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The Emergence of Nucleic Acids in an Iron-Sulphur World

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The Emergence of Nucleic Acids in an Iron-Sulphur World Cardiff University School of Earth, Ocean and Planetary Sciences THE EMERGENCE OF NUCLEIC ACIDS IN AN IRON-SULPHUR WORLD By Bryan Hatton Thesis submitted for the Degree of Philosophiae Doctor September 2007 UMI Number: U585139 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. Dissertation Publishing UMI U585139 Published by ProQuest LLC 2013. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 DECLARATION This work has not previously been accepted in substance for any degree and is not concurrently submitted in candidature for any degree. Signed . { 3 3 ...................(candidate) Date STATEMENT 1 This U ^j^s^being submitted in partial fulfillment of the requirements for the degree of Signed (3. r. 3 3 3 ^ 3 ^ ..............(candidate) STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. Signed 33. (candidate) D a te <3? STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan, and for the title and summary to be made available to outside organisations. Signed . 3 * . ......................(candidate) Date ..... STATEMENT 4: PREVIOUSLY APPROVED BAR ON ACCESS I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loans after expiry of a bar on access previously approved by the Graduate Development Committee. Signed ... .33^.3333^3f^ .................. (candidate) D a,e r Abstract One hypothesis for the origin of life suggests that life emerged in a hydrothermal mineral assemblage containing sulphides and hydroxides. The research reported in this thesis shows that these minerals interact with nucleic acid polymers. This has two consequences. Firstly, metal sulphides, particularly iron sulphides, cause the scission of DNA and thus the survival of DNA in this environment is improbable. On the other hand, the reactions at low concentrations could lead to rapid mutations of DNA-like molecules and thus would have affected its evolution. These reactions also have biochemical consequences. For DNA to retain its function as the hereditary molecule it needs to be separated from concentrations of FeS. This also suggests that the results of the molecular ecology of sulfide-rich environments might be affected by reaction with iron sulphides. The effect that these nanoparticulate sulphides have had on the emergence and survival of nucleic acid polymers has been investigated through plasmid electrophoresis and UV-Vis spectrometry. Metal sulphides interact with DNA in two ways: scission of the DNA backbone and binding with sulphide particles. Treatment of pDNA with FeS, CuS, Fe(II), and Cu(II) breaks the ribo-phosphate backbone of the DNA molecule. This occurs through sulphur-based free radicals produced through redox reactions between S 2 2' and Fe(II) and Cu(I) ions. Migration of oligomeric DNA in electrophoresis is retarded by FeS, CuS and ZnS which is attributed to the binding of nanoparticulate sulphides to the DNA. DNA, RNA, adenine, deoxyadenosine and deoxyadenosine monophosphate bind to FeS, CuS, ZnS and Fe(II)/Fe(III) hydroxides. This occurs through the nucleobase rather than the phosphate. Longer DNA molecules adsorb more readily than oligomers, RNA or monomers. Thus the hypothesis that iron-sulphide minerals could adsorb and concentrate nucleic acid constituents promoting nucleic acid formation and then polymerisation is supported, although the hypothesis that the phosphate group emerged to allow this binding is not necessary In the absence of sulphide, Fe(II) causes similar effects. Scission of the DNA occurs through hydroxyl radicals produced through a reaction with trace amounts of O2 also DNA adsorbed onto precipitated green rusts (Fe(II)/(III) hydroxides). Sulphide, in the absence of metal ions, induced no effect on DNA. In the absence of redox, transition metals oxyhydroxides adsorb to DNA but do not act to break up the molecule. Therefore, non-redox active metal sulphides, such as zinc, could have provided some of the functionality of iron sulphide especially with regards to nucleic acid formation, but without producing free radicals and therefore, simultaneous nucleic acid destruction. Acknowledgements I would like to thank my supervisors, Professor David Rickard and Professor Andrew Weightman and my pastoral supervisor, Robert Riding for their support, encouragement and advice. I would also like to thank Professor David Knight for useful discussions and support. I would like to thank my colleagues in the Cardiff Sulphide Research Group, Dr Ian Butler, Chloe Heywood, Shanshang Huang, Anthony Oldroyd and Andrew Griffiths for practical assistance and constructive comments. Thanks to Dr Gordon Webster for his assistance and instruction in the molecular biology lab. Many thanks to my fellow PhD students at Cardiff Earth Sciences, both those who welcomed me to the department and those who have joined us more recently, for their friendship, support and so much more, especially, Alan, Cathal, Cat, Dave, Helena, Julia, Lizzie, Martin, Rich, Rhodri, Sarah and Simon. Special thanks go to Paivi, you have been a great source of comfort and joy and I’m not sure if I would have gotten through this without you, although, I am sure it wouldn’t have been as much fun. I am grateful to Asta and Sarah for making me feel at home in Cardiff very quickly, for giving me someone to talk to who wasn’t a geologist and for giving me a relaxing and enjoyable environment to come home to after work. Finally, I would like to thank my family, especially my parents David and Pauline, my brother, Lee and my grandparents for their constant support throughout my education. Contents Abstract i Acknowledgements iii Contents iv Preface ix Chapter 1 Introduction ...................................................................................................1 1. Background ............................................................................................2 2. Project aims ............................................................................................6 3. Explanation of experimental approach ................................................. 8 4. Thesis Summary.....................................................................................10 Chapter 2 The FeS-world origin of life hypothesis: A critical review ..............12 1. Introduction ..........................................................................................13 2. Hydrothermal sulphide minerals...........................................................14 3. Carbon fixation and metabolism in an FeS-world ..........................16 3.1. Pyrite-pulled carbon fixation .............................................17 3.2. Fischer-Tropsch synthesis..................................................19 3.3. Formation of the first carbon-carbon bonds ....................20 3.4. Origins of metabolism ........................................................21 3.5. Pyrite-pulled metabolism ...................................................21 3.6. Autocatalytic carbon cycles: fidelity of replication ....... 25 3.7. Carbon fixation and metabolism in FeS compartments..26 3.8. Conclusion of carbon-fixation and proto-metabolsim ...28 4. Evolution from an Autocatalytic Cycle ............................................29 5. Origin of cellularisation ....................................................................... 33 5.1. Wachtershauser’s semi-cellular structures...................... 35 5.2. Pre-formed inorganic cells ................................................ 40 5.2.1. Self cotained redox ..............................................42 5.2.2. Evidence for FeS compartments ........................ 42 5.3. Conclusion of cellularisation section ..................................43 6. Origin of nucleic acids ....................................................................... 44 6.1. Origin of nucleic acid-amino acid interaction in FeS Cells 44 6.2. Genome evolution in an inorganic cell ..............................46 6.3. Conclusion of origin of nucleic acid ..................................50 7. Conditions and Resources in an FeS world .....................................51 7.1. Iron and Sulphur Resources ................................................. 52 8. Conclusions ..........................................................................................54 Chapter 3 An electrophoretic study on the effects of Fe (II) and Fe (III) on plasmid DNA .............................................................................................57 Abstract.........................................................................................................58 1. Introduction .......................................................................................... 58 2. Materials and methods ........................................................................ 61 2.1. Plasmid DNA preparation ....................................................61
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