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Hierarchical Rose Petal Surfaces Delay the Early-Stage Bacterial Biofilm Growth

  • Yunyi Cao
    Yunyi Cao
    School of Engineering, Newcastle University, Newcastle Upon Tyne NE1 7RU, U.K.
    More by Yunyi Cao
    Orcidhttp://orcid.org/0000-0003-3400-0394
  • , 
  • Saikat Jana
    Saikat Jana
    School of Engineering, Newcastle University, Newcastle Upon Tyne NE1 7RU, U.K.
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  • , 
  • Leon Bowen
    Leon Bowen
    Department of Physics, Durham University, Durham DH1 3LE, U.K.
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  • , 
  • Xiaolong Tan
    Xiaolong Tan
    School of Pharmacy, Newcastle University, Newcastle Upon Tyne NE1 7RU, U.K.
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  • , 
  • Hongzhong Liu
    Hongzhong Liu
    School of Mechanical Engineering, Xi’an Jiaotong University, Xi’an 710054, China
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  • , 
  • Nadia Rostami
    Nadia Rostami
    School of Dental Sciences, Newcastle University, Newcastle Upon Tyne NE2 4BW, U.K.
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  • , 
  • James Brown
    James Brown
    Centre for Biomolecular Sciences, University of Nottingham, Nottingham NG7 2RD, U.K.
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  • , 
  • Nicholas S. Jakubovics
    Nicholas S. Jakubovics
    School of Dental Sciences, Newcastle University, Newcastle Upon Tyne NE2 4BW, U.K.
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  • , and 
  • Jinju Chen*
    Jinju Chen
    School of Engineering, Newcastle University, Newcastle Upon Tyne NE1 7RU, U.K.
    *E-mail: [email protected]
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Cite this: Langmuir 2019, 35, 45, 14670–14680
Publication Date (Web):October 20, 2019
https://doi.org/10.1021/acs.langmuir.9b02367
Copyright © 2019 American Chemical Society
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    Abstract

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    A variety of natural surfaces exhibit antibacterial properties; as a result, significant efforts in the past decade have been dedicated toward fabrication of biomimetic surfaces that can help control biofilm growth. Examples of such surfaces include rose petals, which possess hierarchical structures like the micropapillae measuring tens of microns and nanofolds that range in the size of 700 ± 100 nm. We duplicated the natural structures on rose petal surfaces via a simple UV-curable nanocasting technique and tested the efficacy of these artificial surfaces in preventing biofilm growth using clinically relevant bacteria strains. The rose petal-structured surfaces exhibited hydrophobicity (contact angle (CA) ≈ 130.8° ± 4.3°) and high CA hysteresis (∼91.0° ± 4.9°). Water droplets on rose petal replicas evaporated following the constant contact line mode, indicating the likely coexistence of both Cassie and Wenzel states (Cassie–Baxter impregnating the wetting state). Fluorescence microscopy and image analysis revealed the significantly lower attachment of Staphylococcus epidermidis (86.1 ± 6.2% less) and Pseudomonas aeruginosa (85.9 ± 3.2% less) on the rose petal-structured surfaces, compared with flat surfaces over a period of 2 h. An extensive biofilm matrix was observed in biofilms formed by both species on flat surfaces after prolonged growth (several days), but was less apparent on rose petal-biomimetic surfaces. In addition, the biomass of S. epidermidis (63.2 ± 9.4% less) and P. aeruginosa (76.0 ± 10.0% less) biofilms were significantly reduced on the rose petal-structured surfaces, in comparison to the flat surfaces. By comparing P. aeruginosa growth on representative unitary nanopillars, we demonstrated that hierarchical structures are more effective in delaying biofilm growth. The mechanisms are two-fold: (1) the nanofolds across the hemispherical micropapillae restrict initial attachment of bacterial cells and delay the direct contact of cells via cell alignment and (2) the hemispherical micropapillae arrays isolate bacterial clusters and inhibit the formation of a fibrous network. The hierarchical features on rose petal surfaces may be useful for developing strategies to control biofilm formation in medical and industrial contexts.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.9b02367.

    • Method to determine the surface area covered by bacteria. Method to fabricate the nano-pillars. Digital images of evaporation processes of water droplets on surfaces. SEM images of S. epidermidis and P. aeruginosa growth on rose-petal surfaces. Biofilm growth of P. aeruginosa on the flat and rose-petal structured surfaces after 48 h. SEM image of P. aeruginosa biofilm after 24 h on unitary nano-pillar surfaces. (PDF)

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