The role of PilU in the surface behaviors of Pseudomonas aeruginosa

Jingchao Zhang , Yan Luo , Yiwu Zong , Shangping Lu , Yi Shi , Fan Jin , Kun Zhao

mLife ›› 2025, Vol. 4 ›› Issue (1) : 83 -95.

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mLife ›› 2025, Vol. 4 ›› Issue (1) : 83 -95. DOI: 10.1002/mlf2.12165
ORIGINAL RESEARCH

The role of PilU in the surface behaviors of Pseudomonas aeruginosa

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Abstract

In Pseudomonas aeruginosa, the dynamic activity of type IV pilus (TFP) is essential for various bacterial behaviors. While PilU is considered a homolog of the TFP disassembling motor PilT, its specific roles remain unclear. Using pilus visualization and single-cell tracking techniques, we characterized TFP dynamics and surface behaviors in wild-type and ΔpilU mutants. We found that ΔpilU cells displayed increased TFP numbers but reduced cell movement and delayed microcolony formation. Interestingly, beyond affecting the twitching motility, ΔpilU cells formed a thick multilayered colony edge on semi-solid surfaces, slowing colony expansion. Cell–cell collision responses changed from touch-turn dominance in wild type to touch-upright dominance in ΔpilU, affecting colony morphology and expansion. These findings expand our understanding of PilU’s physiological roles and provide potential targets for developing strategies to control P. aeruginosa biofilm formation and virulence.

Keywords

colony expansion / pilU / Pseudomonas aeruginosa / twitching / type IV pili

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Jingchao Zhang, Yan Luo, Yiwu Zong, Shangping Lu, Yi Shi, Fan Jin, Kun Zhao. The role of PilU in the surface behaviors of Pseudomonas aeruginosa. mLife, 2025, 4(1): 83-95 DOI:10.1002/mlf2.12165

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References

[1]

Ellison CK, Whitfield GB, Brun YV. Type IV Pili: dynamic bacterial nanomachines. FEMS Microbiol Rev. 2022; 46: fuab053.

[2]

Gibiansky ML, Conrad JC, Jin F, Gordon VD, Motto DA, Mathewson MA, et al. Bacteria use type IV pili to walk upright and detach from surfaces. Science. 2010; 330:197.

[3]

Wall D, Kaiser D. Type IV pili and cell motility. Mol Microbiol. 1999; 32:01–10.

[4]

Merz AJ, So M, Sheetz MP. Pilus retraction powers bacterial twitching motility. Nature. 2000; 407:98–102.

[5]

Skerker JM, Berg HC. Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci USA. 2001; 98:6901–6904.

[6]

Eriksson J, Eriksson OS, Maudsdotter L, Palm O, Engman J, Sarkissian T, et al. Characterization of motility and piliation in pathogenic Neisseria. BMC Microbiol. 2015; 15:92.

[7]

Nakane D, Nishizaka T. Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria. Proc Natl Acad Sci USA. 2017; 114:6593–6598.

[8]

Mahmoud KK, Koval SF. Characterization of type IV pili in the life cycle of the predator bacterium Bdellovibrio. Microbiology. 2010; 156:1040–1051.

[9]

Utada AS, Bennett RR, Fong JCN, Gibiansky ML, Yildiz FH, Golestanian R, et al. Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment. Nat Commun. 2014; 5:4913.

[10]

Siryaporn A, Kuchma SL, O’Toole GA, Gitai Z. Surface attachment induces Pseudomonas aeruginosa virulence. Proc Natl Acad Sci USA. 2014; 111:16860–16865.

[11]

Persat A, Inclan YF, Engel JN, Stone HA, Gitai Z. Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 2015; 112:7563–7568.

[12]

Ellison CK, Kan J, Dillard RS, Kysela DT, Ducret A, Berne C, et al. Obstruction of pilus retraction stimulates bacterial surface sensing. Science. 2017; 358:535–538.

[13]

Kühn MJ, Talà L, Inclan YF, Patino R, Pierrat X, Vos I, et al. Mechanotaxis directs Pseudomonas aeruginosa twitching motility. Proc Natl Acad Sci USA. 2021; 118:e2101759118.

[14]

Del Medico L, Cerletti D, Schächle P, Christen M, Christen B. The type IV pilin PilA couples surface attachment and cell cycle initiation in Caulobacter crescentus. Proc Natl Acad Sci USA. 2020; 117:9546–9553.

[15]

Snyder RA, Ellison CK, Severin GB, Whitfield GB, Waters CM, Brun YV. Surface sensing stimulates cellular differentiation in Caulobacter crescentus. Proc Natl Acad Sci USA. 2020; 117:17984–17991.

[16]

Pelicic V. Type IV pili: e pluribus unum? Mol Microbiol. 2008; 68:827–837.

[17]

Jacobsen T, Bardiaux B, Francetic O, Izadi-Pruneyre N, Nilges M. Structure and function of minor pilins of type IV pili. Med Microbiol Immunol. 2020; 209:301–308.

[18]

Giltner CL, Habash M, Burrows LL. Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol. 2010; 398:444–461.

[19]

Satyshur KA, Worzalla GA, Meyer LS, Heiniger EK, Aukema KG, Misic AM, et al. Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility. Structure. 2007; 15:363–376.

[20]

Mccallum M, Tammam S, Khan A, Burrows LL, Howell PL. The molecular mechanism of the type IVa pilus motor. Nat Commun. 2017; 8:15091.

[21]

Bischof LF, Friedrich C, Harms A, Søgaard-Andersen L, van der Does C. The type IV pilus assembly ATPase PilB of Myxococcus xanthus interacts with the inner membrane platform protein PilC and the nucleotide-binding protein PilM. J Biol Chem. 2016; 291:6946–6957.

[22]

Chlebek JL, Hughes HQ, Ratkiewicz AS, Rayyan R, Wang JCY, Herrin BE, et al. PilT and PilU are homohexameric ATPases that coordinate to retract type IVa pili. PLoS Genet. 2019; 15:e1008448.

[23]

Whitchurch CB, Mattick JS. Characterization of a gene, pilU, required for twitching motility but not phage sensitivity in Pseudomonas aeruginosa. Mol Microbiol. 1994; 13:1079–1091.

[24]

Han X, Kennan RM, Davies JK, Reddacliff LA, Dhungyel OP, Whittington RJ, et al. Twitching motility is essential for virulence in Dichelobacter nodosus. J Bacteriol. 2008; 190:3323–3335.

[25]

Park H-SM, Wolfgang M, Koomey M. Modification of type IV pilus-associated epithelial cell adherence and multicellular behavior by the PilU protein of Neisseria gonorrhoeae. Infect Immun. 2002; 70:3891–3903.

[26]

Adams DW, Pereira JM, Stoudmann C, Stutzmann S, Blokesch M. The type IV pilus protein PilU functions as a PilT-dependent retraction ATPase. PLoS Genet. 2019; 15:e1008393.

[27]

Talà L, Fineberg A, Kukura P, Persat A. Pseudomonas aeruginosa orchestrates twitching motility by sequential control of type IV pili movements. Nat Microbiol. 2019; 4:774–780.

[28]

Li Y, Huang S, Zhang X, Huang T, Li H. Cloning, expression, and functional analysis of molecular motor pilT and pilU genes of type IV pili in Acidithiobacillus ferrooxidans. Appl Microbiol Biotechnol. 2013; 97:1251–1257.

[29]

Seitz P, Blokesch M. DNA-uptake machinery of naturally competent Vibrio cholerae. Proc Natl Acad Sci USA. 2013; 110:17987–17992.

[30]

Imhaus AF, Duménil G. The number of Neisseria meningitidis type IV pili determines host cell interaction. EMBO J. 2014; 33:1767–1783.

[31]

Angelov A, Bergen P, Nadler F, Hornburg P, Lichev A, Übelacker M, et al. Novel Flp pilus biogenesis-dependent natural transformation. Front Microbiol. 2015; 6:84.

[32]

Zhang J, Li S, Sun T, Zong Y, Zhang W, Zhao K. A simple, switchable pili-labelling method by plasmid-based replacement of pilin. Environ Microbiol. 2021; 23:2692–2703.

[33]

Zhang J, He J, Zhai C, Ma LZ, Gu L, Zhao K. Effects of PslG on the surface movement of Pseudomonas aeruginosa. Appl Environ Microbiol. 2018; 84:e00219-18.

[34]

O’Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol. 2000; 54:49–79.

[35]

Roberts MAJ, Papachristodoulou A, Armitage JP. Adaptation and control circuits in bacterial chemotaxis. Biochem Soc Trans. 2010; 38:1265–1269.

[36]

Zhao K, Tseng BS, Beckerman B, Jin F, Gibiansky ML, Harrison JJ, et al. Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature. 2013; 497:388–391.

[37]

Zhang R, Ni L, Jin Z, Li J, Jin F. Bacteria slingshot more on soft surfaces. Nat Commun. 2014; 5:5541.

[38]

Song F, Brasch ME, Wang H, Henderson JH, Sauer K, Ren D. How bacteria respond to material stiffness during attachment: a role of Escherichia coli flagellar motility. ACS Appl Mater Interfaces. 2017; 9:22176–22184.

[39]

Anyan ME, Amiri A, Harvey CW, Tierra G, Morales-Soto N, Driscoll CM, et al. Type IV pili interactions promote intercellular association and moderate swarming of Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 2014; 111:18013–18018.

[40]

Klausen M, Aaes-Jørgensen A, Molin S, Tolker-Nielsen T. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol. 2003; 50:61–68.

[41]

Eriksson J, Eriksson OS, Jonsson A-B. Loss of meningococcal PilU delays microcolony formation and attenuates virulence in vivo. Infect Immun. 2012; 80:2538–2547.

[42]

Zhang J, Li S, Sun T, Zong Y, Luo Y, Wei Y, et al. Oscillation of type IV pili regulated by the circadian clock in cyanobacterium Synechococcus elongatus PCC7942. Sci Adv. 2024; 10:eadd9485.

[43]

Chiang P, Habash M, Burrows LL. Disparate subcellular localization patterns of Pseudomonas aeruginosa type IV pilus ATPases involved in twitching motility. J Bacteriol. 2005; 187:829–839.

[44]

Kühn MJ, Macmillan H, Talà L, Inclan Y, Patino R, Pierrat X, et al. Two antagonistic response regulators control Pseudomonas aeruginosa polarization during mechanotaxis. EMBO J. 2023; 42:e112165.

[45]

Zheng X, Gomez-Rivas EJ, Lamont SI, Daneshjoo K, Shieh A, Wozniak DJ, et al. The surface interface and swimming motility influence surface-sensing responses in Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 2024; 121:e2411981121.

[46]

Leong CG, Bloomfield RA, Boyd CA, Dornbusch AJ, Lieber L, Liu F, et al. The role of core and accessory type IV pilus genes in natural transformation and twitching motility in the bacterium Acinetobacter baylyi. PLoS One. 2017; 12:e0182139.

[47]

Taylor RG, Welch RD. Recording multicellular behavior in Myxococcus xanthus biofilms using time-lapse microcinematography. J Vis Exp. 2010; 6:2038.

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2025 The Author(s). mLife published by John Wiley & Sons Australia, Ltd on behalf of Institute of Microbiology, Chinese Academy of Sciences.

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