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研究生：	薛成鳳 Xue, Cheng-Feng
論文名稱：	利用磷酸吡哆醛輔因子工程增強基改大腸桿菌生產高值化學品 Cofactor engineering of pyridoxal 5’-phosphate (PLP) toward high-value chemicals production in genetic Escherichia coli
指導教授：	吳意珣 Ng, I-Son
學位類別：	博士 Doctor
系所名稱：	工學院 - 化學工程學系 Department of Chemical Engineering
論文出版年：	2022
畢業學年度：	111
語文別：	英文
論文頁數：	183
中文關鍵詞：	磷酸吡哆醛、輔因子工程、賴氨酸脫羧酶、屍胺、5-氨基酮戊酸、4-氨基丁酸、重組大腸桿菌、小球藻、二氧化碳、冷處理、篩選平台
外文關鍵詞：	pyridoxal 5’-phosphate, cofactor engineering, lysine decarboxylase, cadaverine, 5-aminolevulinic acid, 4-aminobutyric acid, recombinant Escherichia colI, Chlorella sorokiniana, carbon dioxide, cold treatment, screening platform
相關次數：	點閱：104 下載：15
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近年來，隨著生物技術的進步和各種基因編輯工具的發展，利用微生物細胞工廠生產化學品取代傳統化學合成的方法廣受關注。生物製程技術不僅有助於減少環境污染，也有助於實現二氧化碳淨零排放。然而，生物製造三個關鍵性能指標：產量、產率和轉化率仍不能滿足工業級放大生產。
輔因子工程被認為是代謝工程的關鍵策略之一。輔因子在多種生物反應中發揮作用，例如影響氧化還原平衡、細胞代謝及促進催化過程。磷酸吡哆醛 (pyridoxal 5’-phosphate, PLP) 是一種多功能性輔因子，已知參與230多種酶反應。然而，當細胞內累積過量的PLP造成氨基酸代謝失衡且抑制細胞生長。因此，構建高通量平台篩選PLP生產的最佳組合達到最優化反應速率與細胞生長的平衡是其中關鍵。
首先，過表達吡哆醛激酶（PdxY 或 PdxK）和吡哆醇/吡哆胺 5'-磷酸氧化酶（PdxH）以生產PLP自足型生物催化劑，發現大腸桿菌BL21以J23100啟動子驅動pdxY時，PLP積累量達到峰值。將PLP自足型生物催化劑應用於體內和體外戊二胺生產，耦合冷激處理的細胞達到121 g/L/h屍胺產率。本研究證明了PLP超級救援途徑中基因可用於細胞內再生PLP且生產高值化學品。另一方面，吡哆醛激酶PdxY整合的大腸桿菌菌株，有利更多碳流入三羧酸循環，同時減少乙酸等副產物，配合優化前體濃度和補料醱酵策略，取得8.21 g/L 的5-氨基乙酰丙酸 (5-ALA) 之光動力癌症藥物。
基質和產物的質傳速率是全細胞觸媒催化效率的關鍵問題。目前使用化學品或表面活性劑處理細胞增加細胞膜通透性，會增加下游純化的難度。因此，本研究通過冷激處理細胞增強細胞通透性用於4-氨基丁酸（GABA）生產。結果在-20℃冷激處理的細胞中，88.6%的谷氨酸脫羧酶（GadB）在催化過程中遷移到細胞間質，酶轉化率增加了2倍，最終經由十次重覆使用全細胞催化，獲得累積產物850 g/L的GABA。但因1 mole GABA生產將排放1 mole二氧化碳，在本研究將反應釋放的二氧化碳排入氫氧化鈉形成碳酸氫鈉，進一步用於培養小球藻Chlorella sorokiniana （CS）及Chlorella vulgaris （CV）。再以自備的GABA加入微藻培養體系中，分別提升生物量和脂質含量1.65倍和1.43倍。
最後，本論文建立了篩選平台Direct Enzymatic Evaluation Platform (DEEP），在CRISPRi介導pdxB基因下調的菌株中，篩選啟動子、基因與PLP生成前體的最適化組合，用於微調細胞內磷酸吡哆醛生產。結果取得PLP最佳模組菌株WJK，不僅可以增強PLP依賴型蛋白產量及活性，如谷氨酸脫羧酶，精氨酸脫羧酶、賴氨酸脫羧酶、5-ALA合成酶等。同時證明了PLP結合點在Ser-His-Lys，是PLP提高蛋白質表達水準的關鍵。
本文完成磷酸吡哆醛輔因子工程用於生產高值化學品，未來可用於加速PLP依賴性蛋白質定向進化。輔因子工程與體外化學生產相結合的技術，是永續工業生物製程可實現二氧化碳淨零排放的新契機。

In recent years, with the advance of biotechnology and a variety of genetic editing tools, scientists have devoted themselves to constructing microbial cell factories and producing chemicals instead of chemical synthesis towards reducing environmental pollution and achieving net-zero carbon dioxide emission. However, the three critical parameters of bioprocess, including titer, productivity rate, and yield, are crucial to satisfying the industrial scale requirements.
Cofactor engineering has been identified as a crucial strategy in metabolic engineering involving abundant biological reactions, especially for influencing redox balance, cellular metabolism, and even promoting the biocatalytic process. Pyridoxal 5’-phosphate (PLP) participates in more than 230 enzymatic reactions as a versatile cofactor. However, the high level of intracellular PLP could inhibit cell growth due to the imbalance of amino acid metabolism. Therefore, a high throughput screening platform to explore the best combination of genetic elements for PLP production is urgent and a concern.
At first, a PLP self-sufficient biocatalyst by expressing the pyridoxal kinase (PdxY or PdxK) and pyridoxine/pyridoxamine 5'-phosphate oxidase (PdxH) is developed. E. coli BL21 harboring pdxY under the J23100 promoter produced the highest level of PLP. Thus, the best cadaverine productivity of 121 g/L/h using PLP self-sufficient biocatalyst was achieved in the permeabilized cells by cold treatment. The results also proved the function of genes in the PLP super-salvage synthesis pathway was highly efficient for PLP regeneration for high-end chemicals production. On the other hand, a pyridoxal kinase PdxY-integrated E. coli strain could drive more carbon flux into the TCA cycle and diminish the byproduct of acetate. Finally, fermentation with optimized precursor and feeding strategies achieved 8.21 g/L of 5-ALA, a photodynamic therapy cancer drug.
The mass transfer rate of substrate and product is the critical problem of whole-cell bioconversion. Previous reports showed that chemicals or surfactants treated on cell has successfully increased cell membrane permeability but introduced the difficulty of downstream purification. Herein, we developed an efficient physical method to enhance cell permeability by cold treatment on whole-cell for 4-aminobutyric acid (GABA) production. It was observed that 88.6% of GadB in the -20oC-treated cells migrated to the periplasm after the biotransformation. Kinetic studies showed that the enzymatic turnover rate of whole cell biocatalysts increased 2-fold after cold treatment. The accumulative 850 g/L of GABA was obtained from a 10-times recycling biocatalyst as one mole of CO2 would be released along with GABA formation. We captured the CO2 by sodium hydroxide and further used it to cultivate microalgae of Chlorella sorokiniana (CS) and Chlorella vulgaris (CV). Meanwhile, the in vitro GABA was fed into the CS cultivation to stimulate biomass and lipid production of 1.65-fold and 1.43-fold, respectively.
Finally, we established a Direct Enzymatic Evaluation Platform (DEEP) to fine-tune pyridoxal 5’-phosphate-dependent proteins' performance using CRISPRi mediated on pdxB. The relevance of decoy PLP-binding proteins with a PLP amplifier for fine-tuning the quantity and quality of diverse enzymes was demonstrated. This platform could enhance the enzymatic activities of 5-aminolevulinic acid synthase, glutamate decarboxylase, lysine decarboxylase, and arginine decarboxylase by approximately two-fold. Finally, we identified the conserved PLP-binding pocket, Ser-His-Lys, which was critical in PLP sponge strain for enhanced protein expression levels.
In conclusion, cofactor engineering of PLP is not limited to accelerating high-level chemical production but also assisting the evolution of PLP-dependent proteins. By coupling cofactor engineering and in vitro chemical production, a new opportunity is afforded to achieve net-zero carbon emissions toward a sustainable industry.

Memorandum On Copyright Claim Or Disclaimer	I
摘要	II
Abstract	IV
致謝	VI
Contents	VII
Lists Of Figures	XII
List Of Abbreviations	XV
Chapter 1  Introduction	1
1   Motivation and purpose	1
2   Research scope in the dissertation	2
Chapter 2	Literature Review	6
1	From the petrochemical industry to the biological process	6
1.1	Environmental concerns and energy problem	6
1.2	Petrochemical production	6
1.3	Beyond petrochemicals: biotechnology for chemicals production	8
2	System biology engineering approaches	9
2.1.	Synthetic biology	11
2.2.	Systems biology	15
2.3.	Metabolic engineering	16
2.4.	Evolutionary engineering	18
3	E. coli as a sustainable platform for chemicals production	19
3.1	Biorefinery	19
3.2	Biofuels	21
3.3	Bulk chemicals	25
3.4	The limitation of industrial chemicals production in E. coli	26
4	Cofactor engineering of pyridoxal 5’-phosphate (PLP)	27
4.1	PLP is a versatile cofactor in biological process	27
4.2	PLP synthesis pathway in E. coli	29
4.3	The challenge for high-level cofactor regeneration	32
5	High-end chemicals production depends on PLP regeneration	32
5.1	Cadaverine	32
5.2	4-aminobutyric acid (GABA)	33
5.3	5-aminoluvlinic acid (5-ALA)	34
6	Enhancement of mass transfer rate for chemicals production	34
6.1	Chemical treatment methods	34
6.2	Physical treatment methods	35
6.3	Improvement of product secretion by expressing an antiporter	36
Chapter 3  Materials And Methods	37
1	Chemicals and materials	37
2	Instruments	41
3	The strains, plasmids and primers used in this thesis.	42
4	Molecular cloning and genetic strain development	47
4.1	Plasmid DNA extraction	47
4.2	Polymerase Chain Reaction (PCR)	47
4.3	Primer phosphorylation and annealing	50
4.4	Restriction enzyme digestion	50
4.5	Gel extraction and PCR purification	51
4.6	Ligation	51
4.7	Heat-shock competent cell preparation	51
4.8	Heat-shock transformation	52
4.9	Gene integration method	52
4.9.1	Gene integration by phage attachment site	52
4.9.2	Gene integration by one-step phage attachment	52
4.9.3	Resistance removal by FLP recombinase	53
5	Cell culture and conditions	53
5.1	Medium used in this study	53
5.2	Cell culture condition	53
6	Protein analysis	53
6.1	Buffer preparation	53
6.2	Sodium Dodecyl Sulfate-Polyacrylamide Gel Electrophoresis (SDS-PAGE) preparation	54
6.3	Sample preparation	54
6.4	SDS-PAGE running program, staining and de-staining method	55
6.5	Quantifying the relative protein concentration on PAGE	55
6.6	Identify the protein identity by tandem mass spectrometer	55
7	Characterization techniques	55
7.1	Scanning Electron Microscopy (SEM) analysis	55
7.2	Determination of plasmid copy number by quantitative PCR (qPCR)	56
7.3	Determination of biomass	57
8	High-performance liquid chromatography (HPLC) analysis	57
8.1	Determination of amino acid, cadaverine, putrescine and GABA	57
8.2	Determination of intracellular PLP	57
8.3	Determination of metabolism	58
Chapter 4  Efficient Biotransformation Of L-Lysine Into Cadaverine By Strengthening Pyridoxal 5’-Phosphate-Dependent Proteins In Escherichia Coli With Cold Shock Treatment	59
1	Background	59
2	Material and methods	61
2.1	Plasmids construction	61
2.2	Culture condition	61
2.3	In vivo whole-cell biotransformation of L-lysine to cadaverine	61
2.4	In vitro whole-cell biotransformation of L-lysine to cadaverine	62
3	Results and discussion	62
3.1	Effect of super-salvage pathway genes on cell growth	62
3.2	Proteins expression and intracellular PLP production	64
3.3	Enhancement of in vivo cadaverine production by intracellular PLP	66
3.4	Enhancement of cadaverine production by whole-cell biotransformation..68
4   Conclusion	72
Chapter 5  Engineering Pyridoxal Kinase PdxY Integrative Escherichia Coli Strain And Stepwise Optimization For High-Level 5-Aminolevulinic Acid Production	73
1	Introduction	73
2	Materials and methods	75
2.1	Bacterial strains, plasmids, and materials	75
2.2	Genome integration with pdxY and pdxK genes	75
2.3	Culture medium and condition	75
2.4	Ehrlich’s reagent assay	76
2.5	ALAS activity analysis	76
3	Results and discussion	76
3.1	PLP formation, biomass and amino acids profiles between engineered strains…………………………………………………………………………....76
3.2	Effect of PdxY on biomass, ALA production and metabolites	79
3.3	Reinforcing ALA production with chaperone and high copy plasmid	81
3.4	Optimization of substrate and precursor for ALA production	84
3.5	High-level ALA production in fed-batch fermentation	85
4   Conclusion	88
Chapter 6	Migration Of Glutamate Decarboxylase By Cold Treatment On Whole-Cell Biocatalyst Triggered Activity For 4-Aminobutyric Acid Production In Engineering Escherichia Coli	89
1	Introduction	89
2	Materials and methods	90
2.1	Culture conditions	90
2.2	Conversion of MSG into GABA	90
2.3	Cold-treatment of whole-cell biocatalyst	91
2.4	Determination of whole-cell enzyme kinetic and thermodynamic parameters	91
2.5	Zeta potential measurement	91
2.6	Protein extraction from periplasm	91
2.7	Reusability of whole-cell biocatalysts	92
3	Results and discussion	92
3.1	Effect of replication origin and oxygen supply on GadB expression	92
3.2	Kinetic parameters of GadB in different cold treatments	94
3.3	Morphology, charge, and mechanism of cold-treated whole-cell biocatalyst	97
3.4	Reutilization of whole-cell biocatalyst for high-level GABA production101
4	Conclusion	102
Chapter 7	Sustainable Production Of 4-Aminobutyric Acid (GABA) And Cultivation Of Chlorella Sorokiniana And Chlorella Vulgaris As Circular Economy	103
1 Background	103
2	Materials and methods	105
2.1	Cultivation and cell growth in different mediums	105
2.2	Conversion of MSG to GABA using different strains	105
2.3	Optimal biotransformation of GABA	105
2.4	Optimization of whole-cell conversion using in situ CO2	105
2.5	Citrate addition for high-level conversion of GABA	106
2.6	CO2 sequestration and microalgae cultivation	106
2.7	Lipid analysis	107
3	Results and discussion	107
3.1	Optimization of GAD production in different strains	107
3.2	Optimization of GABA production in W3110	109
3.3	In-situ CO2 utilization for higher GABA production	112
3.4	Enhancement of GABA production via PLP regeneration	113
3.5	Citrate-fed strategy for high-level GABA production	114
3.6	Using CO2 by-product and GABA to enhance microalgae growth	118
4	Conclusion	120
Chapter 8	A Novel Direct Enzymatic Evaluation Platform (DEEP) To Fine-Tune The Quality And Quantity Of Pyridoxal-5’-Phosphate-Dependent Proteins	122
1	Background	122
2	Experimental section	123
2.1	Bacterial strains, plasmid, and materials	123
2.2	Cultivation condition and medium for DEEP	123
2.3	Culture condition for elucidating the strain dependence on nitrogen/carbon source	124
2.4	Culture conditions for PLP-dependent proteins	124
2.5	Enzymatic activity analysis	124
2.6	Analysis of PLP binding site and 3-D structure	125
2.7	Molecular dynamics simulation of RcALAS mutant	125
3	Results and discussion	125
3.1	The correlation between nitrogen utilization and PLP dependency	125
3.2	Identification of the essential genes in PLP synthesis pathways	128
3.3	Using CRISPRi to screen sensitive E. coli strains to PLP availability	129
3.4   A novel Direct Enzymatic Evaluation Platform (DEEP)	130
3.5	Explore the best chassis and enzymatic activity via DEEP	134
3.6   Design of a PLP sponge to enhance protein quality and quantity (Q&Q)	137
3.7	A conserved PLP binding pocket is critical in PLP sponge strains	139
4	Conclusion	140
Chapter 9  Future Prospects	142
1   Establishment of a whole cell biosensor for PLP detection is required	142
2   Explore the optimal assemblies for in vivo PLP production	142
3   Apply the DEEP into other strains	142
4   Apply the superior host WJK for high-end chemicals production	143
References	144
Appendix	172
                                    

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