Swarming motility in plant-associated bacteria

Open access


Plant-associated environments harbor a huge number of diverse bacteria that compete and/or cooperate for the occupation of the most nutrient-rich ecological niches. Motility, a common trait among bacteria, has long been assumed to provide a survival advantage to skilful bacteria in invading these environments. Bacterial surface motility, such as swarming, a flagella-driven type of surface movement, although mostly observed and studied on agar substrates, is emerging as a major trait involved in many functions of plant-associated bacteria in regard to their ability to colonize and spread on their host. In this review, we address some novel swarming motility strategies, which enable bacteria to colonize, disperse and compete in plant surfaces.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Alteri C.J. Himpsl S.D. Pickens S.R. Lindner J.R Zora J.S. Miller J.E Arno P.D. Straight S.W. and Mobley H.L. 2013. Multicellular bacteria deploy the type VI secretion system to preemptively strike neighboring cells. PLoS Pathogens 9(9): e1003608

  • Banitz T. Johst K. Wick L.Y. Schamfuß S. Harms H. and Frank K. 2013. Highways versus pipelines: contributions of two fungal transport mechanisms to efficient bioremediation. Environmental Microbiology Reports 5: 211–8.

  • Barak J.D. Gorski L. Liang A.S. and Narm K-E. 2009. Previously uncharacterized Salmonella enteric genes required for swarming play a role in seedling colonization. Microbiology 15: 3701-3709.

  • Be’er A. Ariel G. Kalisman O. Helman Y. Sirota-Madi A. Zhang H.P. Florin E-L. Payne S.M. Ben-Jacob E. and Swinney H. L. 2010. Lethal protein produced in response to competition between sibling bacterial colonies. Proceedings of the National Academy of Sciences of the United States of America 107(14): 6258–6263.

  • Be’er A. Zhang H.P. Florin E.L. Payne S.M. Ben-Jacob E. and Swinney H.L. 2009. Deadly competition between sibling bacterial colonies. Proceedings of the National Academy of Sciences of the United States of America 106: 428–433.

  • Berg G. Rybakovam D. Grube M. and Köberl M. 2015. The plant microbiome explored: implications for experimental botany. Journal of Experimental Botany doi: 10.1093/jxb/erv466

  • Bitas V. Kim H-S. Joan W. Bennett J.W. and Kang S. 2013. Sniffing on microbes: Diverse roles of microbial volatile organic compounds in plant health. Molecular Plant-Microbe Interactions 26: 835–843

  • Bravo D. Cailleau G. Bindschedler S. Simon A. Job D. Verrecchia E. and Junier P. 2013. Isolation of oxalotrophic bacteria able to disperse on fungal mycelium. FEMS Microbiology Letters 348: 157–66.

  • Chernin L. Toklikishvili N. Ovadis M. Kim S. Ben-Ari J. Khmel I. and Vainstein A. 2011. Quorum-sensing quenching by rhizobacterial volatiles. Environmental Microbiology Reports 3: 698–704.

  • Compant S. Duffy B. Nowak J. Clément C. and Barka E.A. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles mechanisms of action and future prospects. Applied and Environmental Microbiology 71: 4951–4959.

  • Covelli J.M. Althabegoiti M.J López M.F. and Lodeiro A.R. 2013. Swarming motility in Bradyrhizobium japonicum. Research in Microbiology 164: 136-44.

  • Daniels R. Vanderleyden J. and Michiels J. 2004. Quorum sensing and swarming migration in bacteria. FEMS Microbiol Reviews 28(3): 261–89.

  • de Boer W. Hundscheid M.P.J. Gunnewiek K. P.J.A. de Ridder-Duine A.S. Thion C. van Veen J.A. and van der Wal A. 2015. Antifungal Rhizosphere Bacteria can increase as Response to the Presence of Saprotrophic Fungi. PLoS ONE 10(9): e0137988.

  • Decoin V. Barbey C. Bergeau D. Latour X. Feuilloley M.G. Orange N. and Merieau A. 2014. A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS ONE 9(2): e89411.

  • Decoin V Gallique M Barbey C LeMauff F Duclairoir Poc C Feuilloley M.G.J. Orange N. and Merieau A. 2015. A Pseudomonas fluorescens type 6 secretion system is related to mucoidy motility and bacterial competition. BMC Microbiology 15: 72.

  • Dulla G. and Lindow S. 2009. Acyl-homoserine lactone mediated cross talk among epiphytic bacteria modulates behavior of Pseudomonas syringae on leaves. The ISME Journal 3: 825–834.

  • Finkelshtein A. Roth D. Ben Jacob E. and Ingham C.J. 2015. Bacterial swarms recruit cargo bacteria to pave the way in toxic environments. mBio 6(3): e00074-15.

  • Fouhy Y. Scanlon K. Schouest K. Spillane C. Crossman L. Avison M.B. Ryan R.P. and Dow J.M. 2007. Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia. Journal of Bacteriology 189: 4964–4968.

  • Furuno S. Remer R. Chatzinotas A. Harms H. and Wick L.Y. 2012. Use of mycelia as paths for the isolation of contaminant-degrading bacteria from soil. Microbial Biotechnology 5(1): 142-8.

  • Gantner S. Schmid M. Durr C. Schuhegger R. Steidle A. Hutzler P. Langebartels C Eberl L. Hartmann A. Dazzo F.B.. 2006. In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiology Ecology 56: 188–194.

  • Garbeva P. Hordijk C. Gerards S. and De Boer W. 2014. Volatile-mediated interactions between phylogenetically different soil bacteria. Frontiers in Microbiology 5: 285–290.

  • Georgakopoulos D.G. Fiddaman P. Leifert C. and Malathrakis N.E. 2002. Biological control of cucumber and sugar beet damping-off caused by Pythium ultimum with bacterial and fungal antagonists. Journal of Applied Microbiology 92: 1078–86.

  • Gibbs K.A. Urbanowski M.L. and Greenberg E.P. 2008. Genetic determinants of self-identity and social recognition in bacteria. Science 321(5886): 256–259.

  • Haapalainen M. Mosorin H. Dorati F. Wu R.F. Roine E. Taira S. Nissinen R. Mattinen L. Jackson R. Pirhonen M. and Lin N.C. 2012. Hcp2 a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000 is required for fitness for competition against bacteria and yeasts. Journal of Bacteriology 194: 4810–4822.

  • Haefele D.M. and Lindow S.E. 1987. Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Journal of Applied Microbiology 53: 2528–2533.

  • Hagai E. Dvora R. Havkin-Blank T. Zelinger E. Porat Z. Schulz S. and Helman Y. 2014. Surface-motility induction attraction and hitchhiking between bacterial species promote dispersal on solid surfaces. The ISME Journal 8: 1147–1151.

  • Hannula S.E de Boer W. and van Veen J.A. 2010. In situ dynamics of soil fungal communities under different genotypes of potato including a genetically modified cultivar. Soil Biology & Biochemistry 42: 2211–2223.

  • Harshey R.M. 2003. Bacterial motility on a surface: Many ways to a common goal. Annual Review of Microbiology 57: 249–273.

  • Harshey R.M. and Partridge J.D. 2015. Shelter in a Swarm. Journal of Molecular Biology 427(23): 3683-94.

  • Ingham C.J. Kalisman O. Finkelshtein A. and Ben-Jacob E. 2011. Mutually facilitated dispersal between the nonmotile fungus Aspergillus fumigates and the swarming bacterium P. vortex. Proceedings of the National Academy of Sciences of the United States of America 108: 19731–19736.

  • Jarrell K.F. and McBride M.J. 2008. The surprisingly diverse ways that prokaryotes move. Nature Reviews Microbiology 6: 466–476.

  • Kearns D.B. 2010. A field guide to bacterial swarming motility. Nature Reviews Microbiology 8: 634–644.

  • Kim K-S. Lee S. and Ryu C-M. 2013. Interspecific bacterial sensing through airborne signals modulates locomotion and drug resistance. Nature Communications 4: 1809-1815.

  • Kohlmeier S. Smits T.H.M. Ford R.M. Keel C. Harms H. and Wick L.Y. 2005. Taking the fungal highway: mobilization of pollutantdegrading bacteria by fungi. Environmental Science and Technology 39: 4640–46.

  • Kraemer S.A. and Velicer G.J. 2014. Social complementation and growth advantages promote socially defective bacterial isolates. Proceeding of the Royal Society B 281: 20140036.

  • Kremmydas G. F. Tampakaki A. P. and Georgakopoulos D. G. 2013. Characterization of the biocontrol activity of Pseudomonas fluorescens strain X reveals novel genes regulated by glucose. PLoS ONE 8(4): e61808.

  • Lee K. Kobayashi N. Watanabe M. Sugita-Konishi Y. Tsubone H. Kumagai S. and Hara-Kudo Y. 2014. Spread and change in stress resistance of Shiga toxin-producing Escherichia coli O157 on fungal colonies. Microbial Biotechnology 7: 621–629.

  • Loper J.E. Hassan K.A. Mavrodi D.V. et al. 2012. Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genetics 8(7): e1002784.

  • Ma L.S. Hachani A. Lin J.S. Filloux A. and Lai E.M. 2014. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host and Microbe 16: 94–104.

  • Mattinen L. Somervuo P. Nykyri P. Nissinen R. Kouvonen P. Corthals G. Auvinen P. Aittamaa M. Valkonen J.P.T. and Pirhonen M. 2008. Microarray profiling of host-extract induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum. Microbiology 154: 2387–2396.

  • McAlester G. O’Gara F. and Morrissey J.P. 2008. Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans. Journal of Medical Microbiology 57: 563–569.

  • Mendes R. Garbeva P. and Raaijmakers J.M. 2013. The rhizosphere microbiome: significance of plant beneficial plant pathogenic and human pathogenic microorganisms. FEMS Microbiology Reviews 37: 634-63.

  • Morello J.E. Pierson E.A. and Pierson L.S. 2004. Negative cross-communication among wheat rhizosphere bacteria: effect on antibiotic production by the biological control bacterium Pseudomonas aureofaciens 30–84. Applied and Environmental Microbiology 70: 3103–3109.

  • Narisawa N. Haruta S. Arai H. Ishii M. and Igarashi Y. 2008. Coexistence of antibiotic-producing and antibiotic sensitive bacteria in biofilms is mediated by resistant bacteria. Applied and Environmental Microbiology 74: 3887–3894.

  • Ngamdee W Tandhavanant S Wikraiphat C Ream-tong O Wuthiekanun V Salje J Low D.A. Peacock S.J. and Chantratita N. 2015. Competition between Burkholderia pseudomallei and B. thai-landensis. BMC Microbiology 15: 56-52.

  • Nazir R Warmink J.A. Boersma H. and van Elsas J.D. 2010. Mechanisms that promote bacterial fitness in fungal-affected soil microhabitats. FEMS Microbiology Ecology 71(2): 169-85.

  • Nelson E.B. 2004. Microbial dynamics and interactions in the spermosphere. Annual Review of Phytopathology 42: 271–309.

  • Park S. 2003. Influence of topology on bacterial social interaction. Proceedings of the National Academy of Sciences of the United States of America 24: 13910–13915.

  • Partridge J.D. and Harshey R.M. 2013. Swarming: Flexible roaming plans. Journal of Bacteriology 195: 909–918.

  • Piechulla B. and Degenhardt J. 2014. The emerging importance of microbial volatile organic compounds. Plant Cell and Environment 37: 811–812.

  • Pion M. Bshary R. Bindschedler S. Filippidou S. Wick L.Y. Job D. and Junier P. 2013. Gains of bacterial flagellar motility in a fungal world. Applied and Environmental Microbiology 79: 6862–6867.

  • Quinones B. Dulla G. and Lindow S.E. 2005. Quorum sensing regulates exopolysaccharide production motility and virulence in Pseudomonas syringae. Molecular Plant-Microbe Interactions 18: 682–693.

  • Quinones B. Pujol C.J. and Lindow S.E. 2004. Regulation of AHL production and its contribution to epiphytic fitness in Pseudomonas syringae. Mol Molecular Plant-Microbe Interactions 17: 521–531.

  • Rajput A. Kaur K. and Kumar M. 2015. SigMol: repertoire of quorum sensing signaling molecules in prokaryotes. Nucleic Acids Research 1: doi: 10.1093/nar/gkv1076.

  • Rendueles O. Zee P.C. Dinkelacker I. Amherd M. Wielgoss S. and Velicer G.J. 2015. Rapid and widespread de novo evolution of kin discrimination. Proceedings of the National Academy of Sciences of the United States of America 112(29): 9076–9081.

  • Reichenbach T. Mobilia M. and Frey E. 2007. Mobility promotes and jeopardizes biodiversity in rock-paper scissors games. Nature 448:1046–1049.

  • Sarris P.F. Trantas E.A. Baltrus D.A. Bull C.T. Wechter W.P. Yan S. Ververidis F. Almeida N.F. Jones C.D. Dangl J.L Panopoulos N.J Vinatzer B.A. and Goumas D.E. 2013. Comparative Genomics of Multiple Strains of Pseudomonas cannabina pv. alisalensis a Potential Model Pathogen of Both Monocots and Dicots. PLoS ONE 8(3): e59366.

  • Sarris P.F. Trantas E.A. Skandalis N. Tampakaki A.P. Kapanidou M. Kokkinidis M. and Panopoulos N.J. 2011. Phytobacterial Type VI Secretion System: Gene Distribution Phylogeny Structure and Biological Functions. 53-84 pp. In: Plant Pathology C.J. R. Cumagan (ed). InTech - Open Access Publisher. ISBN: 978-953-307-933-2. Croatia

  • Simon A. Bindschedler S. Job D. Wick L.Y. Filippidou S. Kooli W.M. Verrecchia E.P. and Junier P. 2015. Exploiting the fungal highway: development of a novel tool for the in situ isolation of bacteria migrating along fungal mycelium. FEMS Microbiology Ecology 91: 1-13.

  • Stefanic P. Kraighera B. Lyonsb N.A. Kolter R. and Mandic-Mulec I. 2014. Kin discrimination between sympatric Bacillus subtilis isolates. Proceedings of the National Academy of Sciences of the United States of America 112(45): 14042-7

  • Schmint R. Cordovez V. deBoer W. and Raaijmamakers L. 2015. Volatille affairs in microbial interactions. The ISME Journal 9(11): 2329-35.

  • Yu X. Lund S.P. Greenwald J.W. Angela H. Records A.H. Scott R.A. Nettleton D. Lindow S.E. Gross D.C. and Beattie G.A. 2013. Transcriptional Analysis of the Global Regulatory Networks Active in Pseudomonas syringae during Leaf Colonization. mBio 5(5): e01683-14.

  • Venturi V. Bertani I. Kerenyi A. Netotea S. and Pongor S. 2010. Co-Swarming and Local Collapse: Quorum Sensing Conveys Resilience to Bacterial Communities by Localizing Cheater Mutants in Pseudomonas aeruginosa. PLoS ONE 5(4): e9998.

  • Vos M. and Velicer G.J. 2009. Social conflict in centimeter- and global-scale populations of the bacterium Myxococcus xanthus. Current Biology 19(20): 1763–1767.

  • Warmink J.A. and van Elsas J.D. 2009. Migratory response of soil bacteria to Lyophyllum sp. strain Karsten in soil microcosms. Applied and Environmental Microbiology 75(9): 2820-2830.

  • Warmink J.A. Nazir R. Corten B. and van Elsas J.D. 2011. Hitchhikers on the fungal highway: the helper effect for bacterial migration via fungal hyphae. Soil Biology & Biochemistry 43:760–765.

  • Wenren L.M. Sullivan N.L. Cardarelli L. Septer A.N. and Gibbs K.A. 2013. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. mBio 4(4): e00374-13.

  • Whitney J.C. Chou S. Russell A.B. Biboy J. Gardiner T.E. Ferrin M.A. Brittnacher M. Vollmer W. and Mougous J.D. 2013. Identification structure and function of a novel type VIsecretion peptidoglycan glycoside hydrolase effector-immunity pair. Journal of Biological Chemistry 288: 26616–26624.

  • Wösten HAB 2001. Hydrophobins: multipurpose proteins. Annual Review of Microbiology 55: 625–46.

  • Xu J. Plat T.G. Fuqua C. 2012. Regulatory Linkages between Flagella and Surfactant during Swarming Behavior: Lubricating the Flagellar Propeller? Journal of Bacteriology 194: 1283-86.

  • Zhu B. He Liu H. Tian W.X. Fan X.Y. Bin Li B. Zhou X.P. Jin G.L. and Xie G.L. 2012. Genome sequence of Stenotrophomonas maltophilia RR-10 isolated as an endophyte from rice root. Journal of Bacteriology 194: 1280-1.

Journal information
Cited By
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 367 188 10
PDF Downloads 163 104 2