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This is a self-archived version of an original article. This version may differ from the original in pagination and typographic details. Author(s): Bandara, Chaturanga D.; Ballerin, Giulia; Leppänen, Miika; Tesfamichael, Tuquabo; Ostrikov, Kostya (Ken); Whitchurch, Cynthia B. Title: Resolving Bio-Nano Interactions of E.coli Bacteria-Dragonfly Wing Interface with Helium Ion and 3D-Structured Illumination Microscopy to Understand Bacterial Death on Nanotopography Year: 2020 Version: Accepted version (Final draft) Copyright: © 2020 American Chemical Society Rights: In Copyright Rights url: http://rightsstatements.org/page/InC/1.0/?language=en Please cite the original version: Bandara, C. D., Ballerin, G., Leppänen, M., Tesfamichael, T., Ostrikov, K. (., & Whitchurch, C. B. (2020). Resolving Bio-Nano Interactions of E.coli Bacteria-Dragonfly Wing Interface with Helium Ion and 3D-Structured Illumination Microscopy to Understand Bacterial Death on Nanotopography. ACS Biomaterials Science & Engineering, 6(7), 3925-3932. https://doi.org/10.1021/acsbiomaterials.9b01973 Subscriber access provided by JYVASKYLAN UNIV Bio-interactions and Biocompatibility Resolving Bio-Nano Interactions of E.coli Bacteria-Dragonfly Wing Interface with Helium Ion and 3D-Structured Illumination Microscopy to Understand Bacterial Death on Nanotopography Chaturanga D Bandara, Giulia Ballerin, Miika Leppänen, Tuquabo Tesfamichael, Kostya (Ken) Ostrikov, and Cynthia B. Whitchurch ACS Biomater. Sci. Eng., Just Accepted Manuscript • DOI: 10.1021/ acsbiomaterials.9b01973 • Publication Date (Web): 09 Jun 2020 Downloaded from pubs.acs.org on June 11, 2020 Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. 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ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts. is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties. Page 1 of 24 ACS Biomaterials Science & Engineering 1 2 3 4 Resolving Bio-Nano Interactions of E. coli Bacteria-Dragonfly Wing Interface with 5 6 7 Helium Ion and 3D-Structured Illumination Microscopy to Understand Bacterial Death 8 9 10 11 on Nanotopography 12 13 14 15 Chaturanga D. Bandara*†‡, Giulia Ballerin†, Miika Leppänen§, Tuquabo 16 17 18 ‡ ‡ † 19 Tesfamichael , Kostya (Ken) Ostrikov , and Cynthia B. Whitchurch 20 21 22 23 †The ithree Institute, University of Technology Sydney, Ultimo, NSW 2007, Australia 24 25 26 27 ‡ 28 School of Chemistry, Physics and Mechanical Engineering, Science and 29 30 31 Engineering Faculty, Queensland University of Technology (QUT), Brisbane, 32 33 34 35 Queensland 4001, Australia 36 37 38 39 §Nanoscience Center, Department of Physics, Department of Biological and 40 41 42 43 Environmental Science, University of Jyvaskyla, FI-40014 Jyvaskyla, Finland 44 45 46 47 Corresponding Author: [email protected] 48 49 50 51 52 53 54 55 56 57 58 59 60 1 ACS Paragon Plus Environment ACS Biomaterials Science & Engineering Page 2 of 24 1 2 3 ABSTRACT 4 5 Obtaining a comprehensive understanding of the bactericidal mechanisms of natural 6 7 nanotextured surfaces is crucial for the development of fabricated nanotextured surfaces with 8 9 10 efficient bactericidal activity. However, the scale, nature, and speed of bacteria-nanotextured 11 12 surface interactions make the characterization of the interaction a challenging task. There are 13 14 currently several different opinions regarding the possible mechanisms by which bacterial 15 16 17 membrane damage occurs upon interacting with nanotextured surfaces. Advanced imaging 18 19 methods could clarify this by enabling visualization of the interaction. Charged particle 20 21 microscopes can achieve the required nanoscale resolution but are limited to dry samples. In 22 23 24 contrast, light-based methods enable the characterization of living (hydrated) samples but are 25 26 limited by the resolution achievable. Here we utilized both helium ion microscopy (HIM) and 27 28 3D structured illumination microscopy (3D-SIM) techniques to understand the interaction of 29 30 Gram-negative bacterial membranes with nanopillars such as those found on dragonfly wings. 31 32 33 Helium ion microscopy enables cutting and imaging at nanoscale resolution while 3D-SIM is 34 35 a super-resolution optical microscopy technique that allows visualization of live, unfixed 36 37 bacteria at ~100 nm resolution. Upon bacteria-nanopillar interaction, the energy stored due to 38 39 40 the bending of natural nanopillars was estimated and compared with fabricated vertically 41 42 aligned carbon nanotubes. With the same deflection, shorter dragonfly wing nanopillars store 43 44 slightly higher energy compared to carbon nanotubes. This indicates that fabricated surfaces 45 46 47 may achieve similar bactericidal efficiency as dragonfly wings. This study reports in situ 48 49 characterization of bacteria-nanopillar interactions in real-time close to its natural state. These 50 51 microscopic approaches will help further understanding of bacterial membrane interactions 52 53 with nanotextured surfaces and the bactericidal mechanisms of nanotopographies so that more 54 55 56 efficient bactericidal nanotextured surfaces can be designed, fabricated, and their bacteria- 57 58 nanotopography interactions can be assessed in situ. 59 60 2 ACS Paragon Plus Environment Page 3 of 24 ACS Biomaterials Science & Engineering 1 2 3 4 KEYWORDS: bactericidal topography, bio-nano interactions, 3D SIM, dragonfly 5 6 7 wing, helium ion microscopy, ion beam milling 8 9 10 INTRODUCTION 11 12 13 The ability of bacteria to adhere, survive and subsequently form biofilms on abiotic 14 15 16 surfaces is the leading cause for infection of prostheses after surgery, resulting in implant 17 18 failure and revision surgery.1-2 In recent years, there have been significant efforts to reduce 19 20 infection by developing various nanotextured surfaces on implantable medical devices.3-4 21 22 These nanotextured surfaces are often inspired by nature, and the fabricated topographies are 23 24 25 expected to reduce initial bacterial adhesion or kill any bacteria attempting to attach to the 26 27 surface. The investigation of bacteria-nanotopography interactions has, therefore, become a 28 29 significant research interest for the efficient and effective development of advanced fabricated 30 31 5-8 32 bactericidal nanotextured surfaces (NTS) for biomaterials application. This is a growing field 33 34 of research as nanotextured surfaces do not leach bactericidal chemicals, and therefore, the 35 36 bactericidal property is conserved for longer periods compared to chemical approaches.9-10 37 38 39 Furthermore, nanotextured surfaces are non-toxic and more effective at controlling bacterial 40 41 strains that produce extracellular polymeric substance (EPS) secretions.11-12 42 43 44 The mechanical bactericidal efficacy of nanotextured surfaces is dependent on the 45 46 nanotopography, architecture of the nanostructures, surface chemistry, and the type of 47 48 bacteria.5, 8, 13-16 However, the antibacterial mechanisms and effectiveness of surface 49 50 51 parameters are not well understood due to the limited understanding of the bacteria- 52 53 nanotopography interactions. Recently, various views and explanations have been proposed for 54 55 understanding the mechanism of membrane damage.5-8, 13, 17-21 56 57 58 Cicada wing-like nanostructures are mainly bactericidal against Gram-negative 59 60 bacteria.7, 22-23 The initial report of bacterial membrane damage upon interaction with cicada 3 ACS Paragon Plus Environment ACS Biomaterials Science & Engineering Page 4 of 24 1 2 3 wing nanostructures used a differential DNA staining method with confocal microscopy to 4 5 6, 24 6 predict the membrane integrity. This approach is an indirect measurement of the membrane 7 8 condition, where two separate fluorescent markers are used to stain the nuclear material. As 9 10 this approach only stains the DNA, it cannot be used to visualize the bacterial membrane 11 12 directly. Furthermore, due to the limitations in spatial resolution, confocal microscopy can only 13 14 15 resolve the color variation of the bacterium