Structure-Based Design of Dual Bactericidal and Bacteria-Releasing Nanosurfaces

Salatto, Daniel; Huang, Zhixing; Benziger, Peter Todd; Carrillo, Jan-Michael Y.; Bajaj, Yashasvi; Gauer, Aiden; Tsapatsaris, Leonidas; Sumpter, Bobby G.; Li, Ruipeng; Takenaka, Mikihito; Yin, Wei; Thanassi, David G.; Endoh, Maya; Koga, Tadanori

doi:10.1021/acsami.2c18121

Title: Structure-Based Design of Dual Bactericidal and Bacteria-Releasing Nanosurfaces

Journal Article · Wed Jan 04 00:00:00 EST 2023 · ACS Applied Materials and Interfaces

DOI:https://doi.org/10.1021/acsami.2c18121· OSTI ID:1908066

Salatto, Daniel ^[1]; Huang, Zhixing ^[1]; Benziger, Peter Todd ^[1];

^[2]; Bajaj, Yashasvi ^[1]; Gauer, Aiden ^[1]; Tsapatsaris, Leonidas ^[1];

^[2]; Li, Ruipeng ^[3]; Takenaka, Mikihito ^[4]; Yin, Wei ^[1]; Thanassi, David G. ^[1];

^[1];

^[1]

Stony Brook Univ., NY (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Sciences (CNMS)
Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)
Kyoto Univ. (Japan)

Here, we report synergistic nanostructured surfaces combining bactericidal and bacteria-releasing properties. A polystyrene-block-poly(methyl methacrylate) (PS-block-PMMA) diblock copolymer is used to fabricate vertically oriented cylindrical PS structures (“PS nanopillars”) on silicon substrates. The results demonstrate that the PS nanopillars (with a height of about 10 nm, size of about 50 nm, and spacing of about 70 nm) exhibit highly effective bactericidal and bacteria-releasing properties (“dual properties”) against Escherichia coli for at least 36 h of immersion in an E. coli solution. Interestingly, the PS nanopillars coated with a thin layer (≈3 nm thick) of titanium oxide (TiO₂) (“TiO₂ nanopillars”) show much improved dual properties against E. coli (a Gram-negative bacterium) compared to the PS nanopillars. Moreover, the dual properties emerge against Listeria monocytogenes (a Gram-positive bacterium). To understand the mechanisms underlying the multifaceted property of the nanopillars, coarse-grained molecular dynamics (MD) simulations of a lipid bilayer (as a simplified model for E. coli) in contact with a substrate containing hexagonally packed hydrophilic nanopillars were performed. The MD results demonstrate that when the bacterium–substrate interaction is strong, the lipid heads adsorb onto the nanopillar surfaces, conforming the shape of a lipid bilayer to the structure/curvature of nanopillars and generating high stress concentrations within the membrane (i.e., the driving force for rupture) at the edge of the nanopillars. Membrane rupture begins with the formation of pores between nanopillars (i.e., bactericidal activity) and ultimately leads to the membrane withdrawal from the nanopillar surface (i.e., bacteria-releasing activity). In the case of Gram-positive bacteria, the adhesion area to the pillar surface is limited due to the inherent stiffness of the bacteria, creating higher stress concentrations within a bacterial cell wall. In conclusion, the present study provides insight into the mechanism underlying the “adhesion-mediated” multifaceted property of nanosurfaces, which is crucial for the development of next-generation antibacterial surface coatings for relevant medical applications.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States). Center for Functional Nanomaterials (CFN); Brookhaven National Laboratory (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); Kyoto University

Grant/Contract Number:: AC05-00OR22725; SC0012704; 2022-96

OSTI ID:: 1908066

Alternate ID(s):: OSTI ID: 1973509

Report Number(s):: BNL-224383-2023-JAAM

Journal Information:: ACS Applied Materials and Interfaces, Vol. 15, Issue 2; ISSN 1944-8244

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (67)

Suppression of Carbon Monoxide Poisoning in Proton Exchange Membrane Fuel Cells via Gold Nanoparticle/Titania Ultrathin Film Heterogeneous Catalysts Wang, Likun; Zhou, Yuchen; Yang, Yuanxi ACS Applied Energy Materials, Vol. 2, Issue 5 https://doi.org/10.1021/acsaem.9b00264	journal	April 2019
Mechanical Model of Vertical Nanowire Cell Penetration Xie, Xi; Xu, Alexander M.; Angle, Matthew R. Nano Letters, Vol. 13, Issue 12 https://doi.org/10.1021/nl403201a	journal	November 2013
Variation in the density, optical polarizabilities, and crystallinity of TiO ₂ thin films deposited via atomic layer deposition from 38 to 150 °C using the titanium tetrachloride-water reaction Piercy, Brandon D.; Leng, Collen Z.; Losego, Mark D. Journal of Vacuum Science & Technology A: Vacuum, Surfaces, and Films, Vol. 35, Issue 3 https://doi.org/10.1116/1.4979047	journal	May 2017
Effective Antibacterial Nanotextured Surfaces Based on Extreme Wettability and Bacteriophage Seeding Boinovich, Ludmila B.; Modin, Evgeny B.; Aleshkin, Andrey V. ACS Applied Nano Materials, Vol. 1, Issue 3 https://doi.org/10.1021/acsanm.8b00090	journal	February 2018
Microtopographic Patterns Affect Escherichia coli Biofilm Formation on Poly(dimethylsiloxane) Surfaces Hou, Shuyu; Gu, Huan; Smith, Cassandra Langmuir, Vol. 27, Issue 6 https://doi.org/10.1021/la1046194	journal	February 2011
Direct and Fast Assessment of Antimicrobial Surface Activity Using Molecular Dynamics Simulation and Time-Lapse Imaging Sibilo, Rafaël; Mannelli, Ilaria; Reigada, Ramon Analytical Chemistry, Vol. 92, Issue 10 https://doi.org/10.1021/acs.analchem.0c00367	journal	April 2020
Engineering Substrate Topography at the Micro- and Nanoscale to Control Cell Function Bettinger, Christopher J.; Langer, Robert; Borenstein, Jeffrey T. Angewandte Chemie International Edition, Vol. 48, Issue 30 https://doi.org/10.1002/anie.200805179	journal	July 2009
Long-term survival during stationary phase: evolution and the GASP phenotype Finkel, Steven E. Nature Reviews Microbiology, Vol. 4, Issue 2 https://doi.org/10.1038/nrmicro1340	journal	February 2006
Graphene oxide conjugated with polymers: a study of culture condition to determine whether a bacterial growth stimulant or an antimicrobial agent? Wu, Ping-Ching; Chen, Hua-Han; Chen, Shih-Yao Journal of Nanobiotechnology, Vol. 16, Issue 1 https://doi.org/10.1186/s12951-017-0328-8	journal	January 2018
Significance and Characteristics ofListeria monocytogenesin Poultry Products Jamshidi, Abdollah; Zeinali, Tayebeh International Journal of Food Science, Vol. 2019 https://doi.org/10.1155/2019/7835253	journal	April 2019
Orientation Control of Block Copolymer Thin Films Placed on Ordered Nanoparticle Monolayers Kim, Taehee; Wooh, Sanghyuk; Son, Jeong Gon Macromolecules, Vol. 46, Issue 20 https://doi.org/10.1021/ma401601f	journal	October 2013
Bactericidal activity of black silicon Ivanova, Elena P.; Hasan, Jafar; Webb, Hayden K. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3838	journal	November 2013
Revealed Architectures of Adsorbed Polymer Chains at Solid-Polymer Melt Interfaces Gin, Peter; Jiang, Naisheng; Liang, Chen Physical Review Letters, Vol. 109, Issue 26 https://doi.org/10.1103/PhysRevLett.109.265501	journal	December 2012
Natural Bactericidal Surfaces: Mechanical Rupture of Pseudomonas aeruginosa Cells by Cicada Wings Ivanova, Elena P.; Hasan, Jafar; Webb, Hayden K. Small, Vol. 8, Issue 16 https://doi.org/10.1002/smll.201200528	journal	June 2012
Biophysical Model of Bacterial Cell Interactions with Nanopatterned Cicada Wing Surfaces Pogodin, Sergey; Hasan, Jafar; Baulin, Vladimir A. Biophysical Journal, Vol. 104, Issue 4 https://doi.org/10.1016/j.bpj.2012.12.046	journal	February 2013
Self-cleaning surfaces — virtual realities Blossey, Ralf Nature Materials, Vol. 2, Issue 5, p. 301-306 https://doi.org/10.1038/nmat856	journal	May 2003
Comment on “Bactericidal Effects of Natural Nanotopography of Dragonfly Wing on Escherichia coli” Linklater, Denver P.; Juodkazis, Saulius; Rubanov, Sergey ACS Applied Materials & Interfaces, Vol. 9, Issue 35 https://doi.org/10.1021/acsami.7b05707	journal	August 2017
Capturing Wetting States in Nanopatterned Silicon Xu, XiuMei; Vereecke, Guy; Chen, Chang ACS Nano, Vol. 8, Issue 1 https://doi.org/10.1021/nn405621w	journal	January 2014
Nanoscale Topography on Black Titanium Imparts Multi-biofunctional Properties for Orthopedic Applications Hasan, Jafar; Jain, Shubham; Chatterjee, Kaushik Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep41118	journal	January 2017
Analysis of different approaches for evaluation of surface energy of microbial cells by contact angle goniometry Sharma, P. K.; Hanumantha Rao, K. Advances in Colloid and Interface Science, Vol. 98, Issue 3 https://doi.org/10.1016/S0001-8686(02)00004-0	journal	August 2002
Atomic layer deposition of titanium dioxide using titanium tetrachloride and titanium tetraisopropoxide as precursors Chaukulkar, Rohan P.; Agarwal, Sumit Journal of Vacuum Science & Technology A: Vacuum, Surfaces, and Films, Vol. 31, Issue 3 https://doi.org/10.1116/1.4798385	journal	May 2013
A Computational Approach for Modeling Neutron Scattering Data from Lipid Bilayers Carrillo, Jan-Michael Y.; Katsaras, John; Sumpter, Bobby G. Journal of Chemical Theory and Computation, Vol. 13, Issue 2 https://doi.org/10.1021/acs.jctc.6b00968	journal	January 2017
Water structure as a function of temperature from X-ray scattering experiments and ab initio molecular dynamics Hura, Greg; Russo, Daniela; Glaeser, Robert M. Physical Chemistry Chemical Physics, Vol. 5, Issue 10 https://doi.org/10.1039/b301481a	journal	January 2003
Atomic layer deposition of nano-TiO₂thin films with enhanced biocompatibility and antimicrobial activity for orthopedic implants Liu, Luting; Bhatia, Ritwik; Webster, Thomas International Journal of Nanomedicine, Vol. Volume 12 https://doi.org/10.2147/IJN.S148065	journal	January 2017
Rough ideas on wetting Quéré, David Physica A: Statistical Mechanics and its Applications, Vol. 313, Issue 1-2 https://doi.org/10.1016/S0378-4371(02)01033-6	journal	October 2002
Mechano-bactericidal actions of nanostructured surfaces Linklater, Denver P.; Baulin, Vladimir A.; Juodkazis, Saulius Nature Reviews Microbiology, Vol. 19, Issue 1 https://doi.org/10.1038/s41579-020-0414-z	journal	August 2020
Development of plasma etching processes to pattern sub-15 nm features with PS- b -PMMA block copolymer masks: Application to advanced CMOS technology Delalande, Michaël; Cunge, Gilles; Chevolleau, Thierry Journal of Vacuum Science & Technology B, Nanotechnology and Microelectronics: Materials, Processing, Measurement, and Phenomena, Vol. 32, Issue 5 https://doi.org/10.1116/1.4895334	journal	September 2014
Histomorphometric, ultrastructural and microhardness evaluation of the osseointegration of a nanostructured titanium oxide coating by metal-organic chemical vapour deposition: an in vivo study Giavaresi, G. Biomaterials, Vol. 25, Issue 25 https://doi.org/10.1016/j.biomaterials.2004.01.017	journal	November 2004
Patterning with block copolymer thin films Segalman, Rachel A. Materials Science and Engineering: R: Reports, Vol. 48, Issue 6, p. 191-226 https://doi.org/10.1016/j.mser.2004.12.003	journal	February 2005
Irena : tool suite for modeling and analysis of small-angle scattering Ilavsky, Jan; Jemian, Peter R. Journal of Applied Crystallography, Vol. 42, Issue 2 https://doi.org/10.1107/S0021889809002222	journal	February 2009
The Anti-Biofouling Properties of Superhydrophobic Surfaces are Short-Lived Hwang, Gi Byoung; Page, Kristopher; Patir, Adnan ACS Nano, Vol. 12, Issue 6 https://doi.org/10.1021/acsnano.8b02293	journal	May 2018
Subtle Variations in Surface Properties of Black Silicon Surfaces Influence the Degree of Bactericidal Efficiency Bhadra, Chris M.; Werner, Marco; Baulin, Vladimir A. Nano-Micro Letters, Vol. 10, Issue 2 https://doi.org/10.1007/s40820-017-0186-9	journal	February 2018
Block Copolymer Lithography: Merging “Bottom-Up” with “Top-Down” Processes Hawker, Craig J.; Russell, Thomas P. MRS Bulletin, Vol. 30, Issue 12, p. 952-966 https://doi.org/10.1557/mrs2005.249	journal	December 2005
Characterization of physicochemical forces involved in adhesion of Listeria monocytogenes to surfaces Mafu, A. A.; Roy, D.; Goulet, J. Applied and Environmental Microbiology, Vol. 57, Issue 7 https://doi.org/10.1128/aem.57.7.1969-1973.1991	journal	July 1991
Formation Mechanism of High-Density, Flattened Polymer Nanolayers Adsorbed on Planar Solids Jiang, Naisheng; Shang, Jun; Di, Xiaoyu Macromolecules, Vol. 47, Issue 8 https://doi.org/10.1021/ma5003485	journal	April 2014
Morphology of Air Nanobubbles Trapped at Hydrophobic Nanopatterned Surfaces Checco, Antonio; Hofmann, Tommy; DiMasi, Elaine Nano Letters, Vol. 10, Issue 4 https://doi.org/10.1021/nl9042246	journal	April 2010
Solvent-free model for self-assembling fluid bilayer membranes: Stabilization of the fluid phase based on broad attractive tail potentials Cooke, Ira R.; Deserno, Markus The Journal of Chemical Physics, Vol. 123, Issue 22 https://doi.org/10.1063/1.2135785	journal	December 2005
Directing cell migration and organization via nanocrater-patterned cell-repellent interfaces Jeon, Hojeong; Koo, Sangmo; Reese, Willie Mae Nature Materials, Vol. 14, Issue 9 https://doi.org/10.1038/nmat4342	journal	July 2015
Dynamics of entangled linear polymer melts: A molecular‐dynamics simulation Kremer, Kurt; Grest, Gary S. The Journal of Chemical Physics, Vol. 92, Issue 8 https://doi.org/10.1063/1.458541	journal	April 1990
Resistance Of Solid Surfaces To Wetting By Water Wenzel, Robert N. Industrial & Engineering Chemistry, Vol. 28, Issue 8, p. 988-994 https://doi.org/10.1021/ie50320a024	journal	August 1936
Wetting and Roughness Quéré, David Annual Review of Materials Research, Vol. 38, Issue 1, p. 71-99 https://doi.org/10.1146/annurev.matsci.38.060407.132434	journal	August 2008
Bacterial Cell Mechanics Auer, George K.; Weibel, Douglas B. Biochemistry, Vol. 56, Issue 29 https://doi.org/10.1021/acs.biochem.7b00346	journal	July 2017
Bactericidal performance of nanostructured surfaces by fluorocarbon plasma Vassallo, E.; Pedroni, M.; Silvetti, T. Materials Science and Engineering: C, Vol. 80 https://doi.org/10.1016/j.msec.2017.05.111	journal	November 2017
The multi-faceted mechano-bactericidal mechanism of nanostructured surfaces Ivanova, Elena P.; Linklater, Denver P.; Werner, Marco Proceedings of the National Academy of Sciences, Vol. 117, Issue 23 https://doi.org/10.1073/pnas.1916680117	journal	May 2020
Implementing molecular dynamics on hybrid high performance computers – short range forces Brown, W. Michael; Wang, Peng; Plimpton, Steven J. Computer Physics Communications, Vol. 182, Issue 4 https://doi.org/10.1016/j.cpc.2010.12.021	journal	April 2011
Antibacterial effects of nanopillar surfaces are mediated by cell impedance, penetration and induction of oxidative stress Jenkins, J.; Mantell, J.; Neal, C. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15471-x	journal	April 2020
Exploring and Engineering the Cell Surface Interface Stevens, M. M. Science, Vol. 310, Issue 5751 https://doi.org/10.1126/science.1106587	journal	November 2005
Calculation of interfacial tension in polymer systems Wu, Souheng Journal of Polymer Science Part C: Polymer Symposia, Vol. 34, Issue 1 https://doi.org/10.1002/polc.5070340105	journal	January 1971
Bactericidal mechanism of nanopatterned surfaces Li, Xinlei Physical Chemistry Chemical Physics, Vol. 18, Issue 2 https://doi.org/10.1039/C5CP05646B	journal	January 2016
Thermoresponsive Nanostructures: From Mechano-Bactericidal Action to Bacteria Release Jiang, Rujian; Yi, Yaozhen; Hao, Lingwan ACS Applied Materials & Interfaces, Vol. 13, Issue 51 https://doi.org/10.1021/acsami.1c16487	journal	December 2021
Tuning antimicrobial properties of biomimetic nanopatterned surfaces Michalska, Martyna; Gambacorta, Francesca; Divan, Ralu Nanoscale, Vol. 10, Issue 14 https://doi.org/10.1039/C8NR00439K	journal	January 2018
Chemically Enhancing Block Copolymers for Block-Selective Synthesis of Self-Assembled Metal Oxide Nanostructures Kamcev, Jovan; Germack, David S.; Nykypanchuk, Dmytro ACS Nano, Vol. 7, Issue 1 https://doi.org/10.1021/nn304122b	journal	December 2012
Influence of High Pressure on the Bending Rigidity of Model Membranes Purushothaman, Sowmya; Cicuta, Pietro; Ces, Oscar The Journal of Physical Chemistry B, Vol. 119, Issue 30 https://doi.org/10.1021/acs.jpcb.5b05272	journal	July 2015
Variation in Resistance of Natural Isolates ofEscherichia coli O157 to High Hydrostatic Pressure, Mild Heat, and Other Stresses Benito, Amparo; Ventoura, Georgia; Casadei, Maria Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/AEM.65.4.1564-1569.1999	journal	April 1999
Dispersion Properties of Optical Polymers Sultanova, N.; Kasarova, S.; Nikolov, I. Acta Physica Polonica A, Vol. 116, Issue 4 https://doi.org/10.12693/APhysPolA.116.585	journal	October 2009
The effect of topography of polymer surfaces on platelet adhesion Koh, Li Buay; Rodriguez, Isabel; Venkatraman, Subbu S. Biomaterials, Vol. 31, Issue 7 https://doi.org/10.1016/j.biomaterials.2009.11.022	journal	March 2010
Structure-induced switching of interpolymer adhesion at a solid–polymer melt interface Jiang, Naisheng; Sen, Mani; Zeng, Wenduo Soft Matter, Vol. 14, Issue 7 https://doi.org/10.1039/C7SM02279D	journal	January 2018
Molecular Modeling and Simulation of the Peptidoglycan Layer of Gram-Positive Bacteria Staphylococcus aureus Pokhrel, Rudramani; Shakya, Rojesh; Baral, Prabin Journal of Chemical Information and Modeling, Vol. 62, Issue 20 https://doi.org/10.1021/acs.jcim.2c00437	journal	August 2022
Surface thermodynamics of bacterial adhesion Absolom, D. R.; Lamberti, F. V.; Policova, Z. Applied and Environmental Microbiology, Vol. 46, Issue 1 https://doi.org/10.1128/aem.46.1.90-97.1983	journal	July 1983
Theoretical study on the bactericidal nature of nanopatterned surfaces Xue, Fudong; Liu, Junjie; Guo, Longfang Journal of Theoretical Biology, Vol. 385 https://doi.org/10.1016/j.jtbi.2015.08.011	journal	November 2015
Quantitatively Predicting Bacterial Adhesion Using Surface Free Energy Determined with a Spectrophotometric Method Zhang, Xinru; Zhang, Qian; Yan, Tao Environmental Science & Technology, Vol. 49, Issue 10 https://doi.org/10.1021/es5050425	journal	May 2015
“Structurally Neutral” Densely Packed Homopolymer-Adsorbed Chains for Directed Self-Assembly of Block Copolymer Thin Films Morimitsu, Yuma; Salatto, Daniel; Jiang, Naisheng Macromolecules, Vol. 52, Issue 14 https://doi.org/10.1021/acs.macromol.9b00597	journal	July 2019
Contact angle measurement and contact angle interpretation Kwok, D. Y.; Neumann, A. W. Advances in Colloid and Interface Science, Vol. 81, Issue 3 https://doi.org/10.1016/S0001-8686(98)00087-6	journal	September 1999
Complicated Catheter-Associated Urinary Tract Infections Due to Escherichia coli and Proteus mirabilis Jacobsen, S. M.; Stickler, D. J.; Mobley, H. L. T. Clinical Microbiology Reviews, Vol. 21, Issue 1 https://doi.org/10.1128/CMR.00019-07	journal	January 2008
Surface Wettability Is a Key Feature in the Mechano-Bactericidal Activity of Nanopillars Valiei, Amin; Lin, Nicholas; McKay, Geoffrey ACS Applied Materials & Interfaces, Vol. 14, Issue 24 https://doi.org/10.1021/acsami.2c03258	journal	June 2022
Bio-Inspired Self-Cleaning Surfaces Liu, Kesong; Jiang, Lei Annual Review of Materials Research, Vol. 42, Issue 1 https://doi.org/10.1146/annurev-matsci-070511-155046	journal	August 2012
Structural and Dynamical Roles of Bound Polymer Chains in Rubber Reinforcement Salatto, Daniel; Carrillo, Jan-Michael Y.; Endoh, Maya K. Macromolecules, Vol. 54, Issue 23 https://doi.org/10.1021/acs.macromol.1c01239	journal	November 2021

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36 MATERIALS SCIENCE
bactericidal
bacteria-releasing
nanopatterned surfaces
block copolymers
titanium oxide

Title: Structure-Based Design of Dual Bactericidal and Bacteria-Releasing Nanosurfaces

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