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研究生：	丁婉雯 Ting, Wan-Wen
論文名稱：	染色體整合T7 RNA聚合酶與基因編輯器進行酶之定向進化實現永續化學品的生物合成 Chromosomal integration of T7 RNA polymerase and base editor for enzyme directed evolution toward sustainable chemical biosynthesis
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：	2023
畢業學年度：	111
語文別：	英文
論文頁數：	228
中文關鍵詞：	合成生物學、T7 RNA聚合酶、戊二胺、5-胺基酮戊酸、衣康酸、碳酸酐酶、CRISPR干擾、定向進化、脫氨酶、低碳足跡
外文關鍵詞：	Synthetic biology, T7 RNA polymerase, cadaverine, 5-aminolevulinic acid, itaconic acid, carbonic anhydrase, CRISPRi, directed evolution, deaminase, low carbon footprint
相關次數：	點閱：105 下載：4
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隨著合成生物學的進展，生物系統的謎團逐漸被揭露，將焦點從系統生物學的反向工程轉向了合成生物學的正向工程。作為一門跨領域的學科融合了生物學、工程學和電腦科學等多學科領域，通過從頭設計合成基因迴路與生物系統已成為一種手段來解決現實世界的挑戰。將合成生物學應用於微生物細胞工廠的發展，為革新基因調控系統和代謝途徑建立了途徑，以實現最佳化生物化學品生產。蛋白質進化透過反覆突變循環對提高酶活性、穩定性與耐受性發揮著至關重要的作用。通過蛋白質工程與合成生物學相結合，我們有望建立永續的生物製造系統。本論文旨在建立蛋白質的調控系統和定向進化系統，應用於低碳足跡化學品生產。
高效率基因調控和編輯工具的需求顯著推動了基因工程的進展。在這些工具中，噬菌體衍生的T7 RNA聚合酶（T7RNAP）及其相應T7啟動子的發現已被認定為重要里程碑之一。T7RNAP的量控制了正交轉錄效率，以達到充分的蛋白質產量。在這項研究中，將三種不同啟動子驅動的T7RNAP模組整合至耐受性菌株大腸桿菌W3110的基因組中，從具有或不具有lacI/lacO調控的目標質粒中評估正交效應。通過誘導表達的菌株W3110::L5在具有lacI/lacO調控的pET載體中實現了82.5%的戊二胺產率，而持續型表達的菌株W3110::pI在不含有lacI/lacO調控的pSU載體中達到了100%的戊二胺產率，超過了商業菌株BL21(DE3)。為了進一步提高戊二胺的產量，利用CRISPR干擾技術下調代謝戊二胺的途徑，獲得了26個基因工程菌株，能在不產生生長負擔的情況下進行代謝調控。除了體內代謝生產，亦於W3110中構建了由J23100啟動子驅動的CadA持續型表達基因迴路。無需誘導的JW生物催化劑在全細胞生物轉化中表現出卓越的性能，以2.5 M L-離胺酸為底物的反應中，可達到2.16 M 的戊二胺產量，為86%的產率。持續型生物催化劑呈現出高量表達、穩定性和可重複使用性，成為有潛力的戊二胺生產菌株。
除了啟動子調控對於蛋白表現的影響，基因在特定染色體位點的整合亦顯著影響遺傳表現，然而整合位點對於代謝通量的影響仍不清楚。因此，基於W3110::L5中T7RNAP基因迴路的設計，我們利用 5-氨基酮戊酸（5-ALA）的生產作為示範，研究染色體位點對基因調控和代謝通量的影響。受到lac operon和轉錄環境的影響，不同位點所轉錄的T7RNAP mRNA量與目標蛋白表達量呈正相關。為達成低碳足跡生產，建立了RuBisCO途徑達表達 1,5-二磷酸核酮糖羧化酶/加氧酶（RuBisCO）及磷酸核酮激酶（PRK），並通過同位素進行代謝通量分析。由C13同位素分析顯示，RSSH菌株更傾向於將添加的底物甘氨酸轉化為生物量，於30小時產生5.79 g/L總生物量。RSSL菌株透過同化CO2達到生物量增量，並從葡萄糖中獲得更高的代謝甘氨酸（C12-甘氨酸），在30小時內分別達到3.75 g/L的生物量和7.01 g/L 的5-ALA。透過依序優化TCA通量和去除醋酸累積，工程菌株RSSLD可生產9.23 g/L 5-ALA，並達成最少CO2釋放量為2.32 g-CO2/g-DCW。推測此菌株差異性來自於所整合的基因間接影響位點附近基因的表現，導致代謝行為的不同。這項研究揭示了不同位點的整合基因會影響局部基因的表現，甚至是不同菌株的代謝行為。
酶的特性在化學品生產中有著不可或缺的作用。定向進化是改善酶性能的一種方法。在本論文中，利用了菌株MutaT7含有整合於基因組中融合於T7RNAP上游的脫氨酶作為基因編輯器，進行體內靶點專一性編輯，我們開發了基於生長依賴之整合型篩選平臺DEPEND-2.0，藉由下調內生必須基因碳酸酐酶（CA）對生長的影響，進行來自Mesorhizobium loti的CA （MlCA）基因突變，結果發現一個P105S點突變導致結構崩塌，造成酶活性完全喪失。考慮到體內突變效率低的限制，改以退化密碼子設計T7啟動子序列，改變T7RNAP與其同源T7啟動子的結合效率，通過流式細胞儀進行sfgfp基因突變株的螢光分布來展示這一概念。另外，我們以順式檸檬酸脫羧酶（CadA）的突變進行功能驗證，利用衣康酸生物感測器進行篩選。針對T7啟動子序列之上游（U）、中游（C）和下游（D）的三個區域設計退化引子而產生不同強度分布的啟動子，經篩選出強（S）、中（M）及弱（W）共9種的螢光分布，進而以dT7啟動子反向設計克隆於CadA下游進行基因突變而不干擾蛋白表達，利用流式細胞儀進行分選，其中以改變T7下游序列的強啟動子DS設計，在sfGFP和CadA的進化提供了一致的螢光分佈，揭示了改變T7啟動子作為調控突變效率的可行方向。
本文闡釋經由染色體不同位點整合T7RNAP，及其啟動子的調控，可實現菌株中蛋白生產及代謝流的調節，結合固碳途徑的建立，可達成低碳排的化學品生產。另一方面，通過改變T7RNAP與T7啟動子間的結合親和力，可調控基於脫氨酶-T7RNAP之定向進化平台的突變效率。綜合應用T7 RNA聚合酶不止於基因表達，更是介導的基因調控和蛋白定向進化的強大工具，可實現低碳排、環保且具經濟效應的永續生物質化學品生產。

With the advance in synthetic biology, the enigma of biological system has gradually been revealed, shifting the focus from reverse engineering of system biology to forward engineering of synthetic biology. As a multidisciplinary field embracing biology, engineering and computer science, the de novo design of synthesizing genetic circuits and biological systems has emerged as a means to tackle the real-world challenges. Applying the synthetic biology into the development of microbial cell factory establishes the avenues to revolutionize gene regulation systems and metabolic pathways achieving optimal biochemical productivity. Protein evolution plays a pivotal role in enhancing the enzymes activity, stability and tolerance through iterative mutagenesis cycles. By coupling the protein engineering with synthetic biology, we hold the promise of building up a sustainable biomanufacturing system. The objective of this dissertation aims to establish protein regulation system and directed evolution system for low-carbon footprint chemical production.
The demands for efficient genetic regulation and editing tools have significantly propelled the progress of genetic engineering. Among these tools, the discovery of the phage-derived T7 RNA polymerase (T7RNAP) and its corresponding T7 promoter has been recognized as a major milestone. The level of T7RNAP controlled the orthogonal transcription efficiency for adequate protein production. In this study, three different promoter-driven T7RNAP cassettes were integrated onto the chromosome of the stress-tolerant Escherichia coli W3110. The orthogonal effect was evaluated from the target plasmids with or without lacI/lacO regulation. The inducible-expression strain W3110::L5 achieved a cadaverine (DAP) yield of 82.5% using the pET backbone with lacI/lacO regulation, while the constitutive-expression strain W3110::pI attained a DAP yield of 100% using the pSU plasmid without lacI/lacO regulation, surpassing that of the commercial BL21(DE3). To further enhance the DAP titer, the DAP catabolism was downregulated using CRISPRi, resulting in 26 genetic strains exhibited metabolic regulation without a growth burden. Apart from the in vivo metabolic production, the constitutive J23100-driven CadA expression circuit was constructed in the W3110. The inducer-free JW biocatalyst demonstrated remarkable performance in whole cell biotransformation, achieving a 2.16 M DAP titer with 86% yield from 2.5 M L-lysine as substrate. The biocatalyst presented high-level constitutive expression, stability and reusability, as a promising strain for DAP production.
In addition to the effect of promoter tuning on protein expression, the integration of genes at specific chromosome loci significantly influences the genetic performance, however, the impact of chromosomal loci on the metabolic flux remained unclear. Thus, upon the genetic design of T7RNAP in W3110::L5, we further investigated the effect of chromosomal loci on the gene regulation and the metabolic control using the 5-aminolevulinic acid (5-ALA) production as demonstration. The mRNA levels of transcribed T7RNAP at different loci exhibited a positive correlation with the gene expression levels, which were affected by the lac operon and transcriptional environment. To reach the low-carbon footprint production, the RuBisCO pathway was established by overexpression of 1,5-bisphosphate ribulose carboxylase/oxygenase (RuBisCO) and phosphorribulose kinase (PRK) and examined the metabolic flux by isotope. The C13 isotope analysis revealed the strain RSSH tend to convert the supplemented precursor glycine into the biomass with 5.79 g/L at 30 h. The strain RSSL reached biomass increment from assimilated CO2 and obtained higher metabolic glycine (C12-glycine) from glucose, achieving 3.75 g/L of biomass and 7.01 g/L of 5-ALA at 30 h, respectively. Through sequentially optimization of TCA flux and bypass the acetate accumulation, the engineered strain RSSLD produced 9.23 g/L of 5-ALA achieving minimum CO2 releasing of 2.32 g-CO2/g-DCW. It is speculated that the different strain behaviors came from the integrated gene indirectly affecting the expression of genes near the locus, resulting in varying metabolic behaviors. This study unveiled the integrated genes at different loci affect the local gene performance and even the metabolic behavior of different strains.
The enzyme properties play the dispensable role in the chemicals production. Diverted evolution is an approach for improving the enzyme performance. Herein, we utilized strain MutaT7, which equipped with a deaminase fusing in the upstream of T7RNAP in the chromosome as genetic editor conducting the in vivo target specific editing. We developed a growth-dependent integrated screening platform DEPEND-2.0 down-regulating essential carbonic anhydrase (CA) to influence the cell growth. Applying to evolving the CA from Mesorhizobium loti (MlCA) resulting in a mutation at P105S led to a loss of enzyme activity due to the structural collapse. Concerning with the limitation of low mutation efficiency from in vivo mutagenesis, our focus shifted towards altering the binding efficiency of T7RNAP on its cognate T7 promoter through degenerated codon design of the T7 promoter sequence. We demonstrated the proof-of-concept using the distribution of sfgfp mutation which was screened by the flow cytometry. On the other hand, we conducted the proof-of-function mutagenesis of cis-aconitate decarboxylase (CadA) which was screened by the itaconic acid biosensor. Three regions of degenerated design in the upstream (U), central (C) and downstream (D) on T7 promoter sequence generate strong (S), medium (M) and weak (W) fluorescence intensity, totaling nine combinations. For the evolution of CadA, we applied the reverse dT7 promoter sequence in the downstream of CadA without disrupting the protein expression. From the screening by flow cytometry, the strong promoter DS from the downstream region of T7 promoter provided the consistent broad fluorescence distribution of sfGFP and CadA evolution revealing the feasibility of altering the T7 promoter as a viable direction for regulating mutation efficiency.
In conclusion, through the integration of T7RNAP at different chromosomal loci and the promoter regulation achieving the tuning of protein production and metabolic flux in bacterial strains, combined with the establishment of carbon fixation pathways, enabling low-carbon emissions in chemicals production. On the other hand, by altering the binding affinity between T7RNAP and the T7 promoter, the mutation efficiency of deaminase-T7RNAP based directed evolution is tunable. Integrated application of T7 RNA polymerase is not only involved in gene regulation but also a powerful tool for mediating gene regulation and protein directed evolution realizing environmentally friendly, low-carbon emission, and economically viable sustainable bio-based chemicals production.

Disclaimer on Author Copyright	II
中文摘要	IV
Abstract	VII
致謝	X
Content	XI
List of Tables	XVI
List of Figure	XVIII
Abbreviations	XXI
Chapter 1 Introduction	1
1	Motivation and purpose	1
2	Research scope of dissertation	4
Chapter 2 Literature Review	8
1 Synthetic Biology and Metabolic Engineering	8
1.1 Emerging of Synthetic Biology	8
1.2 Genetic engineering tools for gene regulation	10
1.3 Metabolic engineering on crucial pathways in E. coli	14
2 The role of T7 system in the synthetic biology	18
2.1 The Origin of T7 system	18
2.2 Regulation of T7 system for versatile applications	19
3 Directed evolution for protein engineering	20
3.1 Development of directed evolution	20
3.2 In vitro gene mutagenesis strategies	21
3.3 In vivo gene mutagenesis strategies	22
3.4 High-throughput screening and selection strategy	25
4 Carbon capture, mineralization and reutilization through bioprocess	28
4.1 Crisis from the petrochemical industry	28
4.2 Carbonic anhydrase for carbon capture and mineralization	28
4.3 RuBisCO-based carbon reutilization	29
4.4 Evaluation the CO2 assimilation ability	32
5 Bio-based chemicals toward low-carbon footprints	34
5.1 Cadaverine as the polymer building blocks	34
5.2 5-aminolevulinic acid as the medicine precursor	36
5.3 Itaconic acid as the polymer building blocks	37
Chapter 3 Materials and Methods	40
1 Chemicals and Materials	40
2 Instrument	43
3 Molecular cloning	44
3.1 Plasmids and genomic DNA extraction	44
3.2 Primer phosphorylation and annealing	45
3.3 Polymerase Chain Reaction (PCR)	46
3.4 Prolonged overlap extension-PCR (POE-PCR)	48
3.5 Enzyme digestion	49
3.6 DNA electrophoresis and DNA gel extraction and purification	49
3.7 Competent cell preparation for heat-shock transformation	50
3.8 Ligation and transformation	50
3.9 Heat-shock transformation	51
4 Engineered strains development	51
4.1 Chromosome integration by phage attachment at specific locus	51
4.2 Gene knockout by homologous recombination	52
4.3 Selective marker removal	52
5	Media preparation and cell culture	52
5.1 Common bacterial strain used in this study	52
5.2 Common media preparation	53
5.3 Cell culture and fermentation	53
6	Protein analysis	54
6.1 Buffer preparation	54
6.2 Sodium Dodecyl Sulfate-Polyacrylamide Gel Electrophoresis (SDS-PAGE) preparation	54
6.3 Sample preparation	54
6.4 Program setup for analysis	55
6.5 Quantification of relative protein amount from SDS-PAGE	55
6.6 Identify the unknown protein by tandem mass spectrometer	55
7 Common Analytic assay	56
7.1 Optical density and fluorescence intensity determination	56
7.2 Dry cell weight and biomass determination	56
7.3 Elemental analysis of cell composition	56
7.4 Plasmid copy number (PCN) quantification by quantitative PCR (qPCR)	57
7.5 Transcription level quantification by quantitative real-time reverse transcription polymerase chain reaction assay (qRT-PCR)	57
7.6 HPLC quantification of organic acids and amino acids	59
8 Specific Analytic assay	59
8.1 Activity measurement of carbonic anhydrase	59
8.2 Carbon sequestration into calcium carbonate	59
8.3 Determination of 5-ALA concentration by Ehrlich’s assay	60
8.4 Intracellular ATP quantification	60
Chapter 4 Development of chromosome-based T7 RNA polymerase and orthogonal T7 promoter circuit in Escherichia coli W3110 as a cell factory	61
1 Background	61
2 Plasmid construction and specific analysis in this study	62
2.1 Construction of CRIM plasmids	62
2.2 Construction of plasmids for heterogeneous protein expression	62
2.3 In vivo DAP production	64
2.4 Protein quantification by densitometry	64
2.5 Analysis protein identity by CE/LC-MS	65
3 Result & Discussion	65
3.1 Engineered E. coli W3110 equipped with T7RNAP	65
3.2 Demonstrate lacI/lacO regulation in the new strains by sfGFP	68
3.3 Carbonic anhydrase expression and activity in engineered W3110 strains	70
3.4 Conversion of L-lysine to DAP by the engineered W3110 strains	71
4 Conclusion	75
Chapter 5 Metabolic manipulation through CRISPRi and gene deletion to enhance cadaverine production in Escherichia coli	76
1 Background	76
2	Plasmid construction and specific analysis in this study	77
2.1 Construction plasmids for CadA expression	77
2.2 Construction plasmids for sgRNA-expressing	78
2.3 Culture conditions	80
2.4 HPLC analysis of lysine and DAP	80
3	Results and discussion	80
3.1 Establish CRISPRi regulation system in E. coli for DAP production	80
3.2 CRISPRi-mediated gene knockdown for enhancing DAP production	82
3.3 Optimal PLP concentration in CRISPRi regulation strains	85
3.4 The effect of lysine concentration and additive time for DAP production	87
3.5 Metabolic manipulation through gene deletion in E. coli	89
4 Conclusion	91
Chapter 6 Whole-cell biocatalyst for cadaverine production using constitutive expression of L-lysine decarboxylase in recombinant Escherichia coli W3110	92
1 Background	92
2	Plasmid construction and specific analysis in this study	93
2.1 E. coli strains and recombinant plasmid construction	93
2.2 Culture medium and cultivation conditions	94
2.3 Tolerance of DAP in different strains	94
2.4 Determination of CadA enzymatic activity	95
2.5 Resistance dosage and passage	95
2.6 Long-term storage	95
2.7 Whole-cell biotransformation of L-lysine to cadaverine and reutilization	96
3	Results and discussion	96
3.1 DAP production and tolerance in different strains	96
3.2 Comparison of J23100 and T7 promoter on CadA expression	97
3.3 Plasmid stability in strain JW	99
3.4 High-cell-density fermentation of whole-cell biocatalyst	102
3.5 Optimal biotransformation using whole-cell biocatalyst	103
4	Conclusion	106
Chapter 7 Genetic and metabolic regulation via chromosomal T7 RNA polymerase toward low-carbon footprint 5-aminolevulinic acid production in Escherichia coli W3110	107
1 Background	107
2 Plasmid construction and specific analysis in this study	109
2.1 Plasmid construction	109
2.2 Adaptive laboratory evolution (ALE) of the strain harboring ALAS	110
2.3 Calculation of CO2 assimilation from 5-ALA production	110
2.4 Glycine utilization index in T7-equipped W3110	111
3 Results and Discussion	112
3.1 Engineered T7-equipped W3110 (WT7) at different loci	112
3.2 Application of WT7 strains for the biosynthesis of 5-ALA	115
3.3 Adaptive Laboratory Evolution (ALE) and amino acid metabolism	117
3.4 Regulation of 5-ALA production using ATP regeneration, central metabolic node and gene knockout	121
3.5 Interpretation of glycine utilization into biomass and 5-ALA under CO2 recycling	124
3.6 CO2 assimilation capability of WT7 strains	126
4	Conclusion	129
Chapter 8 Directed evolution of Mesorhizobium loti carbonic anhydrase for carbon dioxide sequestration by MutaT7 and rational codon design	130
1	Background	130
2	Plasmid construction and specific analysis in this study	132
2.1 Plasmids construction	132
2.2 In vivo target specific directed evolution by MutaT7	133
2.3 Colonies screening by DEPEND-2.0 system	134
2.4 CO2 sequestration	134
2.5 Structure simulation	134
2.6 Generated DNA logo using WebLogo	135
3 Results and Discussion	135
3.1 Establish a screening platform using DEPEND-2.0	135
3.2 Directed evolution of MlCA by MutaT7	137
3.3 Directed evolution of MlCA by degenerated synonymous codons	140
3.4 Stepwise codon optimization of MlCA for CO2 sequestration	141
4 Conclusion	144
Chapter 9 Tunable T7 promoter orthogonality on T7RNAP for direct evolution of cis-aconitate decarboxylase using itaconic acid biosensor	145
1	Background	145
2 Plasmid construction and specific analysis in this study	147
2.1 Biosensor plasmid constructions	147
2.2 Mutation plasmid constructions	147
2.3 Characterization of itaconic acid biosensor	149
2.4 Directed evolution of target protein by MutaT7	149
2.5 Biosensor-based screening	150
2.6 Fluorescence-Activated Cell Sorting (FACS) analysis	150
3 Result and Discussion	150
3.1 Establishment of IA biosensor for high throughput screening	150
3.2 Intracellularly synchronic sensing and IA production	153
3.3 Engineered T7 promoter for altering the mutation efficiency	155
3.4 Applying the reverse T7 promoter for directed evolution of AtCadA	157
4 Conclusion	160
Chapter 10 Challenges and Perspective	161
References	163
Appendix-Tables	192
Appendix-Figure	198
Achievements	202
                                    

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