Tuning antimicrobial properties of biomimetic nanopatterned surfaces

Michalska, Martyna; Gambacorta, Francesca; Divan, Ralu; Aranson, Igor S.; Sokolov, Andrey; Noirot, Philippe; Laible, Philip D.

doi:10.1039/c8nr00439k

Tuning antimicrobial properties of biomimetic nanopatterned surfaces

Journal Article · Tue Mar 27 00:00:00 EDT 2018 · Nanoscale

DOI:https://doi.org/10.1039/c8nr00439k· OSTI ID:1460974

^[1]; Gambacorta, Francesca ^[1]; Divan, Ralu ^[1]; Aranson, Igor S. ^[2]; ^[1]; Noirot, Philippe ^[1]; ^[1]

Argonne National Lab. (ANL), Argonne, IL (United States)
Argonne National Lab. (ANL), Argonne, IL (United States); Pennsylvania State Univ., University Park, PA (United States)

Here, nature has amassed an impressive array of structures that afford protection from microbial colonization/infection when displayed on the exterior surfaces of organisms. Here, controlled variation of the features of mimetics derived from etched silicon allows for tuning of their antimicrobial efficacy. Materials with nanopillars up to 7 μm in length are extremely effective against a wide range of microbial species and exceed the performance of natural surfaces; in contrast, materials with shorter/blunter nanopillars (<2 μm) selectively killed specific species. Using a combination of microscopies, the mechanisms by which bacteria are killed are demonstrated, emphasizing the dependence upon pillar density and tip geometry. Additionally, real-time imaging reveals how cells are immobilized and killed rapidly. Generic or selective protection from microbial colonization could be conferred to surfaces [for, e.g., internal medicine, implants (joint, dental, and cosmetic), food preparation, and the agricultural industry] patterned with these materials as coatings.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1460974

Alternate ID(s):: OSTI ID: 1434121

Journal Information:: Nanoscale, Journal Name: Nanoscale Journal Issue: 14 Vol. 10; ISSN NANOHL; ISSN 2040-3364

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

References (53)

Species differences in unlocking B-side electron transfer in bacterial reaction centers Dylla, Nicholas P.; Faries, Kaitlyn M.; Wyllie, Ryan M. FEBS Letters, Vol. 590, Issue 16 https://doi.org/10.1002/1873-3468.12264	journal	July 2016
Biocompatible Multifunctional Black-Silicon for Implantable Intraocular Sensor Lee, Jeong Oen; Narasimhan, Vinayak; Du, Juan Advanced Healthcare Materials, Vol. 6, Issue 4 https://doi.org/10.1002/adhm.201601356	journal	January 2017
Non-Reflecting Silicon and Polymer Surfaces by Plasma Etching and Replication Sainiemi, Lauri; Jokinen, Ville; Shah, Ali Advanced Materials, Vol. 23, Issue 1 https://doi.org/10.1002/adma.201001810	journal	October 2010
Biotechnological applications of supersonic cluster beam-deposited nanostructured thin films: Bottom-up engineering to optimize cell-protein-surface interactions: Bottom-up Engineering to Optimize Cell-Protein-Surface Interactions Singh, Ajay Vikram Journal of Biomedical Materials Research Part A, Vol. 101, Issue 10 https://doi.org/10.1002/jbm.a.34601	journal	March 2013
Black luminescent silicon Pezoldt, Jörg; Kups, Thomas; Stubenrauch, Mike physica status solidi (c), Vol. 8, Issue 3 https://doi.org/10.1002/pssc.201000388	journal	January 2011
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
Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces Hasan, Jafar; Webb, Hayden K.; Truong, Vi Khanh Applied Microbiology and Biotechnology, Vol. 97, Issue 20 https://doi.org/10.1007/s00253-012-4628-5	journal	December 2012
The susceptibility of Staphylococcus aureus CIP 65.8 and Pseudomonas aeruginosa ATCC 9721 cells to the bactericidal action of nanostructured Calopteryx haemorrhoidalis damselfly wing surfaces Truong, Vi Khanh; Geeganagamage, Nipuni Mahanamanam; Baulin, Vladimir A. Applied Microbiology and Biotechnology, Vol. 101, Issue 11 https://doi.org/10.1007/s00253-017-8205-9	journal	March 2017
Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes Kovach, Michael E.; Elzer, Philip H.; Steven Hill, D. Gene, Vol. 166, Issue 1 https://doi.org/10.1016/0378-1119(95)00584-1	journal	December 1995
The interaction of cells and bacteria with surfaces structured at the nanometre scale Anselme, K.; Davidson, P.; Popa, A. M. Acta Biomaterialia, Vol. 6, Issue 10 https://doi.org/10.1016/j.actbio.2010.04.001	journal	October 2010
A review of the biomaterials technologies for infection-resistant surfaces Campoccia, Davide; Montanaro, Lucio; Arciola, Carla Renata Biomaterials, Vol. 34, Issue 34 https://doi.org/10.1016/j.biomaterials.2013.07.089	journal	November 2013
Versatile antimicrobial peptide-based ZnO quantum dots for in vivo bacteria diagnosis and treatment with high specificity Chen, Haiyan; Zhang, Min; Li, Bowen Biomaterials, Vol. 53 https://doi.org/10.1016/j.biomaterials.2015.02.105	journal	June 2015
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
Matrix-Assisted Pulsed Laser Evaporation: A novel approach to design mesoporous carbon films Axente, Emanuel; Sopronyi, Mihai; Matei Ghimbeu, Camélia Carbon, Vol. 122 https://doi.org/10.1016/j.carbon.2017.06.098	journal	October 2017
Natural and bioinspired nanostructured bactericidal surfaces Tripathy, Abinash; Sen, Prosenjit; Su, Bo Advances in Colloid and Interface Science, Vol. 248 https://doi.org/10.1016/j.cis.2017.07.030	journal	October 2017
Nano-structured antimicrobial surfaces: From nature to synthetic analogues Elbourne, Aaron; Crawford, Russell J.; Ivanova, Elena P. Journal of Colloid and Interface Science, Vol. 508 https://doi.org/10.1016/j.jcis.2017.07.021	journal	December 2017
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
Bactericidal nanospike surfaces via thermal oxidation of Ti alloy substrates Sjöström, Terje; Nobbs, Angela H.; Su, Bo Materials Letters, Vol. 167 https://doi.org/10.1016/j.matlet.2015.12.140	journal	March 2016
A comparison of the surface nanostructure from two different types of gram-negative cells: Escherichia coli and Rhodobacter sphaeroides Oestreicher, Zachery; Taoka, Azuma; Fukumori, Yoshihiro Micron, Vol. 72 https://doi.org/10.1016/j.micron.2015.02.001	journal	May 2015
Application of Black Silicon for Nanostructure-Initiator Mass Spectrometry Gao, Jian; de Raad, Markus; Bowen, Benjamin P. Analytical Chemistry, Vol. 88, Issue 3 https://doi.org/10.1021/acs.analchem.5b03452	journal	January 2016
In-Situ Fabrication of a Self-Aligned Selective Emitter Silicon Solar Cell Using the Gold Top Contacts To Facilitate the Synthesis of a Nanostructured Black Silicon Antireflective Layer Instead of an External Metal Nanoparticle Catalyst Lu, Yen-Tien; Barron, Andrew R. ACS Applied Materials & Interfaces, Vol. 7, Issue 22 https://doi.org/10.1021/acsami.5b01008	journal	May 2015
Cicada Wing Surface Topography: An Investigation into the Bactericidal Properties of Nanostructural Features Kelleher, S. M.; Habimana, O.; Lawler, J. ACS Applied Materials & Interfaces, Vol. 8, Issue 24 https://doi.org/10.1021/acsami.5b08309	journal	November 2015
“Race for the Surface”: Eukaryotic Cells Can Win Pham, Vy T. H.; Truong, Vi Khanh; Orlowska, Anna ACS Applied Materials & Interfaces, Vol. 8, Issue 34 https://doi.org/10.1021/acsami.6b06415	journal	August 2016
Bactericidal Effects of Natural Nanotopography of Dragonfly Wing on Escherichia coli Bandara, Chaturanga D.; Singh, Sanjleena; Afara, Isaac O. ACS Applied Materials & Interfaces, Vol. 9, Issue 8 https://doi.org/10.1021/acsami.6b13666	journal	February 2017
Bioinspired Hierarchical Surface Structures with Tunable Wettability for Regulating Bacteria Adhesion Dou, Xiao-Qiu; Zhang, Di; Feng, Chuanliang ACS Nano, Vol. 9, Issue 11 https://doi.org/10.1021/acsnano.5b04231	journal	October 2015
Designer Dual Therapy Nanolayered Implant Coatings Eradicate Biofilms and Accelerate Bone Tissue Repair Min, Jouha; Choi, Ki Young; Dreaden, Erik C. ACS Nano, Vol. 10, Issue 4 https://doi.org/10.1021/acsnano.6b00087	journal	March 2016
Biochemical characterization and electron-transfer reactions of sym1, a Rhodobacter capsulatus reaction center symmetry mutant which affects the initial electron donor Taguchi, Aileen K. W.; Stocker, Jonathan W.; Alden, Rhett G. Biochemistry, Vol. 31, Issue 42 https://doi.org/10.1021/bi00157a024	journal	October 1992
Comparison of M-Side Electron Transfer in Rb. sphaeroides and Rb. capsulatus Reaction Centers Kirmaier, Christine; Laible, Philip D.; Czarnecki, Kazimierz The Journal of Physical Chemistry B, Vol. 106, Issue 7 https://doi.org/10.1021/jp013264w	journal	February 2002
Superhydrophilic and Superwetting Surfaces: Definition and Mechanisms of Control Drelich, Jaroslaw; Chibowski, Emil Langmuir, Vol. 26, Issue 24 https://doi.org/10.1021/la1039893	journal	December 2010
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
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
High-throughput 3D tracking of bacteria on a standard phase contrast microscope Taute, K. M.; Gude, S.; Tans, S. J. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9776	journal	November 2015
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Cicada-inspired cell-instructive nanopatterned arrays Diu, Ting; Faruqui, Nilofar; Sjöström, Terje Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep07122	journal	November 2014
Antibacterial titanium nano-patterned arrays inspired by dragonfly wings Bhadra, Chris M.; Khanh Truong, Vi; Pham, Vy T. H. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16817	journal	November 2015
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
Black silicon: fabrication methods, properties and solar energy applications Liu, Xiaogang; Coxon, Paul R.; Peters, Marius Energy Environ. Sci., Vol. 7, Issue 10 https://doi.org/10.1039/C4EE01152J	journal	January 2014
Nanotopography as a trigger for the microscale, autogenous and passive lysis of erythrocytes Pham, Vy T. H.; Truong, Vi Khanh; Mainwaring, David E. J. Mater. Chem. B, Vol. 2, Issue 19 https://doi.org/10.1039/C4TB00239C	journal	January 2014
Bacterial viability on chemically modified silicon nanowire arrays Susarrey-Arce, A.; Sorzabal-Bellido, I.; Oknianska, A. Journal of Materials Chemistry B, Vol. 4, Issue 18 https://doi.org/10.1039/C6TB00460A	journal	January 2016
Dynamic viscoelastic behavior of individual Gram-negative bacterial cells Vadillo-Rodriguez, Virginia; Dutcher, John R. Soft Matter, Vol. 5, Issue 24 https://doi.org/10.1039/b912227c	journal	January 2009
Viscoelasticity of the bacterial cell envelope Vadillo-Rodríguez, Virginia; Dutcher, John R. Soft Matter, Vol. 7, Issue 9 https://doi.org/10.1039/c0sm01054e	journal	January 2011
Superhydrophobic surfaces for the reduction of bacterial adhesion Zhang, Xiaoxue; Wang, Ling; Levänen, Erkki RSC Advances, Vol. 3, Issue 30 https://doi.org/10.1039/c3ra40497h	journal	January 2013
Structure and function of bacterial outer membrane proteins: barrels in a nutshell Koebnik, Ralf; Locher, Kaspar P.; Van Gelder, Patrick Molecular Microbiology, Vol. 37, Issue 2 https://doi.org/10.1046/j.1365-2958.2000.01983.x	journal	July 2000
The structural and optical properties of black silicon by inductively coupled plasma reactive ion etching Steglich, Martin; Käsebier, Thomas; Zilk, Matthias Journal of Applied Physics, Vol. 116, Issue 17 https://doi.org/10.1063/1.4900996	journal	November 2014
Bacterial flagella explore microscale hummocks and hollows to increase adhesion Friedlander, R. S.; Vlamakis, H.; Kim, P. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14 https://doi.org/10.1073/pnas.1219662110	journal	March 2013
Structure-related antibacterial activity of a titanium nanostructured surface fabricated by glancing angle sputter deposition Sengstock, Christina; Lopian, Michael; Motemani, Yahya Nanotechnology, Vol. 25, Issue 19 https://doi.org/10.1088/0957-4484/25/19/195101	journal	April 2014
Black silicon method: X. A review on high speed and selective plasma etching of silicon with profile control: an in-depth comparison between Bosch and cryostat DRIE processes as a roadmap to next generation equipment Jansen, H. V.; de Boer, M. J.; Unnikrishnan, S. Journal of Micromechanics and Microengineering, Vol. 19, Issue 3, Article No. 033001 https://doi.org/10.1088/0960-1317/19/3/033001	journal	February 2009
The black silicon method: a universal method for determining the parameter setting of a fluorine-based reactive ion etcher in deep silicon trench etching with profile control Jansen, H.; Boer, M. de; Legtenberg, R. Journal of Micromechanics and Microengineering, Vol. 5, Issue 2 https://doi.org/10.1088/0960-1317/5/2/015	journal	June 1995
Different walls for rods and balls: the diversity of peptidoglycan: The diversity of peptidoglycan Turner, Robert D.; Vollmer, Waldemar; Foster, Simon J. Molecular Microbiology, Vol. 91, Issue 5 https://doi.org/10.1111/mmi.12513	journal	January 2014
Nanopatterned polymer surfaces with bactericidal properties Dickson, Mary Nora; Liang, Elena I.; Rodriguez, Luis A. Biointerphases, Vol. 10, Issue 2 https://doi.org/10.1116/1.4922157	journal	June 2015
The Ethanologenic Bacterium Zymomonas mobilis Divides Asymmetrically and Exhibits Heterogeneity in DNA Content Fuchino, Katsuya; Chan, Helena; Hwang, Ling Chin Applied and Environmental Microbiology, Vol. 87, Issue 6 https://doi.org/10.1128/aem.02441-20	journal	February 2021
Hydrophobic pinning with copper nanowhiskers leads to bactericidal properties Singh, Ajay Vikram; Baylan, Semanur; Park, Byung-Wook PLOS ONE, Vol. 12, Issue 4 https://doi.org/10.1371/journal.pone.0175428	journal	April 2017
Natural Insect and Plant Micro-/Nanostructsured Surfaces: An Excellent Selection of Valuable Templates with Superhydrophobic and Self-Cleaning Properties Nguyen, Song; Webb, Hayden; Mahon, Peter Molecules, Vol. 19, Issue 9 https://doi.org/10.3390/molecules190913614	journal	September 2014

Cited By (5)

Ultrafast physical bacterial inactivation and photocatalytic self-cleaning of ZnO nanoarrays for rapid and sustainable bactericidal applications Xie, Yuan; Qu, Xi; Li, Jinyang Science of The Total Environment, Vol. 738 https://doi.org/10.1016/j.scitotenv.2020.139714	journal	October 2020
Effects of Nanopillar Size and Spacing on Mechanical Perturbation and Bactericidal Killing Efficiency Velic, Amar; Jaggessar, Alka; Tesfamichael, Tuquabo Nanomaterials, Vol. 11, Issue 10 https://doi.org/10.3390/nano11102472	journal	September 2021
High‐Aspect‐Ratio Nanostructured Surfaces as Biological Metamaterials Higgins, Stuart G.; Becce, Michele; Belessiotis‐Richards, Alexis Advanced Materials, Vol. 32, Issue 9 https://doi.org/10.1002/adma.201903862	journal	January 2020
Biomimetic antimicrobial material strategies for combating antibiotic resistant bacteria Chee, Eunice; Brown, Ashley C. Biomaterials Science, Vol. 8, Issue 4 https://doi.org/10.1039/c9bm01393h	journal	January 2020
Adhesion and bactericidal properties of nanostructured surfaces dependent on bacterial motility Jindai, Keisuke; Nakade, Kazuki; Masuda, Kyosuke RSC Advances, Vol. 10, Issue 10 https://doi.org/10.1039/c9ra08282d	journal	January 2020