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Project Summary METABOLIC ENGINEERING AND PROCESS DEVELOPMENT FOR ENHANCED PROPIONIC ACID PRODUCTION BY PROPIONIBACTERIUM ACIDIPROPIONICI DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By An Zhang, M.S. * * * * * The Ohio State University 2009 Dissertation Committee: Approved by Professor Shang-Tian Yang, Adviser Professor Jeffrey Chalmers Adviser Professor Hua Wang Chemical and Biomolecular Engineering Graduate Program ABSTRACT Propionic acid is an important mold inhibitor. Its salt forms, such as ammonium, sodium, calcium, and potassium salts, are widely used as preservatives for animal feed and human foods. Moreover, propionic acid is an important chemical intermediate, widely used in the synthesis of cellulose fibers, herbicides, perfumes, and pharmaceuticals. Propionate esters are also used as flavors and fragrances. Currently, propionic acid is mainly produced via petrochemical processes. However, concerns over the sustainability of the crude oil supply have generated interest in investigating alternative way to produce propionic acid. Like most organic acid fermentations, the production of propionic acid suffers from low productivity, yield, and final concentration caused by end-product inhibition. The goal of this project was to develop an economical fermentation process for propionic acid production from glucose and processing wastes via integrated metabolic and process engineering approaches. Propionibacterium acidipropionici has been extensively studied for propionic acid production, with acetic acid as the main byproduct. In order to eliminate or reduce acetate formation and increase propionic acid production, gene knock-out through homologous recombination was performed to inactivate acetate kinase gene (Ack) in the acetate formation pathway. Compared to the wild type strain, the mutant (ACK-Tet) ii produced more propionate and less acetate, but the specific growth rate of the mutant was also decreased due to less ATP can be generated from the impaired acetic acid synthesis pathway. The mutant was used in a fibrous bed bioreactor (FBB), which has been shown to have many advantages in microbial fermentation, to further improve propionic acid production from glucose. The results showed that the maximum theoretical propionic acid yield of ~0.54 g/g glucose could be achieved. In fed-batch FBB fermentation, the final propionic acid concentration reached ~104 g/l, which was 43% higher than the highest concentration (~72 g/l) previously reported. Clearly, the bacteria in the FBB had adapted and acquired a higher tolerance to propionic acid. A growth kinetics experiment showed that the adapted mutant from the FBB was ~10 times less sensitive to propionic acid inhibition. The increased acid tolerance was partially attributed to increased expression of H+-ATPase, which plays a key role in proton pumping and maintaining the intracellular pH. Furthermore, after adaptation in the FBB, the ACK-Tet mutant recovered its specific growth rate to the same level as that of its parent wild-type strain. Besides the final concentration of propionic acid in the fermentation broth, the P/A ratio (propionic acid vs. acetic acid) is another key factor affecting downstream purification and the overall production cost of propionic acid. Many prior studies have indicated that the oxidation level of the carbon source can determine the metabolic flux distribution in propionic acid fermentation. In general, the lower the oxidation level of the carbon source is, the higher the P/A ratio can be obtained due to the intracellular iii NADH/NAD+ balance. Glycerol is thus an attractive substrate for the production of reductive chemicals (e.g., H2, ethanol, and propionic acid) because of its low oxidation state. There are also abundant supplies of low-cost glycerol as a waste product from the biodiesel industry. P. acidipropionici could use glycerol for growth and propionic acid production, with a high yield of 0.71 g/g glycerol, which was ~30% higher than that from glucose (0.55 g/g glucose). In addition, almost no acetic acid was produced from glycerol; the acetate yield was only 0.03 g/g glycerol (vs. 0.1 g/g glucose). Thus, glycerol fermentation produced a high-purity propionic acid with the propionic acid to acetic acid ratio of ~24 (vs. ~5 from glucose fermentation), facilitating the recovery and purification of propionic acid from the fermentation broth by simple solvent extraction. The highest propionic acid concentration obtained from glycerol fermentation was ~106 g/l, which was 2.5 times of the maximum concentration of ~42 g/l reported in the literature. Moreover, a stoichiometric metabolic model was set up based on the NADH/NAD+ balance and maximum ATP production. The trend predicted by the model fitted the experimental data very well. - The effects of CO2 (HCO3 ) on cell growth and acids production from glycerol were studied. The productivity of propionic acid in glycerol fermentation with CO2 - - (HCO3 ) reached 2.94 g/l/day, which was markedly higher than that without CO2 (HCO3 ) (1.56 g/l/day). However, the propionic acid yield was decreased slightly from 0.77 to - 0.67 g/g glycerol due to the higher biomass production when CO2 (HCO3 ) was iv supplemented in the media. Meanwhile, the yield and productivity of succinate increased 81% and 280%, respectively, suggesting a significant increase in the Wood-Werkman cycle rate that could be attributed to the increased activities of key enzymes (e.g. phosphoenolpyruvate carboxylase and propionyl CoA transferase) stimulated by CO2 - (HCO3 ). Propionyl-CoA:succinate CoA transferase (CoA T, EC# 2.8.3.- ) catalyzes the rate-limiting step in the propionic acid formation pathway. The genome of Propionibacterium acidipropionici ATCC 4875 was sequenced by 454 sequencing and annotated. The CoA transferase gene was identified in the 454 genome sequence database, and was obtained by PCR amplification and then inserted into an expression vector (pET-CoA). With IPTG induction, the CoA transferase gene was expressed in Escherichia coli BL21 (DE3) under both aerobic and anaerobic conditions. However, due to high sensitivity to oxygen, P. acidipropionici CoA transferase activity was only observed in the crude extract of BL21 (DE3) harboring pET-CoA grown anaerobically. In addition, a consensus Shine-Dalgarno sequence was found four bases upstream of the AUG codon and two inverted repeat regions were located at the downstream of the TGA stop codon. The amino acid alignment of the P. acidipropionici propionyl-CoA:succinate CoA transferase with other reported CoA transferases illustrated the presence of conserved sites in the amino acid sequence for CoA binding. v Dedicated to my parents vi ACKNOWLEDGMENTS My grateful acknowledgment goes to my advisor, Dr. Shang-Tian Yang, for his invaluable guidance, patience, kindness and support throughout my graduate study. I have benefited a lot from his expertise in science, deep insights in our research as well as his great personality. I wish to thank Dr. Jeffrey Chalmers and Dr. Hua Wang for their time serving on my committee and their valuable inputs to my research project. I want to give my sincere thanks and regards to all the previous and current laboratory members, especially Dr. Supaporn Suwannakham, Dr. Anli Ouyang, Dr. Robin Ng, Dr. Xiaodong Tong, Dr. Xiaoying Liu and Shin-Chwen Wang for their support, encouragement and friendship. I benefited a lot from discussions with them and sharing the knowledge on my research. I am grateful to have the privilege of working with them. Financial supports from the University Fellowship, the Presidential Fellowship of Graduate School, and the Alumni Grants for Graduate Research and Scholarship (AGGRS) to this work are also acknowledged. Finally I wish to thank my parents and my wife for their unconditional love and support, all the other family members and all my friends, for their encouragement and believing in me. vii VITA Nov. 26, 1974…………………………………….. Born-Hebei, P.R. China Jul.1997…………………………………………... B.S. Biochemical Engineering, East China Univ. of Sci. & Technol. Shanghai, China Jul. 2002………………………………………….. M.S. Biochemical Engineering, East China Univ. of Sci. & Technol. Shanghai, China 2004-2005…………………………………….... University Fellow the Ohio State University 2005-2007……………………………………..... Graduate Research Associate Chemical & Biomolecular Engineering the Ohio State University 2007-2008……………………………………..... Presidential Fellow Graduate School the Ohio State University PUBLICATIONS 1. Zhang A, Wu H-Z, Zhou X-F, Zhang H-Z, Zhang S-L. 2002, Cloning of the ddsA gene from Gluconobacter oxydans and its expression in E. coli, J. East China Univ. of Sci. & Tech., 28: 321-325. 2. Ouyang A, Bennett P, Zhang A, Yang ST, 2007. Affinity chromatographic separation of secreted alkaline phosphatase and glucoamylase using reactive dyes, Process Biochemistry, 42:561 569. FIELDS OF STUDY Major Field: Chemical Engineering Specialty: Biochemcial Engineering viii TABLE OF CONTENTS Page Abstract. ii Dedication . vi Acknowledgments. vii Vita . viii List of Figures . xvi List of Tables. xx Chapters: 1. Introduction . 1 2. Literature Review. 12 2.1 Propionic acid fermentation . .. 12 2.1.1 Microorganisms. 12 2.1.2 Propionic acid. 14 2.1.3 Fermentation processes. 17 2.1.3.1 State of the art. .. 17 2.1.3.2 Improved fermentation processes with inexpensive media. 18 2.1.3.3 Process improvement in propionic acid yield. .. 21 2.1.3.4 Process improvement in propionic acid productivity. 23 2.1.3.5 Process improvement in final propionic acid concentration. 24 2.1.3.6 Process optimization by mathematical models. 25 ix 2.2 Immobilized cell fermentation. 25 2.2.1 Immobilized cell physiology. 25 2.2.2 Immobilized cell bioreactor. .. 27 2.2.3 Immobilized cell fermentation. .. 28 2.3 Metabolic engineering of P. aicidipropionici. 29 2.3.1 State of the art. 29 2.3.2 Metabolic flux analysis of Propionibacterium . 30 2.3.3 Genetic engineering of Propionibacteria . 32 2.3.3.1 Dicarboxylic acid pathway in Propionibacteria . 32 2.3.3.2 Genetic manipulation for flux redistribution in the fermentation pathway.
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