspergillus fumigatus Biofilm
Sass, G., Nazik, H., Penner, J., Shah, H., Ansari, S. R., Clemons, K. V., Groleau, M.-C., Dietl, A.-M., Visca, P., Haas, H., et al. (2018) · Journal of Bacteriology · doi:10.1128/jb.00345-17 · Cited by 128 · see citing works
Pseudomonas aeruginosa -Catecholamine Inotrope Interactions
Freestone, P. P., Hirst, R. A., Sandrini, S. M., Sharaff, F., Fry, H., Hyman, S., & O'Callaghan, C. (2012) · Chest · doi:10.1378/chest.11-2614 · Cited by 107 · see citing works
Current concepts regarding the effect of wound microbial ecology and biofilms on wound healing
Black, C. E., & Costerton, J. W. (2010) · Surgical Clinics of North America · doi:10.1016/j.suc.2010.08.009 · Cited by 99 · see citing works
Molecular Strategies for Fimbrial Expression and Assembly
Wu, H., & Fives-Taylor, P. M. (2001) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/10454411010120020101 · Cited by 87 · see citing works
Staphylococcus epidermidis adhesion on hydrophobic and hydrophilic textured biomaterial surfaces
Xu, L.-C., & Siedlecki, C. A. (2014) · Biomedical Materials · doi:10.1088/1748-6041/9/3/035003 · Cited by 75 · see citing works
Mechanisms of Antibiotic and Biocide Resistance That Contribute to Pseudomonas aeruginosa Persistence in the Hospital Environment
Verdial, C., Serrano, I., Tavares, L., Gil, S., & Oliveira, M. (2023) · Biomedicines · doi:10.3390/biomedicines11041221 · Cited by 71 · see citing works
Flexible survival strategies of Pseudomonas aeruginosa in biofilms result in increased fitness compared with Candida albicans
Purschke, F. G., Hiller, E., Trick, I., & Rupp, S. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m112.017673 · Cited by 60 · see citing works
Gamma-aminobutyric acid acts as a specific virulence regulator in Pseudomonas aeruginosa
Dagorn, A., Hillion, M., Chapalain, A., Lesouhaitier, O., Duclairoir Poc, C., Vieillard, J., Chevalier, S., Taupin, L., Le Derf, F., & Feuilloley, M. G. J. (2013) · Microbiology · doi:10.1099/mic.0.061267-0 · Cited by 51 · see citing works
Temperature-Regulated Microcolony Formation byBurkholderia pseudomalleiRequirespilAand Enhances Association with Cultured Human Cells
Boddey, J. A., Flegg, C. P., Day, C. J., Beacham, I. R., & Peak, I. R. (2006) · Infection and Immunity · doi:10.1128/iai.00569-06 · Cited by 51 · see citing works
Swarming motility is modulated by expression of the putative xenosiderophore transporter SppR-SppABCD in Pseudomonas aeruginosa PA14
Pletzer, D., Braun, Y., & Weingart, H. (2016) · Antonie van Leeuwenhoek · doi:10.1007/s10482-016-0675-8 · Cited by 29 · see citing works
Function and benefits of natural competence in cyanobacteria: from ecology to targeted manipulation
Schirmacher, A. M., Hanamghar, S. S., & Zedler, J. A. Z. (2020) · Life · doi:10.3390/life10110249 · Cited by 28 · see citing works
Pili and other surface proteins influence the structure and the nanomechanical properties of Lactococcus lactis biofilms
Drame, I., Lafforgue, C., Formosa-Dague, C., Chapot-Chartier, M.-P., Piard, J.-C., Castelain, M., & Dague, E. (2021) · Scientific Reports · doi:10.1038/s41598-021-84030-1 · Cited by 28 · see citing works
Detection and Molecular Identification of Persistent Water Vessel Colonizing Bacteria in a Table Water Factory in Nigeria
Nwaiwu, O., & Nwachukwu, M. (2016) · British Microbiology Research Journal · doi:10.9734/bmrj/2016/24378 · Cited by 6 · see citing works

Dynamics and force generation of flagellum and pili in Caulobacter crescentus
Sauter, N. (2018) · edoc (University of Basel) · doi:10.5451/unibas-007085291
Cross-regulation of Pseudomonas motility systems: the intimate relationship between flagella, pili and virulence
Kazmierczak, B. I., Schniederberend, M., & Jain, R. (2015) · Current Opinion in Microbiology · doi:10.1016/j.mib.2015.07.017 · Cited by 120 · see citing works
Social gliding is correlated with the presence of pili in Myxococcus xanthus.
Kaiser, D. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.5952 · Cited by 570 · see citing works
Parasites in motion: flagellum-driven cell motility in African trypanosomes
Hill, K. L. (2010) · Current Opinion in Microbiology · doi:10.1016/j.mib.2010.05.015 · Cited by 25 · see citing works
Prokaryotic motility structures
Bardy, S. L., Ng, S. Y. M., & Jarrell, K. F. (2003) · Microbiology · doi:10.1099/mic.0.25948-0 · Cited by 218 · see citing works

Authors: O'Toole, G. A., & Kolter, R.
Affiliations: Harvard University (US)
Corresponding author: Kolter, Roberto
ORCID: Kolter, Roberto
Venue: Molecular Microbiology
Publisher: Wiley
Published: 1998-10
Volume: 30
Issue: 2
Pages: 295-304
ISSN: 0950-382X (ISSN-L)
1365-2958
DOI: 10.1046/j.1365-2958.1998.01062.x
OpenAlex: W2016158447
Cited by: 2,697
References: 54
Citations by year: 2026: 50 · 2025: 77 · 2024: 82 · 2023: 90 · 2022: 125 · 2021: 131 · 2020: 115 · 2019: 117 · 2018: 89 · 2017: 109 · 2016: 136 · 2015: 140 · 2014: 155 · 2013: 125 · 2012: 133
FWCI: 13.28
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 1247 d)
Locations: Molecular Microbiology (publishedVersion)
PubMed (publishedVersion)
Funders: Damon Runyon Cancer Research Foundation
National Institutes of Health
National Institute of General Medical Sciences (R01GM058213, GM58213)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Pseudomonas aeruginosa, biofilm formation, flagellar motility, twitching motility, type IV pili, surface adhesion, microcolony formation, cell aggregation, abiotic surfaces, polyvinyl chloride, biofilm growth
MeSH terms: Flagella, Microscopy, Phase-Contrast, Mutation, Fimbriae, Bacterial, Pseudomonas aeruginosa, Biofilms

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks