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Synechococcus Elongatus PCC7942 for Photo-Bioelectricity Generation

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Synechococcus Elongatus PCC7942 for Photo-Bioelectricity Generation Strategies to enhance extracellular electron transfer rates in wild-type cyanobacterium Synechococcus elongatus PCC7942 for photo-bioelectricity generation Arely Carolina Gonzalez Aravena Department of Chemical Engineering and Biotechnology University of Cambridge This dissertation is submitted for the degree of Doctor of Philosophy September 2017 Churchill College Strategies to enhance extracellular electron transfer rates in wild-type cyanobacterium Synechococcus elongatus PCC7942 for photo-bioelectricity generation Arely Carolina Gonzalez Aravena Abstract The aim of this thesis is to enhance the extracellular electron transfer rates (exoelectrogenesis) in cyanobacteria, to be utilised for photo-bioelectricity generation in biophotovoltaics (electrochemical cell). An initial cross comparison of the cyanobacterium Synechococcus elongatus PCC7942 against other exoelectrogenic cultures showed a hindered exoelectrogenic capacity. Nonetheless, in mediatorless biophotovoltaics, it outperformed the microalgae Chlorella vulgaris. Furthermore, the performance of S. elongatus PCC7942 was improved by constructing a more efficient design (lower internal resistance), which was fabricated with carbon fibres and nitrocellulose membrane, both inexpensive materials. To strategically obtain higher exoelectrogenic rates, S. elongatus PCC7942 was conditioned by iron limitation and CO2 enrichment. Both strategies are novel in improving cyanobacteria exoelectrogenesis. Iron limitation induced unprecedented rates of extracellular ferricyanide reduction (24-fold), with the reaction occurring favourably around neutral pH, different to the cultural alkaline pH. Iron limited cultures grown in 5% and 20% CO2 showed increased exoelectrogenic rates in an earlier stage of growth in comparison to air grown cultures. Conveniently, the cultural pH under enriched CO2 was around neutral pH. Enhanced photo-bioelectricity generation in ferricyanide mediated biophotovoltaics was demonstrated. Power generation was six times higher with iron limited cultures at neutral pH than with iron sufficient cultures at alkaline pH. The enhanced performance was also observed in mediatorless biophotovoltaics, especially in the dark phase. Exoelectrogenesis was mainly driven by photosynthetic activity. However, rates in the dark were also improved and in the long term it appeared that the exoelectrogenic activity under illumination tended to that seen in the dark. i Proteins participating in iron uptake by an alleged reductive mechanism were overexpressed (2-fold). However, oxidoreductases in the outer membrane remain to be identified. Furthermore, electroactive regions in biofilms of S. elongatus PCC7942 were established using cyclic voltammetry. Double step potential chronoamperometry was also successfully tested in the biofilms. Thus, the electrochemical characterisation of S. elongatus PCC7942 was demonstrated, implying that the strategies presented in this thesis could be used to screen for cyanobacteria and/or electrode materials to further develop systems for photo-bioelectricity generation. ii In memory of my father who always believed in me. iii Preface The work described in this PhD thesis was carried out in the Department of Chemical Engineering and Biotechnology at the University of Cambridge, between October 2013 and September 2017. This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except as declared and specified in the text. It is not substantially the same as any that I have submitted, or, is being concurrently submitted for a degree or diploma or other qualification at the University of Cambridge or any other University or similar institution. I further state that no substantial part of my dissertation has already been submitted, or, is being concurrently submitted for any such degree, diploma or other qualification at the University of Cambridge or any other University or similar institution. This thesis contains 64,336 words and 99 figures. Arely Carolina Gonzalez Aravena Department of Chemical Engineering and Biotechnology University of Cambridge September 2017 iv Acknowledgments I wish to acknowledge my supervisor Dr Adrian Fisher for all his support during my time as a PhD candidate. I also wish to acknowledge Dr Kamran Yunus for all his help and guidance. I wish to acknowledge my family. To my husband Damian Brogden for his love and unconditional support, to my mother Nieves Aravena for always being there for me, to my brother Werner Gonzalez for being always a friend, and to the memory of my father Werner Gonzalez for being the inspiration he was for me. I would like to thank my colleagues in the CREST group, especially my good friend Aazraa Oumayyah for the time shared, help and constant support. Also, to my good friends Antonio del Rio, Dongda Zhang, Fabio Fiorelli, Hassan Alderazi, Jana Weber and Parminder Kaur Heer, for their help and friendship. I would like to thank my collaborators in NTU Singapore for helping me to carry out some of the work in this thesis. Also, to the staff in electronics, mechanical workshop, stores and technicians in the Department of Chemical Engineering and Biotechnology. Finally, I would like to acknowledge Conicyt Becas Chile and Cambridge Trust for the financial support I received to pursue my PhD studies. v Contents Abstract …….. ........................................................................................................................................... i Preface …….. ........................................................................................................................................... iv Acknowledgments ................................................................................................................................... v Contents …….. ........................................................................................................................................... vi Glossary …… ........................................................................................................................................... xi Nomenclature ...................................................................................................................................... xiii Acronyms …. ..........................................................................................................................................xvi Chapter 1 Introduction ........................................................................................................................ 1 1.1 Bioenergy and photosynthetic bioprocesses .......................................................................... 2 1.2 Bioelectrochemical systems .................................................................................................... 4 1.3 Extracellular electron transfer: exoelectrogenesis ................................................................. 7 1.4 Electrochemical characterisation of exoelectrogenic microorganisms .................................. 9 1.4.1 Electrochemical reactions at the electrode interface ..................................................... 9 1.4.2 Electrocatalysis by microorganisms .............................................................................. 15 1.4.3 Cyclic voltammetry ........................................................................................................ 16 1.4.4 Potential step chronoamperometry ............................................................................. 20 1.4.5 Electrochemical characterisation of microorganisms ................................................... 23 1.5 Microbial bioelectrochemical cells for bioelectricity generation ......................................... 25 1.5.1 Electrochemical cell theory ........................................................................................... 26 1.5.2 Electrochemical cell characterisation ........................................................................... 28 1.5.3 Microbial fuel cells ........................................................................................................ 32 1.5.4 Photo-microbial fuel cells ............................................................................................. 33 1.5.5 Biophotovoltaics ........................................................................................................... 35 1.6 Biophotovoltaics operational conditions .............................................................................. 37 1.6.1 Light ............................................................................................................................... 37 vi 1.6.2 Temperature ................................................................................................................. 38 1.6.3 Cultural pH .................................................................................................................... 38 1.6.4 Media conductivity ....................................................................................................... 39 1.6.5 Mediator concentration ................................................................................................ 39 1.6.6 Nutrients ....................................................................................................................... 40 1.6.7 CO2 ................................................................................................................................ 40 1.6.8 Biomass ........................................................................................................................
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