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An In-Depth Biochemical Analysis of Spider and Silkworm Silk

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An In-Depth Biochemical Analysis of Spider and Silkworm Silk Unravelling the secrets of silk: an in-depth biochemical analysis of spider and silkworm silk Hamish Cameron Craig A thesis in fulfilment of the requirements for the degree of Doctor of Philosophy School of Biological, Earth and Environmental Sciences Evolution and Ecology Research Centre UNSW February 2019 THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: Craig First name: Hamish Other name/s: Cameron Abbreviation for degree as given in the University calendar: PhD School: School of Biological, Earth and Environmental Sciences Faculty: Faculty of Science Title: Unravelling the secrets of silk: a detailed examination of silk biology and structure Abstract: Silk is a protein-based biopolymer produced by many different invertebrate species from amphipods to spiders. Its incredible material properties, biocompatibility and antimicrobial properties make it one of the most desirable natural fibres in the race for new materials, with major potential impacts in everything from biomedical research to its aerospace applications. Although silk has been studied in detail since the latter part of the 20th century the field is still unable to produce truly comparable synthetics due to the complexity of biological factors involved in influencing silks properties. The major focus of this thesis is examining biological and structural factors that impact silk properties within spiders and silkworms. To examine this, I analysed silk across many scales from phylogenetic trends in amino acid composition and material properties, down to the Nano-scale examining the impacts of molecular structure, pioneering new methods of silk analysis through utilisation of dynamic nuclear polarization (DNP) solid-state nuclear magnetic resonance (ssNMR) spectroscopy. Using a comparative meta-analysis, I found that within spiders MaSp composition is a major influencing factor broadly across phylogeny and that glycine and serine concentration have a more influential impact than previously thought, whilst confirming the importance of proline in influencing silks elastic properties. I explore the inconsistency and spread of isotopically labelled alanine within spider’s silk and further our understanding of metabolic pathways into silk proteins and silk structure. I then provide and examine the efficacy of an alternative to isotopic labelling, DNP ssNMR, which reveals unprecedented detail into silks molecular structure, boasting a > 50 fold signal enhancement allowing determination of the structural role of lower abundance amino acids like arginine and revealing the presence of the first known example of a post-translational modified amino acid hydroxyproline within silk. lastly, I explore the major implications of hitherto undocumented voids found within native silkworm silks, the molecular structural influences that help create them, their impact on mechanical property measurements and potential development and utilisation ecologically improving the insulative properties of their cocoons. Ultimately, whilst revealing invaluable new information and methods for the silk field to help it towards its goal of producing comparable bio-mimetics, this thesis highlights the need for a biologically minded and holistic study of biomaterials such as silk to understand all the factors that help organisms achieve such incredible and complex materials. Declaration relating to disposition of project thesis/dissertation I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses only). Signature Witness Signature Date The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use. Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and require the approval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: Originality Statement ‘I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged.’ Signed Date Authenticity Statement ‘I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. No emendation of content has occurred and if there are any minor variations in formatting, they are the result of the conversion to digital format.’ Signed Date Copyright Statement ‘I hereby grant the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all proprietary rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstract International (this is applicable to doctoral theses only). I have either used no substantial portions of copyright material in my thesis or I have obtained permission to use copyright material; where permission has not been granted, I have applied/will apply for a partial restriction of the digital copy of my thesis or dissertation.' Signed Date INCLUSION OF PUBLICATIONS STATEMENT UNSW is supportive of candidates publishing their research results during their candidature as detailed in the UNSW Thesis Examination Procedure. Publications can be used in their thesis in lieu of a Chapter if: • The student contributed greater than 50% of the content in the publication and is the “primary author”, ie. the student was responsible primarily for the planning, execution and preparation of the work for publication • The student has approval to include the publication in their thesis in lieu of a Chapter from their supervisor and Postgraduate Coordinator. • The publication is not subject to any obligations or contractual agreements with a third party that would constrain its inclusion in the thesis Please indicate whether this thesis contains published material or not. This thesis contains no publications, either published or submitted for publication (if this ☐ box is checked, you may delete all the material on page 2) Some of the work described in this thesis has been published and it has been documented in the relevant Chapters with acknowledgement (if this box is checked, you ☒ may delete all the material on page 2) This thesis has publications (either published or submitted for publication) incorporated ☐ into it in lieu of a chapter and the details are presented below CANDIDATE’S DECLARATION I declare that: • I have complied with the Thesis Examination Procedure • where I have used a publication in lieu of a Chapter, the listed publication(s) below meet(s) the requirements to be included in the thesis. Name Signature Date (dd/mm/yy) Hamish Craig Postgraduate Coordinator’s Declaration (to be filled in where publications are used in lieu of Chapters) I declare that: • the information below is accurate • where listed publication(s) have been used in lieu of Chapter(s), their use complies with the Thesis Examination Procedure • the minimum requirements for the format of the thesis have been met. PGC’s Name PGC’s Signature Date (dd/mm/yy) Summary of Collaborators’ Contributions In all chapters and manuscripts submitted, and in preparation in which I was listed as first author, I was the primary investigator. This included being the main researcher in data collection, analysis and interpretation, and preparation of the manuscript. Michael Kasumovic and Sean Blamires were my primary supervisors, Aditya Rawal was my main advisor in the training, collection and analysis of NMR involved in this manuscript. Shinichi Nakagawa and Dakota Piorkowski were my main collaborators in the first chapter, Shinichi providing advice and expertise in conducting a meta-analysis and Dakota assisting with the back search and editing the manuscript. James Hook and Marc-Antoine Sani contributed to the access, design, and assisted in data collection of DNP NMR experiments as well as editing the manuscript in Chapter 3. Rangam Rajkhowa provided access to silkworm silk samples and assisted in mechanical property measurements in chapter 4. Yin Yao and Nicholas Ariotti provided training and assistance in the collection and processing of AFM and electron tomography data within chapter 4. Acknowledgements In the words of the late Stephen Hawking “Science is not only a discipline of reason but, also, one of romance and passion”. This is very true of my experience throughout my PhD and I am extremely grateful to be in a position to be able to purse my passions and thirst for gaining and sharing knowledge. Much like a romantic relationship my PhD has had its ups and downs, its hardships and its moments of splendour, but ultimately I’ve emerge a different and more experienced and developed person.
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