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Understanding Extracellular Electron Transport of Industrial Microorganisms and Optimization for Production Application

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Understanding extracellular electron transport of industrial microorganisms and optimization for production application Frauke Kracke Dipl.-Ing., Bio-chemical Engineering, Technical University Dortmund, Germany A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2016 School of Chemical Engineering Advanced Water Management Centre Centre for Microbial Electrochemical Systems ABSTRACT Microbial electrosynthesis (MES) and electro-fermentation are novel approaches to increase microbial production by stimulating the metabolism of the cells electrically. The technique is still in its infancy and while already hyped as promising method to convert CO2 or cheap carbon sources and electrical energy into valuable chemicals and fuels, little is known about its true potential. This project uses a combination of in silico and in vivo approaches to gather novel information about the benefits and limitations of microbial electrosynthesis as well as its fundamental mechanisms. Understanding microbial electron transport mechanisms is the key to optimization of any bioelectrochemical technology. Therefore, this work analyses the different electron transport chains that nature offers for organisms such as metal respiring bacteria and acetogens, but also standard biotechnological organisms currently used in bioproduction. Special focus lies on the essential connection of redox and energy metabolism, which is often ignored when studying bioelectrochemical systems. The possibility of extracellular electron exchange at different points in each organism is discussed regarding required redox potentials and effect on cellular redox and energy levels. Key compounds such as electron carriers (e.g. cytochromes, ferredoxins, quinones, flavins) are identified and analysed regarding their possible role in electrode-microbe-interactions. Based on these findings a stoichiometric network analysis is performed analysing the effect of electrical stimulation on the microbial metabolism theoretically. Escherichia coli is used as model organism for production with the aim to identify target processes for MES. For the first time, 20 different valuable products were screened for their potential to show increased yields during anaerobic electrically enhanced fermentation. Surprisingly it was found that an increase in product formation by electrical enhancement is not necessarily dependent on the degree of reduction of the product but rather the metabolic pathway it is derived from. Contrary to the usual assumption a reduced product would always require electron supply by a cathode this study shows that a complex metabolic analysis is needed to identify the overall redox state of each process. A variety of beneficial processes is presented with product yield increases of maximal +36% in reductive and +84% in oxidative fermentations and final theoretical product yields up to 100%. This includes compounds that are already produced at industrial scale such as succinic acid, i lysine and diaminopentane as well as potential novel bio-commodities such as isoprene, para-hydroxybenzoic acid and para-aminobenzoic acid. Furthermore, it is shown that the way of electron transport has major impact on achievable biomass and product yields. The coupling of electron transport to energy conservation could be identified as crucial for most processes. The in vivo approach of this project introduces the development of a standardised reactor platform suitable for reproducible, fully controlled electrically enhanced fermentations. Different organisms that are used in industrial bio-production were screened for their ability of electron uptake: E. coli, Propionibacterium (P.) acidipropionici, P. freudenreichii, Citrobacter werkmanii and Clostridium (C.) autoethanogenum. A growth-related current consumption was monitored for all tested strains, however in most cases the electron uptake was too small compared to substrate uptake to result in significant metabolic changes. An exception is presented by the GRAM-positive acetogen C. autoethanogenum, which shows a considerable metabolic shift from acetate towards lactate and 2,3-butanediol caused by extracellular electron supply. This is the first report of electro- activity of the close relative to C. ljungdahlii. In heterotrophic fermentations, extracellular electron supply cut acetate production by more than half while production of lactate and 2,3-butanediol increased thirty-five fold and three fold, respectively. Interestingly this metabolic response crucially depends on the redox potential at which the electrons are supplied, which is proven by the use of different mediator molecules. In agreement with the findings from the in silico study, this again is an indication for the importance of the metabolic pathway by which electrons enter the cellular metabolism for the success of microbial electrosynthesis. This work applies a powerful metabolic modelling tool and studies electron transport mechanisms in the industrial alcohol producing Clostridium autoethanogenum. As such it adds an important piece of fundamental understanding of microbial electron transport possibilities to the research community and will help to optimize and advance bio- electrochemical techniques beyond the level of lab-scale studies. ii iii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. iv Publications during candidature Peer reviewed papers: - Kracke, F., and Krömer, J. O. (2014). Identifying target processes for microbial electrosynthesis by elementary mode analysis. BMC Bioinformatics, 15(1), 410. doi:10.1186/s12859-014-0410-2 - Harnisch, F., Rosa, L.F.M., Kracke, F., Virdis, B., and Krömer, J.O. (2015). Electrifying White Biotechnology: Engineering and Economic Potential of Electricity- Driven Bio-Production. ChemSusChem 8, 758-766. doi: 10.1002/cssc.201402736 Featuring a cover story and image: doi: 10.1002/cssc.201403199 - Kracke, F., Vassilev, I., and Krömer, J.O. (2015). Microbial electron transport and energy conservation – the foundation for optimizing bioelectrochemical systems. Frontiers in Microbiology 6. doi: 10.3389/fmicb.2015.00575 Peer reviewed conferences: Kracke, F., & Krömer, J. O.; “Understanding benefits and limitations of Microbial Electrosynthesis: An elementary mode analysis of microbial production during electrically enhanced fermentation.”, 4TH INTERNATIONAL FUEL CELL CONFERENCE, September 2013 Cairns, Australia, oral presentation Averesch, K. F. G. , Kracke, F., Lekieffre N., Krömer, J. O.; “Parallel reactor system for the study of cathodic bioprocesses.”, 4TH INTERNATIONAL FUEL CELL CONFERENCE, September 2013 Cairns, Australia, poster presentation Kracke, F., and Krömer, J.O.; “Making the connection: Metabolic pathway study of microbial systems for electrosynthesis”, 5TH INTERNATIONAL MEETING ON MICROBIAL ELECTROCHEMISTRY AND TECHNOLOGIES, October 2015 Tempe, AZ, America, poster presentation v Publications included in this thesis - Kracke, F., & Krömer, J. O. (2014). Identifying target processes for microbial electrosynthesis by elementary mode analysis. BMC Bioinformatics, 15(1), 410. doi:10.1186/s12859-014-0410-2 This publication was slightly modified to fit the thesis and was incorporated as chapter 4.2. Contributor Statement of contribution Frauke Kracke (Candidate) Designed study (60%) Conducted the experiments (80%) Wrote the paper (100%) Jens O. Krömer Designed study (40%) Conducted the experiments (20%) Critically reviewed and edited paper (100%) - Kracke, F., Vassilev, I., and Krömer, J.O. (2015). Microbial electron transport and energy conservation – the foundation for optimizing bioelectrochemical systems. Frontiers in Microbiology 6. doi: 10.3389/fmicb.2015.00575 This publication was slightly modified to fit the thesis and was incorporated as chapter 4.1. Contributor Statement of contribution Frauke Kracke (Candidate) Designed the study (50%) Performed calculations (100%) Wrote the paper (70%) Igor Vassilev Designed the study (20%) vi Wrote the paper (30%) Jens O. Krömer Designed the
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