The accumulation and growth of Pseudomonas aeruginosa on surfaces is modulated by surface mechanics via cyclic-di-GMP signaling.


Journal

NPJ biofilms and microbiomes
ISSN: 2055-5008
Titre abrégé: NPJ Biofilms Microbiomes
Pays: United States
ID NLM: 101666944

Informations de publication

Date de publication:
10 Oct 2023
Historique:
received: 31 05 2023
accepted: 12 09 2023
medline: 1 11 2023
pubmed: 11 10 2023
entrez: 10 10 2023
Statut: epublish

Résumé

Attachment of bacteria onto a surface, consequent signaling, and accumulation and growth of the surface-bound bacterial population are key initial steps in the formation of pathogenic biofilms. While recent reports have hinted that surface mechanics may affect the accumulation of bacteria on that surface, the processes that underlie bacterial perception of surface mechanics and modulation of accumulation in response to surface mechanics remain largely unknown. We use thin and thick hydrogels coated on glass to create composite materials with different mechanics (higher elasticity for thin composites; lower elasticity for thick composites) but with the same surface adhesivity and chemistry. The mechanical cue stemming from surface mechanics is elucidated using experiments with the opportunistic human pathogen Pseudomonas aeruginosa combined with finite-element modeling. Adhesion to thin composites results in greater changes in mechanical stress and strain in the bacterial envelope than does adhesion to thick composites with identical surface chemistry. Using quantitative microscopy, we find that adhesion to thin composites also results in higher cyclic-di-GMP levels, which in turn result in lower motility and less detachment, and thus greater accumulation of bacteria on the surface than does adhesion to thick composites. Mechanics-dependent c-di-GMP production is mediated by the cell-surface-exposed protein PilY1. The biofilm lag phase, which is longer for bacterial populations on thin composites than on thick composites, is also mediated by PilY1. This study shows clear evidence that bacteria actively regulate differential accumulation on surfaces of different stiffnesses via perceiving varied mechanical stress and strain upon surface engagement.

Identifiants

pubmed: 37816780
doi: 10.1038/s41522-023-00436-x
pii: 10.1038/s41522-023-00436-x
pmc: PMC10564899
doi:

Substances chimiques

bis(3',5')-cyclic diguanylic acid 61093-23-0
Cyclic GMP H2D2X058MU

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

78

Subventions

Organisme : NIAID NIH HHS
ID : R37 AI083256
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI121500
Pays : United States

Commentaires et corrections

Type : UpdateOf

Informations de copyright

© 2023. Springer Nature Limited.

Références

Cheng, B. et al. Cellular mechanosensing of the biophysical microenvironment: a review of mathematical models of biophysical regulation of cell responses. Phys. Life Rev. 22, 88–119 (2017).
pubmed: 28688729
Iskratsch, T., Wolfenson, H. & Sheetz, M. P. Appreciating force and shape—the rise of mechanotransduction in cell biology. Nat. Rev. Mol. Cell Biol. 15, 825–833 (2014).
pubmed: 25355507 pmcid: 9339222
Persat, A. Bacterial mechanotransduction. Curr. Opin. Microbiol. 36, 1–6 (2017).
pubmed: 28068612
Gordon, V. D. & Wang, L. Bacterial mechanosensing: the force will be with you, always. J. Cell Sci. 132, jcs227694 (2019).
pubmed: 30944157 pmcid: 6467485
Dufrêne, Y. F. & Persat, A. Mechanomicrobiology: how bacteria sense and respond to forces. Nat. Rev. Microbiol.18, 1–14 (2020).
Ellison, C. K. et al. Obstruction of pilus retraction stimulates bacterial surface sensing. Science 358, 535–538 (2017).
pubmed: 29074778 pmcid: 5805138
Hug, I., Deshpande, S., Sprecher, K. S., Pfohl, T. & Jenal, U. Second messenger–mediated tactile response by a bacterial rotary motor. Science 358, 531–534 (2017).
pubmed: 29074777
Persat, A., Inclan, Y. F., Engel, J. N., Stone, H. A. & Gitai, Z. Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 112, 7563–7568 (2015).
pubmed: 26041805 pmcid: 4475988
Luo, Y. et al. A hierarchical cascade of second messengers regulates Pseudomonas aeruginosa surface behaviors. mBio 6, e02456–02414 (2015).
pubmed: 25626906 pmcid: 4324313
Siryaporn, A., Kuchma, S. L., O’Toole, G. A. & Gitai, Z. Surface attachment induces Pseudomonas aeruginosa virulence. Proc. Natl Acad. Sci. USA 111, 16860–16865 (2014).
pubmed: 25385640 pmcid: 4250119
Talà, L., Fineberg, A., Kukura, P. & Persat, A. Pseudomonas aeruginosa orchestrates twitching motility by sequential control of type IV pili movements. Nat. Microbiol. 4, 774–780 (2019).
pubmed: 30804544
O’Neal, L. et al. The Wsp system of Pseudomonas aeruginosa links surface sensing and cell envelope stress. Proc. Natl Acad. Sci. USA 119, e2117633119 (2022).
pubmed: 35476526 pmcid: 9170161
Rodesney, C. A. et al. Mechanosensing of shear by Pseudomonas aeruginosa leads to increased levels of the cyclic-di-GMP signal initiating biofilm development. Proc. Natl Acad. Sci. USA 114, 5906–5911 (2017).
pubmed: 28533383 pmcid: 5468607
Sanfilippo, J. E. et al. Microfluidic-based transcriptomics reveal force-independent bacterial rheosensing. Nat. Microbiol. 4, 1274–1281 (2019).
pubmed: 31086313 pmcid: 6656604
Nguyen, Y. et al. Pseudomonas aeruginosa minor pilins prime type IVa pilus assembly and promote surface display of the PilY1 adhesin. J. Biol. Chem. 290, 601–611 (2015).
pubmed: 25389296
Guimarães, C. F., Gasperini, L., Marques, A. P. & Reis, R. L. The stiffness of living tissues and its implications for tissue engineering. Nat. Rev. Mater. 1–20 (2020).
Wang, Y. et al. Interactions of Staphylococcus aureus with ultrasoft hydrogel biomaterials. Biomaterials 95, 74–85 (2016).
pubmed: 27131630
Campoccia, D., Montanaro, L. & Arciola, C. R. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 27, 2331–2339 (2006).
pubmed: 16364434
Funt, D. & Pavicic, T. Dermal fillers in aesthetics: an overview of adverse events and treatment approaches. Clin. Cosmet. Investig. Dermatol. 6, 295 (2013).
pubmed: 24363560 pmcid: 3865975
Wald, H. L. & Kramer, A. M. Nonpayment for harms resulting from medical care: catheter-associated urinary tract infections. Jama 298, 2782–2784 (2007).
pubmed: 18165672
Koch, M. D., Black, M. E., Han, E., Shaevitz, J. W. & Gitai, Z. Pseudomonas aeruginosa distinguishes surfaces by stiffness using retraction of type IV pili. Proc. Natl Acad. Sci. USA 119, e2119434119 (2022).
pmcid: 9171759
Cont, A., Vermeil, J. & Persat, A. Material Substrate Physical Properties Control Pseudomonas aeruginosa Biofilm Architecture. mBio 14, e03518–e03522 (2023).
Bayoudh, S. et al. Quantification of the adhesion free energy between bacteria and hydrophobic and hydrophilic substrata. Mater. Sci. Eng. C. 26, 300–305 (2006).
Bruinsma, G., Van der Mei, H. & Busscher, H. Bacterial adhesion to surface hydrophilic and hydrophobic contact lenses. Biomaterials 22, 3217–3224 (2001).
pubmed: 11700793
Yang, K. et al. Bacterial anti-adhesion surface design: Surface patterning, roughness and wettability: A review. J. Mater. Sci. Technol. 99, 82–100 (2022).
Yuan, Y., Hays, M. P., Hardwidge, P. R. & Kim, J. Surface characteristics influencing bacterial adhesion to polymeric substrates. RSC Adv. 7, 14254–14261 (2017).
Wang, Y., Lee, S. M. & Dykes, G. The physicochemical process of bacterial attachment to abiotic surfaces: Challenges for mechanistic studies, predictability and the development of control strategies. Crit. Rev. Microbiol. 41, 452–464 (2015).
pubmed: 24635643
Cheng, Y., Feng, G. & Moraru, C. I. Micro-and nanotopography sensitive bacterial attachment mechanisms: a review. Front. Microbiol. 10, 191 (2019).
pubmed: 30846973 pmcid: 6393346
Vadillo-Rodriguez, V., Busscher, H. J., van der Mei, H. C., de Vries, J. & Norde, W. Role of lactobacillus cell surface hydrophobicity as probed by AFM in adhesion to surfaces at low and high ionic strength. Colloids Surf. B: Biointerf. 41, 33–41 (2005).
Zhang, X. et al. Interpretation of adhesion behaviors between bacteria and modified basalt fiber by surface thermodynamics and extended DLVO theory. Colloids Surf. B: Biointerf. 177, 454–461 (2019).
Carniello, V., Peterson, B. W., van der Mei, H. C. & Busscher, H. J. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Adv. Colloid Interf. Sci. 261, 1–14 (2018).
Kolewe, K. W., Peyton, S. R. & Schiffman, J. D. Fewer bacteria adhere to softer hydrogels. ACS Appl. Mater. Interf. 7, 19562–19569 (2015).
Peng, Q. et al. Three-dimensional bacterial motions near a surface investigated by digital holographic microscopy: effect of surface stiffness. Langmuir 35, 12257–12263 (2019).
pubmed: 31423792
Kolewe, K. W., Zhu, J., Mako, N. R., Nonnenmann, S. S. & Schiffman, J. D. Bacterial adhesion is affected by the thickness and stiffness of poly (ethylene glycol) hydrogels. ACS Appl. Mater. Interf. 10, 2275–2281 (2018).
Song, F. et al. How bacteria respond to material stiffness during attachment: a role of Escherichia coli flagellar motility. ACS Appl. Mater. Interf. 9, 22176–22184 (2017).
Straub, H. et al. Bacterial Adhesion on Soft Materials: Passive Physicochemical Interactions or Active Bacterial Mechanosensing? Adv. Healthc. Mater. 8, 1801323 (2019).
Carniello, V., Peterson, B. W., Sjollema, J., Busscher, H. J. & van der Mei, H. C. Surface enhanced fluorescence and nanoscopic cell wall deformation in adhering Staphylococcus aureus upon exposure to cell wall active and non-active antibiotics. Nanoscale 10, 11123–11133 (2018).
pubmed: 29873372
Otto, K. & Silhavy, T. J. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl Acad. Sci. USA 99, 2287–2292 (2002).
pubmed: 11830644 pmcid: 122357
Shimizu, T., Ichimura, K. & Noda, M. The surface sensor NlpE of enterohemorrhagic Escherichia coli contributes to regulation of the type III secretion system and flagella by the Cpx response to adhesion. Infect. Immun. 84, 537–549 (2016).
pubmed: 26644384 pmcid: 4730559
Booth, I. R. Bacterial mechanosensitive channels: progress towards an understanding of their roles in cell physiology. Curr. Opin. Microbiol. 18, 16–22 (2014).
pubmed: 24607989 pmcid: 4005912
Booth, I. R., Edwards, M. D., Black, S., Schumann, U. & Miller, S. Mechanosensitive channels in bacteria: signs of closure? Nat. Rev. Microbiol. 5, 431 (2007).
pubmed: 17505523
Laventie, B.-J. & Jenal, U. Surface sensing and adaptation in bacteria. Annu. Rev. Microbiol. 74, 735–760 (2020).
pubmed: 32905753
Lee, C. K. et al. Multigenerational memory and adaptive adhesion in early bacterial biofilm communities. Proc. Natl Acad. Sci. USA 115, 4471–4476 (2018).
pubmed: 29559526 pmcid: 5924909
Lee, C. K. et al. Social cooperativity of bacteria during reversible surface attachment in young biofilms: a quantitative comparison of Pseudomonas aeruginosa PA14 and PAO1. mBio 11, e02644–19 (2020).
Wang, C., Hou, J., van der Mei, H. C., Busscher, H. J. & Ren, Y. Emergent properties in Streptococcus mutans biofilms are controlled through adhesion force sensing by initial colonizers. mBio 10, 01908–01919 (2019).
Conrad, J. C. et al. Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa. Biophys. J. 100, 1608–1616 (2011).
pubmed: 21463573 pmcid: 3072661
Gibiansky, M. L. et al. Bacteria use type IV pili to walk upright and detach from surfaces. Science 330, 197–197 (2010).
pubmed: 20929769
Bennett, R. R. et al. Species-dependent hydrodynamics of flagellum-tethered bacteria in early biofilm development. J. R. Soc. Interf.13, 20150966 (2016).
Jenal, U., Reinders, A. & Lori, C. Cyclic di-GMP: second messenger extraordinaire. Nat. Rev. Microbiol. 15, 271 (2017).
pubmed: 28163311
Hengge, R. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7, 263–273 (2009).
pubmed: 19287449
Rybtke, M. T. et al. Fluorescence-based reporter for gauging cyclic di-GMP levels in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78, 5060–5069 (2012).
pubmed: 22582064 pmcid: 3416407
Blacutt, J., Lan, Z., Cosgriff-Hernandez, E. M. & Gordon, V. D. Quantitative confocal microscopy and calibration for measuring differences in cyclic-di-GMP signalling by bacteria on biomedical hydrogels. R. Soc. Open Sci. 8, 201453 (2021).
pubmed: 33614081 pmcid: 7890475
Laventie, B.-J. et al. A surface-induced asymmetric program promotes tissue colonization by Pseudomonas aeruginosa. Cell Host Microbe 25, 140–152.e146 (2019).
pubmed: 30581112
Bertrand, R. L. Lag phase is a dynamic, organized, adaptive, and evolvable period that prepares bacteria for cell division. J. Bacteriol. 201, e00697–00618 (2019).
pubmed: 30642990 pmcid: 6416914
Park, S. & Sauer, K. Controlling Biofilm Development Through Cyclic di-GMP Signaling. Pseudomonas aeruginosa: Biol. Pathogen. Control Strategies, 1386; 69–94 (2022).
Lichtenberg, M. et al. Cyclic-di-GMP signaling controls metabolic activity in Pseudomonas aeruginosa. Cell Rep. 41, 111515 (2022).
pubmed: 36260996
Webster, S. S. et al. Force-induced changes of PilY1 drive surface sensing by Pseudomonas aeruginosa. mBio 13, e03754–03721 (2022).
pmcid: 8806160
Geiger, C. J. & O’Toole, G. A. Evidence for the Type IV Pilus Retraction Motor PilT as a Component of the Surface Sensing System in Pseudomonas aeruginosa. J. Bacteriol. 205, e00179–00123 (2023).
pubmed: 37382531
Trivedi, R. R. et al. Mechanical genomic studies reveal the role of D-alanine metabolism in Pseudomonas aeruginosa cell stiffness. mBio 9; e01340–18 (2018).
Formosa, C., Grare, M., Duval, R. E. & Dague, E. Nanoscale effects of antibiotics on. P. aeruginosa. Nanomed.: NBM 8, 12–16 (2012).
Mathelié-Guinlet, M. et al. Detrimental impact of silica nanoparticles on the nanomechanical properties of Escherichia coli, studied by AFM. J. Colloid Interf. Sci. 529, 53–64 (2018).
Rojas, E. R. et al. The outer membrane is an essential load-bearing element in Gram-negative bacteria. Nature 559, 617–621 (2018).
pubmed: 30022160 pmcid: 6089221
Auer, G. K. & Weibel, D. B. Bacterial cell mechanics. Biochemistry 56, 3710–3724 (2017).
pubmed: 28666084
Tuson, H. H. et al. Measuring the stiffness of bacterial cells from growth rates in hydrogels of tunable elasticity. Mol. Microbiol. 84, 874–891 (2012).
pubmed: 22548341 pmcid: 3359400
Vadillo-Rodriguez, V., Schooling, S. R. & Dutcher, J. R. In situ characterization of differences in the viscoelastic response of individual gram-negative and gram-positive bacterial cells. J. Bacteriol. 191, 5518–5525 (2009).
pubmed: 19581369 pmcid: 2725611
Kumar, U., Vivekanand, K. & Poddar, P. Real-time nanomechanical and topographical mapping on live bacterial cells-Brevibacterium casei under stress due to their exposure to Co
pubmed: 19438181
Francius, G., Domenech, O., Mingeot-Leclercq, M. P. & Dufrêne, Y. F. Direct observation of Staphylococcus aureus cell wall digestion by lysostaphin. J. Bacteriol. 190, 7904–7909 (2008).
pubmed: 18835985 pmcid: 2593208
Thwaites, J. J. & Mendelson, N. H. Mechanical behaviour of bacterial cell walls. Adv. Microb. Physiol. 32, 173–222 (1991).
pubmed: 1882728
Timoshenko, S. P. & Woinowsky-Krieger, S. Theory of plates and shells. (McGraw-hill, 1959).
Matias, V. R., Al-Amoudi, A., Dubochet, J. & Beveridge, T. J. Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J. Bacteriol. 185, 6112–6118 (2003).
pubmed: 14526023 pmcid: 225031
Hayhurst, E. J., Kailas, L., Hobbs, J. K. & Foster, S. J. Cell wall peptidoglycan architecture in Bacillus subtilis. Proc. Natl Acad. Sci. USA 105, 14603–14608 (2008).
pubmed: 18784364 pmcid: 2567149
Saha, N., Monge, C., Dulong, V., Picart, C. & Glinel, K. Influence of Polyelectrolyte Film Stiffness on Bacterial Growth. Biomacromolecules 14, 520–528 (2013).
pubmed: 23289403 pmcid: 4312771
Guégan, C. et al. Alteration of bacterial adhesion induced by the substrate stiffness. Colloids Surf. B Biointerf. 114, 193–200 (2014).
Jacobs, M. A. et al. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 100, 14339–14344 (2003).
pubmed: 14617778 pmcid: 283593
Shillaber, C. P. Photomicrography in theory and practice. (Wiley, 1944).
Krieg, M. et al. Atomic force microscopy-based mechanobiology. Nat. Rev. Phys. 1, 41–57 (2019).
Tivol, W. F., Briegel, A. & Jensen, G. J. An improved cryogen for plunge freezing. Microsc. Microanal. 14, 375–379 (2008).
pubmed: 18793481 pmcid: 3058946
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
Stanzione, D. et al. in Practice and Experience in Advanced Research Computing 106-111 (2020).
Silhavy, T. J., Kahne, D. & Walker, S. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, a000414 (2010).
pubmed: 20452953 pmcid: 2857177
Morris, D. M. & Jensen, G. J. Toward a biomechanical understanding of whole bacterial cells. Annu. Rev. Biochem. 77, 583–613 (2008).
pubmed: 18355161
Shaevitz, J. W. Microbiology: peeling back the layers of bacterial envelope mechanics. Curr. Biol. 28, R1210–R1211 (2018).
pubmed: 30352194
Lo, C.-J., Leake, M. C. & Berry, R. M. Fluorescence measurement of intracellular sodium concentration in single Escherichia coli cells. Biophys. J. 90, 357–365 (2006).
pubmed: 16227503
Ipiña, E. P., Otte, S., Pontier-Bres, R., Czerucka, D. & Peruani, F. Bacteria display optimal transport near surfaces. Nat. Phys. 15, 610 (2019).
Tinevez, J.-Y. et al. TrackMate: An open and extensible platform for single-particle tracking. Methods 115, 80–90 (2017).
pubmed: 27713081
Shanks, R. M., Caiazza, N. C., Hinsa, S. M., Toutain, C. M. & O’Toole, G. A. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl. Environ. Microbiol. 72, 5027–5036 (2006).
pubmed: 16820502 pmcid: 1489352
Rudenko, O. & Barnes, A. C. Gibson Assembly facilitates bacterial allelic exchange mutagenesis. J. Microbiol. Methods 144, 157–163 (2018).
pubmed: 29196271
Ben-David, A. & Davidson, C. E. Estimation method for serial dilution experiments. J. Microbiol. Methods 107, 214–221 (2014).
pubmed: 25205541
Nunamaker, E. A., Otto, K. J. & Kipke, D. R. Investigation of the material properties of alginate for the development of hydrogel repair of dura mater. J. Mech. Behav. Biomed. 4, 16–33 (2011).

Auteurs

Liyun Wang (L)

Department of Physics, Center for Nonlinear Dynamics, The University of Texas at Austin, Austin, TX, 78712, USA.

Yu-Chern Wong (YC)

Department of Physics, Center for Nonlinear Dynamics, The University of Texas at Austin, Austin, TX, 78712, USA.
Department of Mechanical Engineering, The University of Texas at Austin, Austin, TX, 78712, USA.

Joshua M Correira (JM)

Department of Chemistry, The University of Texas at Austin, Austin, TX, 78712, USA.

Megan Wancura (M)

Department of Chemistry, The University of Texas at Austin, Austin, TX, 78712, USA.

Chris J Geiger (CJ)

Geisel School of Medicine at Dartmouth, Hanover, NH, 03755, USA.

Shanice S Webster (SS)

Geisel School of Medicine at Dartmouth, Hanover, NH, 03755, USA.

Ahmed Touhami (A)

Department of Physics and Astronomy University of Texas Rio Grande Valley, One West University Blvd, Brownsville, TX, 78520, USA.

Benjamin J Butler (BJ)

Surfaces, Microstructure and Fracture Group, Cavendish Laboratory, University of Cambridge, Cambridge, CB3 0HE, UK.

George A O'Toole (GA)

Geisel School of Medicine at Dartmouth, Hanover, NH, 03755, USA.

Richard M Langford (RM)

Surfaces, Microstructure and Fracture Group, Cavendish Laboratory, University of Cambridge, Cambridge, CB3 0HE, UK.

Katherine A Brown (KA)

Surfaces, Microstructure and Fracture Group, Cavendish Laboratory, University of Cambridge, Cambridge, CB3 0HE, UK.
Oden Institute for Computational Engineering & Sciences, The University of Texas at Austin, Austin, TX, 78712, USA.

Berkin Dortdivanlioglu (B)

Department of Civil, Architectural, and Environmental Engineering, The University of Texas at Austin, Austin, TX, 78712, USA.

Lauren Webb (L)

Department of Chemistry, The University of Texas at Austin, Austin, TX, 78712, USA.

Elizabeth Cosgriff-Hernandez (E)

Department of Biomedical Engineering, The University of Texas at Austin, Austin, TX, 78712, USA.

Vernita D Gordon (VD)

Department of Physics, Center for Nonlinear Dynamics, The University of Texas at Austin, Austin, TX, 78712, USA. gordon@chaos.utexas.edu.
LaMontagne Center for Infectious Disease, The University of Texas at Austin, Austin, TX, 78712, USA. gordon@chaos.utexas.edu.
Interdisciplinary Life Sciences Graduate Program, The University of Texas at Austin, Austin, TX, 78712, USA. gordon@chaos.utexas.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH