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Investigation of the Molecular Organisation of Antibacterial Insect Wing Surfaces

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Investigation of the Molecular Organisation of Antibacterial Insect Wing Surfaces Investigation of the molecular organisation of antibacterial insect wing surfaces Submitted in total fulfilment of the requirements for the degree of Doctor of Philosophy by Song Ha Nguyen Department of Chemistry and Biotechnology Faculty of Science, Engineering, and Technology Swinburne University of Technology May 2015 ______________________________________________________________________ Abstract It has been known for some time that the surfaces of many plants and insects exhibit superhydrophobicity and self-cleaning properties. Plant leaves have been intensively studied for over a decade since the discovery of the “lotus effect”, where water droplets readily roll off the surfaces of lotus leaves. The water droplets, once landed on the surfaces of the leaves, retain their spherical shape. This arises from the superhydrophobicity of the surface. When this surface is tilted on a small angle (θtilt < 10°), the water droplets roll off the surface of the leaves, collecting all the dirt and contaminants as they go, affording the leaves the ability to ‘self-clean’. A large amount of information has been obtained regarding the surface properties of lotus leaves; however the surface properties of insects have not received as much attention in this context, despite the fact that they often present similarly effective self-cleaning properties. This work was undertaken in an effort to fill this gap in scientific knowledge. Insect wings surfaces are covered by an epicuticle layer that is composed of hydrophobic substances, which are responsible for imparting the superhydrophobic and self-cleaning properties to some species. The surfaces of dragonfly wings are covered by an array of nanopillars, which were recently discovered to have bactericidal activity. In this work, the molecular organisation of dragonfly wings was investigated to gain an insight into how the individual nanopillars were constructed and behave when coming into contact with attaching bacterial species. Over 60 different substances were identified as comprising the insect wing surfaces, including aliphatic hydrocarbons and fatty acids. The precise chemical compositions not only directly contribute to the superhydrophobic properties of the wings, but also determine their nano-architectures. A new sub-layer of the dragonfly wing epicuticle is proposed, the meso-epicuticle, which is composed only of aliphatic hydrocarbons. This meso-epicuticle is distinct from the outer- and inner-epicuticular layers. The bactericidal properties of dragonfly wings have been reported to arise purely due to physical means, and hence the surface morphologies and topographies of the dragonfly wings were characterised to investigate the nature of the mechanism(s) responsible for the bactericidal effect. The wing surfaces of two species of dragonfly, Hemianax papuensis and Diplacodes bipunctata, were investigated for this purpose. It ii was suggested that mechano-bactericidal and self-cleaning properties of the wings are two distinct mechanisms that dragonflies have developed in order to cope with bacterial contamination. Wetting and adhesion are affected by both the surface topography and surface chemistry with the presence of precisely defined topographical features resulting in bactericidal properties. Moreover, a subtle change in the morphological parameters may instead enhance the ability for the surface to self-clean. This knowledge about the relative contribution of molecular organisation and surface topology to the overall surface properties of dragonfly wings was used to inform the synthetic stage of the project. Eicosane, docosane, palmitic acid and stearic acid, all of which were found to be major components present in the epicuticular layer of dragonfly wings, were allowed to self-assemble on the surface of highly-ordered pyrolytic graphite (HOPG) to produce an ordered structure, which may replicate the antibacterial properties of dragonfly wings. Both of the alkanes assembled into ‘micro- rodlet’ type structures, while the fatty acids recrystallised into sharper ‘micro-blades’. In the case of the alkane micro-rodlets, bacterial cells coming into contact with the substrate surface containing these rodlets were found to align along the alkane crystallites. The mechanism responsible for this behaviour was determined to be a result of the air-pockets trapped between the surface structures, and hence the bacteria were limited in their colonisation to the areas of the surface that could be accessed by water. Bacterial alignment on the fatty acid interfaces was less obvious; however these surfaces were capable of killing the bacteria. The structure of the micro-blades was integral in this case; it appeared that the high radius of curvature of the sharp edge were able to rupture the bacterial cells through high stress upon contact and adhesion. The results of this study contribute to the general knowledge available on the molecular organisation of the epicuticle of dragonfly wings, with specific contribution to the surface properties of the wings, such as their superhydrophobicity, bactericidal behaviour and their ability to self-clean. The key mechanisms responsible for each of these properties were proposed to be closely related to the interplay between the wettability of the surface and the ability of the surface to retain air between the topographical structures. This study also introduced a fast and facile method of producing artificial surfaces, being the self-assembly of lipids onto ordered substrata. The resulting surfaces were found to be successful in exerting antibacterial effects both before and after bacteria attachment. iii Acknowledgements First and foremost, I would like to acknowledge and send my greatest appreciation to my primary supervisor, Professor Elena Ivanova for all of her advice and support during the course of my study. Just like a mother figure, her inspiration, motivation, and encouragement were the driving forces pushing me forward to completion of this work. She does not mind to stand up for her students whenever they are treated unfairly. Despite her busy schedule, she has always taken time to talk with me whenever I stumbled across problems, and I’m really grateful for that. Similarly, I would also like to thank Professor Russell Crawford, Professor David Mainwaring, and Dr. Peter Mahon for co-supervising the project, and for spending time helping me on various manuscripts and papers that I prepared. Being supervisors of a non-English speaking student would not be an easy job and they have always been patient with me, I really appreciate that. Special thank you to Dr. Peter Mahon, who is my supervisor and also supporter, for talking to me caringly as a friend rather than simply a teacher and I’m very thankful for that. To Vy and Hiệp, sometimes I questioned our friendships, and felt doubtful, but when I look around I always see you guys right there, and I think that’s what matters the most. I’m thankful for this confusing friendship because when I need your supports the most, you guys never fail me, and I really appreciate that. To Nguyên and Chris, you two are my rocks. Thanks for being here with me, for your co-operation in numerous impossible-sounding missions, and for your emotional support. When things are down, you guys have always brought me back to my ground. I would like to send my gratitude to Dr. Jafar Hasan, Dr. Mohammad Al Kobaisi, Dr. Vi Khanh Truong, and Dr. Hooi Jun Ng for their knowledge and assistance in operating various instruments, and techniques. Also, thank you to Veselin ‘Vanya’ Boshkovikj, you are one of the funniest guys I have ever met. You guys made my PhD life more colourful and much easier. Thank you to Dr. James Wang for his assistance in performing SEM experiments. Similarly, I would like to thank Dr. Mark Tobin and Dr. Ljiljana Puskar for helping with our work at the Australian Synchrotron, FTIR beamline; without their expertise, I would not be able to become a regular there. iv A special thanks and gratitude to chú Ngân, Soula, Savithri, Chris, Rebecca and all the laboratory technicians who have helped me throughout the course of this work. Talking to you all made me sometimes forget how tough PhD life can be. To all my friends here at Swinburne, you guys have made my every day more fun and enjoyable. I will never forget our little office where the temperature is always above 30°, with the white board where everyone writes their thoughts. It’s a pity that around the time I write all this, you guys are not around. I would rather say my thankful words out loud individually, but I’m afraid that I’ll in tears before I complete my sentences, so I send my special gratitude here, to Yến, Matt, Kaylass, Shanthi, Phong and Qudsia. To our lovely and handsome dog, Sammy. You are my mascot and on my wallpaper screen; looking at you make my days go by much easier, so if you can understand, I would like to say thanks to you. Especially, thank you to my new and current family. The word by itself says a lot how much you all mean to me. To my new family, I came along and you all took me in with your kindest hearts, treated me as part of the family, giving me support and advice which always touch my heart. To my husband, Dr. Hayden Webb, I don’t know how many words are enough to express my gratitude to you for your endless emotional support, thanks for always being by my side sharing my happiness and motivating me through the toughest times despite my difficult nature. Before being my friend, my husband, you are my senior, my teacher who does not mind to be harsh to me for my improvement. Con muốn gửi những lời cám ơn sâu sắc nhất tới ba, mẹ và bé Ngân. Con khô khan, nhưng con hy vọng mọi người hiểu được là con mang ơn mọi người như thế nào. Sự hy sinh thầm lặng của mẹ luôn là động lực vực con đứng dậy trong ư4ng tháng ngày khó khăn.
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