A field guide to bacterial swarming motility

Daniel B. Kearns

doi:10.1038/nrmicro2405

journal article Aug 09, 2010

A field guide to bacterial swarming motility

Daniel B. Kearns

Nature Reviews Microbiology Vol. 8 No. 9 pp. 634-644 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/nrmicro2405

Topics

No keywords indexed for this article. Browse by subject →

References

137

[1]

Living on a surface: swarming and biofilm formation

Natalie Verstraeten, Kristien Braeken, Bachaspatimayum Debkumari et al.

Trends in Microbiology 2008 10.1016/j.tim.2008.07.004

[2]

Henrichsen, J. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36, 478–503 (1972). This landmark study characterizes the motile behaviour of over 500 bacterial isolates and defines the main types of bacterial movement: swimming, swarming, twitching, gliding and sliding. 10.1128/mmbr.36.4.478-503.1972

[3]

Jarrell, K. F. & McBride, M. J. The surprisingly diverse ways that prokaryotes move. Nature Rev. Microbiol. 6, 466–476 (2008). 10.1038/nrmicro1900

[4]

Mattick, J. S. Type IV pili and twitching motility. Annu. Rev. Biochem. 56, 289–314 (2002).

[5]

Mignot, T. The elusive engine in Myxococcus xanthus gliding motility. Cell. Mol. Life Sci. 64, 2733–2745 (2007). 10.1007/s00018-007-7176-x

[6]

Matsuyama, T. et al. A novel extracellular cyclic lipopeptide which promotes flagellum-dependent and -independent spreading growth of Serratia marcescens. J. Bacteriol. 174, 1769–1776 (1992). 10.1128/jb.174.6.1769-1776.1992

[7]

Kinsinger, R. F., Kearns, D. B., Hale, M. & Fall, R. Genetic requirements for potassium ion-dependent colony spreading in Bacillus subtilis. J. Bacteriol. 187, 8462–8469 (2005). 10.1128/jb.187.24.8462-8469.2005

[8]

Murray, T. S. & Kazmierczak, B. I. Pseudomonas aeruginosa exhibits sliding motiliy in the absence of type IV pili and flagella. J. Bacteriol. 190, 2700–2708 (2008). 10.1128/jb.01620-07

[9]

Matsuyama, T., Bhasin, A. & Harshey, R. M. Mutational analysis of flagellum-independent surface spreading of Serratia marcescens 274 on a low-agar medium. J. Bacteriol. 177, 987–991 (1995). 10.1128/jb.177.4.987-991.1995

[10]

Be'er, A. et al. Paenibacillus dendritiformis bacterial colony growth depends on surfactant but not on bacterial motion. J. Bacteriol. 191, 5758–5764 (2009). 10.1128/jb.00660-09

[11]

Kearns, D. B. & Losick, R. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49, 581–590 (2003). A comprehensive phenotypic and genetic analysis of swarming motility. 10.1046/j.1365-2958.2003.03584.x

[12]

Patrick, J. E. & Kearns, D. B. Laboratory strains of Bacillus subtilis do not exhibit swarming motility. J. Bacteriol. 191, 7129–7133 (2009). 10.1128/jb.00905-09

[13]

Swarming Behavior of and Hemolysin BL Secretion by Bacillus cereus

Emilia Ghelardi, Francesco Celandroni, Sara Salvetti et al.

Applied and Environmental Microbiology 2007 10.1128/aem.02345-06

[14]

Kim, W. & Surette, M. G. Prevalence of surface swarming behavior in Salmonella. J. Bacteriol. 187, 6580–6583 (2005). 10.1128/jb.187.18.6580-6583.2005

[15]

Velicer, G. J., Kroos, L. & Lenski, R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376–12380 (1998). 10.1073/pnas.95.21.12376

[16]

Julkowska, D., Obuchowski, M., Holland, B. I. & Séror, S. J. Comparative analysis of the development of swarming communities of Bacillus subtilis 168 and a natural wild type: critical effects of surfactin and the composition of the medium. J. Bacteriol. 187, 65–76 (2005). 10.1128/jb.187.1.65-76.2005

[17]

Young, G. M., Smith, M. J., Minnich, S. A. & Miller, V. L. The Yersinia enterocolitica motility master regulatory operon, flhDC, is required for flagellin production, swimming motility, and swarming motility. J. Bacteriol. 181, 2823–2833 (1999). Another comprehensive phenotypic and genetic analysis of swarming motility. 10.1128/jb.181.9.2823-2833.1999

[18]

Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells.

R M Harshey, T Matsuyama

Proceedings of the National Academy of Sciences 1994 10.1073/pnas.91.18.8631

[19]

Jones, H. E. & Park, R. W. A. The influence of medium composition on the growth and swarming of Proteus. J. Gen. Microbiol. 47, 369–378 (1967). 10.1099/00221287-47-3-369

[20]

Eberl, L., Molin, S. & Givskov, M. Surface motility of Serratia liquefaciens MG1. J. Bacteriol. 181, 1703–1712 (1999). An excellent data-filled review specific to S. liquefaciens swarming that serves as a template that is generally applicable to many systems. 10.1128/jb.181.6.1703-1712.1999

[21]

Tremblay, J. & Déziel, E. Improving the reproducibility of Pseudomonas aeruginosa swarming motility assays. J. Basic Microbiol. 48, 509–515 (2008). 10.1002/jobm.200800030

[22]

Mayfield, C. I. & Inniss, W. E. A rapid, simple method for staining bacterial flagella. Can. J. Microbiol. 23, 1311–1313 (1977). 10.1139/m77-198

[23]

Turner, L., Ryu, W. S. & Berg, H. C. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182, 2793–2801 (2000). The authors devise a simple, rapid and robust means of fluorescently labelling the flagella of Gram-negative bacteria. This work is a great leap forward for the imaging of flagellar dynamics. 10.1128/jb.182.10.2793-2801.2000

[24]

Copeland, M. F., Flickinger, S. T., Tuson, H. H. & Weibel, D. B. Studying the dynamics of flagella in multicellular communities of Escherichia coli by using biarsenical dyes. Appl. Environ. Microbiol. 76, 1241–1250 (2010). An important first effort towards monitoring flagellar dynamics in a swarm. 10.1128/aem.02153-09

[25]

Development of Flagella by Proteus mirabilis

J. F. M. HOENIGER

Journal of General Microbiology 1965 10.1099/00221287-40-1-29

[26]

Ultrastructure of Proteus mirabilis Swarmer Cell Rafts and Role of Swarming in Catheter-Associated Urinary Tract Infection

Brian V. Jones, Robert Young, Eshwar Mahenthiralingam et al.

Infection and Immunity 2004 10.1128/iai.72.7.3941-3950.2004

[27]

Coordinating assembly of a bacterial macromolecular machine

Fabienne F. V. Chevance, Kelly T. Hughes

Nature Reviews Microbiology 2008 10.1038/nrmicro1887

[28]

Shinoda, S. & Okamoto, K. Formation and function of Vibrio parahaemolyticus lateral flagella. J. Bacteriol. 129, 1266–1271 (1977). The first observation that synthesis of lateral flagella is induced in V. parahaemolyticus by contact with a surface. 10.1128/jb.129.3.1266-1271.1977

[29]

Alberti, L. & Harshey, R. M. Differentiation of Serratia marcescens 274 into swimmer and swarmer cells. J. Bacteriol. 172, 4322–4328 (1990). 10.1128/jb.172.8.4322-4328.1990

[30]

Merino, S., Shaw, J. G. & Tomás, J. M. Bacterial lateral flagella: an inducible flagella system. FEMS Microbiol. Lett. 263, 127–135 (2006). 10.1111/j.1574-6968.2006.00403.x

[31]

Ulitzur, S. & Kessel, M. Giant flagellar bundles of Vibrio alginolyticus (NCMB 1803). Arch. Mikrobiol. 94, 331–339 (1973). 10.1007/bf00769028

[32]

Schneider, W. R. & Doetsch, R. N. Effect of viscosity on bacterial motility. J. Bacteriol. 117, 696–701 (1974). 10.1128/jb.117.2.696-701.1974

[33]

Berg, H. C. & Turner, L. Movement of microorganisms in viscous environments. Nature 278, 349–351 (1979). 10.1038/278349a0

[34]

Atsumi, T. et al. Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolyticus. J. Bacteriol. 178, 5024–5026 (1996). 10.1128/jb.178.16.5024-5026.1996

[35]

Zhang, R., Turner, L. & Berg, H. C. The upper surfaces of an Escherichia coli swarm is stationary. Proc. Natl Acad. Sci. USA 107, 288–290 (2010). A simple and fascinating approach to measuring the thickness of the fluid surrounding a swarm, including the unexpected finding that the top surface of the swarm fluid is relatively static. 10.1073/pnas.0912804107

[36]

Darnton, N. C., Turner, L., Rojevsky, S. & Berg, H. C. Dyanmics of bacterial swarming. Biophys. J. 98, 2082–2090 (2010). 10.1016/j.bpj.2010.01.053

[37]

Turner, L., Zhang, R., Darnton, N. C. & Berg, H. C. Visualization of flagella during bacterial swarming. J. Bacteriol. 192, 3259–3267 (2010). An important first effort towards monitoring flagellar dynamics in a swarm. 10.1128/jb.00083-10

[38]

Ragatz, L., Jiang, Z. Y., Bauer, C. & Gest, H. Macroscopic phototactic behavior of the purple photosynthetic bacterium Rhodospirillum centenum. Arch. Microbiol. 163, 1–6 (1995). 10.1007/bf00262196

[39]

Gavín, R. et al. Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43, 383–397 (2002). 10.1046/j.1365-2958.2002.02750.x

[40]

Lateral Flagella and Swarming Motility in Aeromonas Species

Sylvia M. Kirov, Bronwen C. Tassell, Annalese B. T. Semmler et al.

Journal of Bacteriology 2002 10.1128/jb.184.2.547-555.2002

[41]

McCarter, L. L. & Wright, M. E. Identification of genes encoding components of the swarmer cell flagellar motor and propeller and a sigma factor controlling differentiation of Vibrio parahaemolyticus. J. Bacteriol. 175, 3361–3371 (1993). 10.1128/jb.175.11.3361-3371.1993

[42]

Kim, Y. K. & McCarter, L. L. Analysis of the polar flagellar gene system of V. parahaemolyticus. J. Bacteriol. 182, 3693–3704 (2000). 10.1128/jb.182.13.3693-3704.2000

[43]

Doyle, T. B., Hawkins, A. C. & McCarter, L. L. The complex flagellar torque generator of Pseudomonas aeruginosa. J. Bacteriol. 186, 6341–6350 (2004). 10.1128/jb.186.19.6341-6350.2004

[44]

Toutain, C. M., Zegans, M. E., & O'Toole, G. A. Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J. Bacteriol. 187, 771–777 (2005). 10.1128/jb.187.2.771-777.2005

[45]

Senesi, S. et al. Swarming motility in Bacillus cereus and characterization of a fliY mutant impaired in swarm cell differentiation. Microbiology 148, 1785–1794 (2002). 10.1099/00221287-148-6-1785

[46]

A swarming-defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase

Hsin-Chih Lai, Daniel Gygi, Gillian M. Fraser et al.

Microbiology 1998 10.1099/00221287-144-7-1957

[47]

Negative feedback from a Proteus class II flagellum export defect to the flhDC master operon controlling cell division and flagellum assembly

R B Furness, G M Fraser, N A Hay et al.

Journal of Bacteriology 1997 10.1128/jb.179.17.5585-5588.1997

[48]

Köhler, T., Curty, L. K., Barja, F., Van Delden, C. & Pechère, J.C. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182, 5990–5996 (2000). 10.1128/jb.182.21.5990-5996.2000

[49]

Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa

M. Harunur Rashid, Arthur Kornberg

Proceedings of the National Academy of Sciences 2000 10.1073/pnas.060030097

[50]

A nonswarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator

N A Hay, D J Tipper, D Gygi et al.

Journal of Bacteriology 1997 10.1128/jb.179.15.4741-4746.1997

Showing 50 of 137 references

Cited By

1,300

Dual antibacterial action of ethyl ferulate as antibiofilm molecule and antibiotic synergist against Escherichia coli

Zhijin Zhang, Yubin Bai · 2026

Frontiers in Cellular and Infection...

CspA regulates stress resistance, flagellar motility and biofilm formation in Salmonella Enteritidis

Xiang Li, Yan Cui · 2025

Food Bioscience

BfrR-mediated biofilm regulation in the seafood-borne pathogen Vibrio parahaemolyticus

Hui Sun, Miaomiao Zhang · 2025

Food Research International

Minimum sampling density determines soil bacterial diversity through ecosystem multifunctionality in a typical steppe

Xinzhou Zhao, Lan Li · 2025

Journal of Environmental Management

Movement of bacteria in the soil and the rhizosphere

Gladys Alexandre · 2025

Applied and Environmental Microbiol...

The Function of Root Exudates in the Root Colonization by Beneficial Soil Rhizobacteria

Lin Chen, Yunpeng Liu · 2024

Biology

Run-and-tumble kinematics of Enterobacter Sp. SM3

Silverio Johnson, Brian Freedman · 2024

Physical Review E

Root colonization by beneficial rhizobacteria

Yunpeng Liu, Zhihui Xu · 2023

FEMS Microbiology Reviews

Submicron‐Sized In Situ Osmotic Pressure Sensors for In Vitro Applications in Biology

Wenbo Zhang, Luca Bertinetti · 2023

Advanced Healthcare Materials

Bacterial Motility and Its Role in Skin and Wound Infections

Katarzyna Zegadło, Monika Gieroń · 2023

International Journal of Molecular...

Exposure to lysed bacteria can promote or inhibit growth of neighboring live bacteria depending on local abiotic conditions

Fokko Smakman, Alex R Hall · 2022

FEMS Microbiology Ecology

Chemically and Biologically Engineered Bacteria‐Based Delivery Systems for Emerging Diagnosis and Advanced Therapy

Yixin Wang, Jun Liu · 2021

Advanced Materials

Poultry and beef meat as potential seedbeds for antimicrobial resistant enterotoxigenic Bacillus species: a materializing epidemiological and potential severe health hazard

Kamelia M. Osman, Anthony D. Kappell · 2018

Scientific Reports

Helical micropumps near surfaces

Justas Dauparas, Debasish Das · 2018

Biomicrofluidics

The first world swimming championships of roseobacters—Phylogenomic insights into an exceptional motility phenotype

Pascal Bartling, John Vollmers · 2018

Systematic and Applied Microbiology

A structural model of flagellar filament switching across multiple bacterial species

Andrew M. Burrage, Sandra Postel · 2017

Nature Communications

Bacteria exploit a polymorphic instability of the flagellar filament to escape from traps

Marco J. Kühn, Felix K. Schmidt · 2017

Proceedings of the National Academy...

The effects of sodium hypochlorite against selected drinking water-isolated bacteria in planktonic and sessile states

I.B. Gomes, M. Simoes · 2016

Science of The Total Environment

From Cell Differentiation to Cell Collectives: Bacillus subtilis Uses Division of Labor to Migrate

Jordi van Gestel, Hera Vlamakis · 2015

PLOS Biology

Division of Labor in Biofilms: the Ecology of Cell Differentiation

Jordi van Gestel, Hera Vlamakis · 2015

Microbiology Spectrum

Metrics

1,300

Citations

137

References

Details

Published: Aug 09, 2010
Vol/Issue: 8(9)
Pages: 634-644
License: View

Authors

D

Daniel B. Kearns

Cite This Article

Daniel B. Kearns (2010). A field guide to bacterial swarming motility. Nature Reviews Microbiology, 8(9), 634-644. https://doi.org/10.1038/nrmicro2405

A field guide to bacterial swarming motility

You May Also Like