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Succinic Acid Production Using Metabolically Engineered Escherichia Coli

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Succinic Acid Production Using Metabolically Engineered Escherichia Coli 2007:12 LICENTIATE T H E SI S Succinic acid production using metabolically engineered Escherichia coli Christian Andersson Luleå University of Technology Department of Chemical Engineering and Geosciences Division of Biochemmical and Chemical Process Engineering 2007:12|: 102-1757|: -c -- 07⁄12 -- Succinic acid production using metabolically engineered Escherichia coli Christian Andersson Division of Biochemical and Chemical Process Engineering Department of Chemical Engineering and Geosciences Luleå University of Technoogy S-971 87 Luleå February 2007 Abstract The prospects of peak oil, climate change and the dependency of fossil carbon have urged research and development of production methods for the manufacture of fuels and chemicals from renewable resources (biomass). To date, the primary emphasis has been placed on the replacement of oil for transportation fuels. A highly significant subset of petroleum usage is the production of chemicals, which represents 10-15% of the petroleum usage. White biotechnology, also called industrial biotechnology, is a fast evolving technology with a large potential to have a substantial impact on the industrial production of fuels and chemicals from biomass. This work addresses the issue of chemical production by investigating the production of bio-based succinic acid, which can be used in a wide range of applications to replace petroleum based chemicals. Succinic acid can be produced by fermentation of sugar by a number of organisms; one is Escherichia coli (E. coli). It is known that E. coli under anaerobic conditions produces a mixture of organic acids. In order to obtain a cost-effective production it is necessary to metabolically engineer the organism to produce succinic acid in greater yield than the other acids. In the current work, E. coli mutant AFP184 was used. AFP184 originates from a near wild type strain, the C600 (ATCC 23724), which can ferment both five and six carbon sugars and has mutations in the glucose specific phosphotransferase system (ptsG), the pyruvate formate lyase system (pfl) and in the fermentative lactate dehydrogenase system (ldh). The previous studies using different organisms have all used cultivation mediums supplemented to some degree with different nutrients like biotin, thiamine and yeast extract. In order to apply the technology to large scale, production must be cost-effective and it is important to minimise the use of additional supplements. The first part of this work aimed to investigate the fermentation characteristics of AFP184 in a medium consisting of corn steep liquor, inorganic salts and different sugar sources without supplementation of other additional nutrients. It addresses questions regarding the effect of different sugars on succinic acid kinetics and yields in an industrially relevant medium. In order to gain a sustainable production of succinic acid from biomass feedstocks (sugar from biomass) it is important to investigate how well the organism can utilise different sugars in the biomass. The sugars studied were sucrose, glucose, fructose, xylose and equal mixtures of glucose- fructose and glucose-xylose at a total initial sugar concentration of 100 g L-1. AFP184 was able to utilise all sugars and sugar combinations except sucrose for biomass generation and succinate production. Using glucose resulted in the highest yield, 0.83 (g succinic acid per g sugar consumed anaerobically). Fructose resulted in a yield of 0.66 and xylose of 0.5. Using a high i initial sugar concentration made it possible to obtain volumetric productivities of almost 3 g L- 1h-1, which is above estimated values for feasible economic production. Succinic acid production ceased at final concentrations greater than 40 g L-1. In order to further increase succinic acid concentrations, this inhibitory effect was studied in the second part of the present work. The inhibitory effects can be two-fold including pH-based inhibition and an anion specific effect on metabolism. It has been reported that high concentrations of ammonia inhibit E. coli growth and damage cell membranes. In order to limit toxic and inhibitory effects different neutralising agents were tested. First the use of NH4OH was optimised with respect to fermentation pH and it was found that the best results were obtained at pH 6.5-6.7. Optimal pH was then used with NaOH, KOH, and Na2CO3 as neutralising agents and it was shown that NaOH, KOH, and Na2CO3 neutralised fermentations could reach succinic acid concentrations of 69 and 61 and 78 g L-1 respectively without any significant decrease in succinic acid productivity. It was observed that cells lost viability during the cause anaerobic phase. It resulted in decreasing succinic acid productivities. It is believed that the viability decrease is a combined effect of organic acids concentration and the osmolarity of the medium. The work done in this thesis is aimed towards increasing the economical feasibility of a biochemical succinic acid production. Keywords: Industrial biotechnology, Fermentation, Succinic acid, Escherichia coli, Productivity ii Acknowledgements First of all I would like to thank my supervisor Professor Kris A. Berglund. Your constant good mood and undying enthusiasm is close to contagious. You are never too tired for a discussion be it politics or fermentation technology. Thank you for including me in your team. My deepest gratitude and thankfulness I would like to extend to my secondary supervisor Dr. Ulrika Rova. You taught me the basics of microbiology. Without you there would be no thesis. Your care and resourcefulness are the foundation of our division. Thank you for all the work you have put in. I extend a special thanks to my master thesis worker and fermentation engineer Jonas Helmerius. You came when I needed you the most. It has been a pleasure supervising you. Thank you for all your help. I am also grateful to Josefine Enman, Magnus Sjöblom, David Hodge, and all my friends and colleges at the Department of Chemical Engineering and Geosciences. Working with you guys is great fun. My earlier master thesis workers Andreas Lennartsson, Ksenia Bolotova, and Mario Winkler are all acknowledged. You all did great jobs. I also thank all my students. Our discussions and your curiosity help me to develop. Min närmste vän Ivan Kaic och min bror Fredrik Andersson, ni är speciellt tackade. Ert stöd och er vänskap är ovärderlig. Mina föräldrar Jarl och Margaretha Andersson. Jag har inte ord att beskriva vad ni betyder. Ni är mina förebilder. Mitt rättesnöre. Finally, my love Antonina Lobanova. You came to me. I still cannot believe it is true. You have changed everything. ə ɥɸɛɥɸ ɬɟɛɹ. Luleå 2007, Christian Andersson iii iv List of papers This thesis is based on the work contained in the following papers, referred to in the text by Roman numerals. I Effects of different carbon sources on the production of succinic acid using metabolically engineered Escherichia coli Christian Andersson, David Hodge, Kris A. Berglund, and Ulrika Rova Biotechnology Progress, In press II Impact of neutralising agent and pH on the succinic acid production by metabolically engineered Escherichia coli in dual-phase fermentations Christian Andersson, Jonas Helmerius, David Hodge, Kris A. Berglund, and Ulrika Rova Manuscript v vi Contents INTRODUCTION ..........................................................................................1 PRODUCTION OF BIO-BASED FUELS AND CHEMICALS ..........................................................2 THE INTEGRATED FOREST BIOREFINERY (IFBR) ................................................................4 CURRENT LEVEL OF SUCCINIC ACID PRODUCTION.............................................................7 THEORY ..................................................................................................... 11 BASIS FOR THE EXPERIMENTAL WORK ..............................................................................11 SUGAR METABOLISM IN AFP184 .......................................................................................11 Glucose..............................................................................................................12 Fructose .............................................................................................................16 Xylose ...............................................................................................................16 ACID RESISTANCE, INHIBITION, AND TOXICITY IN ESCHERICHIA COLI..............................16 Energy generation and the chemiosmotic theory ..............................................................16 Background to pH homeostasis..................................................................................17 Organic acid, metabolic uncoupling and anion accumulation...............................................18 Acid resistance systems............................................................................................20 OSMOTIC STRESS IN ESCHERICHIA COLI ...........................................................................23 Osmotic pressure, osmolarity and turgor pressure ............................................................23 The role of compatible solutes in the response of Escherichia coli to osmotic stress ......................25 RESULTS AND DISCUSSION ....................................................................... 29 SUGAR UTILISATION .........................................................................................................29 IMPACT OF THE NEUTRALISING AGENT
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