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The Mechanisms of Extracellular Electron Transfer

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The Mechanisms of Extracellular Electron Transfer The mechanisms of extracellular electron transfer Christy Ann Grobbler Bachelor of Science (Hon I) The University of Queensland, Brisbane, Australia A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2015 School of Chemical Engineering Advanced Water Management Centre 1 Abstract In bioelectrochemical systems (BESs) microbial activity facilitates electricity generation and product synthesis. Using the microbial process of extracellular electron transfer (EET) Shewanella and Geobacter species can respire using a solid terminal electron acceptor, such as an anode in BES. Study of these microorganisms and how they behave at the molecular level is important for shining light on geomicrobial processes and development of BES. Through the use of molecular and electrochemical techniques, this PhD thesis will focus on the molecular mechanisms employed by bacterial biofilms on the anode of a BES, specifically Shewanella oneidensis MR-1 and Geobacter sulfurreducens DL-1. The physiology of these microorganisms appears to be directly associated with the operational conditions of the BES. The application of electrochemical and molecular studies enables the comparison and understanding of the cellular response to the BES operation, in particular on how they respond to changes in the anode potential. Quantitative proteomics from low biomass, biofilm samples is not well documented. The first objective of this thesis was to show the successful use of SWATH-MS for quantitative proteomic analysis of a microbial electrochemically active biofilm of Shewanella oneidensis MR-1. After growth at different potentials (+0.5 V, 0.0 V & -0.4 V vs. Ag/AgCl), biofilm proteins were extracted from anodes for proteomic assessment. SWATH-MS analysis identified 704 proteins, and quantitative comparison was made of those associated with tricarboxcylic acid (TCA) cycle. Metabolic differences detected between the biofilms suggested a branching of the S. oneidensis TCA cycle when grown at the different electrode potentials. In addition, the higher abundance of enzymes involved in the TCA cycle at higher potential indicated an increase in metabolic activity. This objective demonstrated SWATH-MS as a suitable method for studying differences between biomass limited biofilm samples. Subsequently, SWATH-MS and electrochemical methods were used to characterize anodic biofilms of S. oneidensis MR-1 and G. sulfurreducens DL-1. Experiments were conducted at the different electrode potentials of +0.5 V, 0.0 V and -0.4 V or at +0.1 V and +0.6 V for S. oneidensis and G. sulfurreducens respectively. SWATH-MS analysis revealed different strategies of adaption to changes in potential for both microorganisms, with S. oneidensis showing an increase in the relative abundance of its EET cytochromes with increased potential. In addition, these findings support the model that S. oneidensis nanowires are extensions of the outer membrane. Conversely, the majority of EET cytochromes quantified for G. sulfurreducens showed little or no significant change in relative abundance in response to electrode 2 potential. These results suggest S. oneidensis has greater adaptability in its regulation of EET cytochromes compared to G. sulfurreducens. Proteomic, bioelectrochemical and UV- HPLC methods, confirm the involvement and dominance of mediated electron transfer in biofilms of S. oneidensis respiring with an electrode. Furthermore, the relative higher abundance of a riboflavin biosynthesis protein, suggested the involvement of flavins in the EET of biofilms of G. sulfurreducens. Biofilms of G. sulfurreducens grown at the highly oxidative potential of +0.6 V, showed indications of oxidative stress, with lower current production, lower bioelectrochemical signals, and the presence of certain cellular protection mechanisms. Furthermore, similarities between the species were detected, with an increase in the relative abundance of TCA cycle proteins observed with higher rates of EET. In summary, this PhD thesis provides evidence that SWATH-MS is a reliable method to observe changes in the relative abundance of proteins in anodic biofilms of S. oneidensis and G. sulfurreducens. Furthermore, it provides insight into regulation of EET proteins, the physiological response to electrode potential, and how these differ between species of dissimilatory metal respiring bacteria. 3 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. 4 Publications during candidature Peer-reviewed papers: Grobbler, C.; Virdis, B.; Nouwens, A.; Harnisch, F.; Rabaey, K.; Bond, P.L. Use of SWATH mass spectrometry for quantitative proteomic investigation of Shewanella oneidensis MR-1 biofilms grown on graphite cloth electrodes. SYST APPL MICROBIOL. 2014, DOI: 10.1016/j.syapm.2014.11.007 Conference presentations: Grobbler, C.; Virdis, B.; Nouwens, A.; Harnisch, F.; Rabaey, K.; Bond, P.L. Effect of the anodic potential in the extracellular electron transfer capability of Shewanella oneidensis MR-1. Australian Society for Microbiology 2012 Annual Scientific Meeting, 1 to 4 July 2012. Brisbane (Australia). (Poster presentation) Grobbler, C.; Virdis, B.; Nouwens, A.; Harnisch, F.; Rabaey, K.; Bond, P.L. Molecular mechanisms of extracellular electron transfer. The University of Queensland Postgraduate Engineering Conference. 3rd of June 2013. Brisbane (Australia) (Oral presentation) Grobbler, C.; Virdis, B.; Nouwens, A.; Harnisch, F.; Rabaey, K.; Bond, P.L. Effect of the anodic potential in the extracellular electron transfer capability of Shewanella oneidensis MR-1. 4th International Microbial Fuel Cell Conference. 1 to 4 September 2013. Cairns (Australia). (Oral presentation) Grobbler, C.; Virdis, B.; Nouwens, A.; Harnisch, F.; Rabaey, K.; Bond, P.L. Quantitative proteomic analysis from biomass limited electroactive biofilms of Shewanella oneidensis MR-1 through SWATH-MS. 15th ISME International Symposium on Microbial Ecology. 24 to 29 August 2014. Seoul (South Korea). (Oral presentation) 5 Publications included in this thesis Grobbler, C.; Virdis, B.; Nouwens, A.; Harnisch, F.; Rabaey, K.; Bond, P.L. Use of SWATH mass spectrometry for quantitative proteomic investigation of Shewanella oneidensis MR-1 biofilms grown on graphite cloth electrodes. SYST APPL MICROBIOL. 2014, DOI: 10.1016/j.syapm.2014.11.007 This paper has been modified and included as part of sections 4.1.1 and 5.1. The original paper is attached as Appendix A. Contributor Statement of contribution Christy Grobbler (Candidate) Designed experiments (60%) Conducted experiments (100%) Performed SWATH data analysis (95%) Wrote the paper (100%) Bernardino Virdis Designed experiments (20%) Edited paper (20%) Amanda Nouwens Operation of mass spectrometer (100%) Assisted with SWATH data analysis (5%) Edited the paper (5%) Falk Harnisch Designed experiments (5%) Edited the paper (10%) Korneel Rabaey Designed experiments (5%) Edited the paper (5%) Philip L. Bond Designed experiments (10%) Edited the paper (60%) 6 Contributions by others to the thesis This thesis includes the reporting of some important contributions made by other researchers that I have collaborated with throughout the duration of my PhD. These contributions are acknowledged as follows: Prof. Korneel Rabaey (Ghent University) and Dr. Bernardino Virdis (AWMC, UQ), who assisted with the set up and design of the bioelectrochemical systems and experiments. Dr. Amanda Nouwens, from the School of Chemical and Molecular Biosciences (SCMB, UQ) for assistance with proteomic procedures and the operation of the mass spectrometer, as well as initial interpretation of proteomic spectra. Statement of parts of the thesis submitted to qualify for the award of another degree None. 7 Acknowledgements My PhD has been a long and rewarding journey and one that could have never been completed on my own. First, I would like to thank my principle advisor Dr. Phil Bond who has guided me through both my honours and PhD research projects. No matter what the problem or question, I could always come
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