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研究生：	譚世一 Tan, Shih-I
論文名稱：	以合成生物學與 CRISPR/Cas9 系統開發大腸桿菌作為全細胞生物感測器及綠色生物工廠 Tailoring Echerichia coli as whole-cell biosensor and green biorefinery via synthetic biology and CRISPR/Cas9 system
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：	2021
畢業學年度：	109
語文別：	英文
論文頁數：	263
中文關鍵詞：	合成生物學、大腸桿菌、T7 RNA 聚合酶、CRISPR 技術、生物固碳、碳酸酐酶、ALA 合成酶、賴氨酸脫羧酶、加氧酶、磷酸二氫激酶
外文關鍵詞：	synthetic biology, Escherichia coli, T7 RNA polymerase, CRISPR technology, biological carbon fixation, carbonic anhydrase, 5-aminolevulinic synthetase, lysine decarboxylase, RuBisCO, PRK
相關次數：	點閱：99 下載：12
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本研究旨在利用合成生物學技術開發大腸桿菌的多功能應用。合成生物學的中心思維是精準且有效調控生物的轉錄及轉譯，以最佳的基因、最有效率的工具在最佳的生物底盤上快速實現醫、農、工、食品、能源及生物材料等領域的應用。本論文中，我們欲釐清且解決幾個科學問題：（一）基於T7系統建立可廣義使用的基因放大器；（二）提昇葡萄糖分子之生物感測靈敏度於醫療診斷；（三）以CRISPRi來達成酶活篩選的平台；（四）同步固碳與生產高價化學品的技術。
近年來，開發非自生的轉錄及轉譯系統越來越受關注，當中T7系統是最強大的非自生轉錄裝置；T7系統依靠整合在染色體的T7 RNA聚合酶與T7啟動子專一結合並引發大量的轉錄mRNA可實現外源蛋白的工業級生產，卻受限於單一的大腸桿菌 BL21(DE3)。質體驅動的T7系統（PDT7）可廣義地應用在不同宿主，但常被認為對生物具有毒性且不穩定，原因尚未闡明。本研究構築16個自組成型PDT7系統，可以用於驅動高量的螢光蛋白並放大基因的表現。此外，本研究首次證實PDT7的細胞毒性及不穩定性是源自高表達T7 RNA聚合酶的正交效應造成細胞資源的過度利用。由於PDT7具有基因放大的效果，分別可提高27倍及5倍對葡萄糖及銅離子感應的靈敏度。而且PDT7系統能用於表達碳酸酐酶、賴氨酸脫羧酶和5-ALA合成酶、及在非模式生物的希瓦氏菌中實現於廣義物種的應用。
生物傳感器相較於傳統的化學及物理方式，具有原位分析及生物相容性的優點，是醫療診斷的新趨勢。本研究第二部分，我們以葡萄糖響應的啟動子（PI promoter）比較三種遺傳效應子，包括核酶調節劑（RiboJ）、成簇的規則間隔的短回文重複序列干擾（CRISPRi）和PDT7來增強糖分子的偵測效能。RiboJ可將動態範圍（dynamic range）增加到2989 a.u.，但將信噪比（S/N）降低到1.59；CRISPRi介導的NIMPLY邏輯門將動態範圍及信噪比都增加到5720 a.u.及4.58；PDT7可達到44180 a.u的動態範圍，但信噪比仍為3.08。通過偶聯PDT7和CRISPRi介導的NIMPLY，我們構建了一個最佳的PIGAS菌株，維持了高的動態範圍，並由於降低了基礎表達，提高信噪比到4.95。我們將合成細菌引入微型裝置中，提供非侵入式及方便攜帶的尿糖檢查系統，可作為糖尿病診斷的替代方法。
定向進化是合成生物學的核心工作，當中酶的改造必須依靠高通量的篩選平台，利用CRISPRi開發直接酶性能評估與確認技術（DEPEND）是本研究的第三個主題。我們在大腸桿菌以CRISPRi系統靶向碳酸酐酶基因（CRISPRi :: CA）控制細胞的生長，通過轉化具有目標基因的質體來恢復細胞生長，結果顯示基於CRISPRi :: CA的DEPEND系統可以篩選不同活性的碳酸酐酶。此外，利用五氨基乙酰丙酸合成酶（ALAS）可轉換甘氨酸和琥珀酸-CoA釋放出CO2分子的特性而補償生物量，亦可由高通量微孔板直接挑選出具有最佳ALAS活性的菌株。
二氧化碳（CO2）排放一直是化學工程備受關注的原因，科學家致力開發降低及再利用二氧化碳的技術，其中光合生物代謝二氧化碳受限生長緩慢，基因工具及基因訊息缺乏，難以利用基改調控生產多樣性的化學品。本研究第四部分旨在建立大腸桿菌表達核糖1,5-雙磷酸羧化酶/加氧酶（RuBisCO）和磷酸二氫激酶（PRK）來吸收二氧化碳。首先我們建立簡易的CO2同化效率計算來評估其固碳能力。比較三種不同的設備：FIC、TLD及CBD；結果顯示在CBD中通入5%的CO2達到最佳的固碳能力為-2.63 g-CO2/g-DCW。通過共表達GroELS分子伴侶可增強CO2同化能力，進一步達到-1.81 g-CO2/g-DCW的固碳能力，減少32% CO2釋放。接著，我們比較了不同來源的RuBisCOs和PRKs，逐步整合基因（RuBisCO和PRK）到染色體，並搭配CRISPRi干擾zwf和pfkAB將碳流導向RuBisCO途徑，最終達成-1.58 g-CO2/g-DCW的同化能力。C13同位素分析證明配備RuBisCO的大腸桿菌確實可同化CO2並可同步循環利用CO2來生產各種蛋白質，分別生產了光動力治療的五氨基戊酮酸（5-ALA）癌症藥物及取代尼龍單體的二元胺1,5-二胺基戊烷（DAP），完成大腸桿菌高效利用二氧化碳的綠色細胞工廠。

This research aims to harness the power of synthetic biology technology to develop multifunctional applications in E. coli. The central dogma of synthetic biology is to precisely and efficiently control the transcription and translation in the best cell by using the best gene and most efficient genetic tools to achieve unprecedented applications in medical, agricultural, industrial, food, energy, and biomaterial fields. In this dissertation, we intended to uncover the four unsolved scientific issues: (I) the host-independent genetic amplifier based on the T7 system; (II) enhancement of the sensitivity of whole-cell glucose biosensor; (III) establishment of screening platform for enzymatic activity based on the CRISPRi technology; (IV) simultaneous carbon assimilation and chemical production.
In recent years, the development of host-independent transcription and translation systems has attracted more and more attention. Among host-independent transcription and translation systems, the T7 system is the most powerful one. The T7 system relies on the high activity of T7 RNA polymerase integrated on the chromosome and the specific binding to the T7 promoter to activate considerable transcription for industrial-level production of heterologous proteins in E. coli. However, it is restricted to E. coli chassis BL21(DE3). Plasmid-driven T7 system (PDT7) has also been reported to be broadly applied in different organisms, but the plasmid-driven T7 system is toxic and unstable, and the reason has not been explored. This study first constructed 16 constitutive PDT7s which could be used to express high-level sfGFP and to amplify the gene expression. Besides, we clarified that the cell toxicity and instability were attributed to the excessive utilization of cell resources caused by the orthogonality of the highly expressed T7 RNA polymerase to the T7 promoter. Due to the capability to gene amplification via PDT7, the sensitivity of glucose sensing and copper sensing increased by 27 times and 5 times, respectively. Furthermore, PDT7 can be used to express carbonic anhydrase, lysine decarboxylase, and 5-ALA synthetase as well as applied in Shewanella oneidensis MR-1 which is a non-canonical organism as a host-independent system.
Compared with traditionally chemical and physical sensors, whole-cell biosensors possessed the advantages of high biocompatibility and in situ detection, so that it has been regarded as a new medical diagnosis. In the second part of this dissertation, we compared the genetic efficacy of three genetic effectors, including ribozyme regulator (RiboJ), clustered regularly spaced short palindromic repeat interference (CRISPRi), and plasmid-based T7RNA Polymerase (PDT7) in a glucose-responsive system (i.e., PI promoter) to further enhance the glucose-sensing performance. RiboJ can increase the dynamic range to 2989 a.u., but reduce the signal-to-noise ratio (S/N) to 1.59, while the CRISPRi-mediated NIMPLY logic gate increased the dynamic range and signal-to-noise ratio to 5720 a.u. and 4.58, respectively. The use of PDT7 can reach a dynamic range of 44180 a.u, but the signal-to-noise ratio is maintained at 3.08. By coupling PDT7 and CRISPRi-mediated NIMPLY, we have constructed an optimal PIGAS strain that maintained a high dynamic range and improved the signal-to-noise ratio to 4.95 due to reduced basic expression. Finally, we introduced synthetic bacteria into a miniature device to provide a portable system for daily urine glucose inspection, which will be an alternative method of diabetic diagnosis in the future.
Direct evolution is the central work in the field of synthetic biology. In such work, a high throughput screening platform must be established to screen a better enzyme modification. Thus, a CRISPRi-mediated direct enzyme performance evaluation and determination (DEPEND) system was established in this dissertation. We harnessed the CRISPRi system targeting on the essential carbonic anhydrase gene, can (CRISPRi::CA) to control cell growth. By one-step transformation of the plasmid harboring the targeted enzyme into CRISPRi::CA to recover the cell growth as a direct enzyme performance evaluation and determination (DEPEND) system, it showed that the DEPEND system could be used to screen carbonic anhydrase with different activities. Besides, the DEPEND system also distinguished the activity of aminolevulinic acid synthase which can convert glycine and succinate-CoA to release CO2 molecules for release of cell arrest and the best enzyme target could be screened in a round of high throughput microwell experiment.
The issue of CO2 emission is always the very reason that chemical engineering is highlighted. The scientists have devoted themselves to developing the technology to reduce the carbon dioxide emissions and to convert and utilize carbon dioxide. Among the biobased approaches, photosynthetic organisms grow slowly, and the lack of genetic tools and genetic information makes it difficult to regulate their metabolism to produce diverse chemicals through genetic modification. The fourth part in this study was to establish RuBisCO-equipped E. coli that expressed ribose 1,5-bisphosphate carboxylase/oxygenase (RuBisCOs) and phosphate dihydrogen kinase (PRK). First, we set up a simple calculation to evaluate its ability to assimilate carbon dioxide. Deciphering the effect of culture device in FIC, TLD and CBD showed that, in the CBD with forced diffusion of 5% CO2, carbon assimilation capacity achieved the optimal value of -2.63 g-CO2/g-DCW. In addition, co-expression of GroELS molecular chaperones can further enhance CO2 assimilation capability to -1.81 g-CO2/g-DCW and reduce CO2 release by 32%. Next, we compared different combinations of two ribose 1,5-bisphosphate carboxylase/oxygenases (RuBisCOs) and four phosphate dihydrogen kinases (PRKs) from different sources as well as integrated genetic element of RuBisCO and PRK with the introduction of CRISPRi system knocking down zwf and pfkAB to redirect the carbon flow to the RuBisCO pathway, which finally reached -1.58 g-CO2/g-DCW. The C13 isotope analysis revealed that the RuBisCO-equipped E. coli indeed simultaneously assimilated CO2 and produced various proteins for further production of high-value molecules, including 5-aminolevulinic acid (ALA) that could be applied in photo dynamic therapy of cancer, and 1,5-diaminopentane (DAP) to replace the petroleum-based nylon monomer.

中文摘要 I 
Abstract IV 
致謝 VIII
Table of Content IX
Abbreviations XX 
Chapter 1 Introduction 1
1 Motivation and Purpose 1 
2 Research Scope 4 
Chapter 2 Literature Review 8
1 Synthetic Biology 8
1.1 Development of genetic tools 8
1.2 Biosensor is one of the prominent fields 11
2 T7 RNA Polymerase as a Genetic Tool 14
2.1 Integration of T7RNAP into genome 14
2.2 Plasmid-driven T7RNAP system (PDT7) 17
3 CRISPR System 19
3.1 Origin and mechanism of CRISPR system 19
3.2 Classification of CRISPR system 20
3.3 CRISPR as a gene editing tool 22
3.4 CRISPR as gene expression regulation tool 24
4 CO2 as the Carbon Source 26
4.1 Bio-based CO2 conversion is ecofriendly 26
4.2 Approaches to assess the CO2 assimilation capability 28
4.3 Physiology effect of RuBisCO system 33
4.4 Strategies to enhance the RuBisCO system 37
4.5 Transforming the heterotroph to autotroph 44
4.6 Prospective of RuBisCO-based chemical production 49
Chapter 3 Materials and Methods 52
1 Chemicals and Materials 52
2 Equipment 54
3 Cell Culture and Devices 55
3.1 Mediums used in this study 55
3.2 Cell culture condition and devices 55
3.3 Observation of cell morphology 56
4 Molecular Cloning and Recombinant Strain Construction 58
4.1 Plasmid DNA extraction 58
4.2 Restriction enzyme digestion 59
4.3 Primer phosphorylation and annealing 60
4.4 Polymer chain reaction (PCR) 60
4.5 DNA electrophoresis 62
4.6 Gel extraction and PCR purification 62
4.7 Ligation 63
4.8 Heat-shock competent cell preparation 63
4.9 Heat-shock transformation 64
4.10 Gene integration via one-step cloning and integration method 64
5 Protein Analysis 66
5.1 Reagent and solution preparation 66
5.2 Sample preparation 66
5.3 SDS-PAGE preparation 67
5.4 SDS-PAGE running and staining method 67
5.5 Qantifying the relative protein concentration on PAGE 68
5.6 Identify the protein identity by tandem mass spectrometer 68
6 Analytical Methods 69
6.1 Determination of optical density, biomass and sfGFP florescence intensity 69
6.2 Determination of biosensing parameters using Hill’s equation. 69
6.3 Determination of plasmid copy number by quantitative PCR (qPCR) 70
6.4 Determination of relative transcription level by quantitative reverse transcriptase PCR (q-RT-PCR) 70
6.5 Determination of carbonic anhydrase activity 73
6.6 Determination of lysine decarboxylase activity 74
6.7 Determination of ALA concentration 75
6.8 Determination of organic acid metabolites by HPLC 76
6.9 Determination of CO2 assimilation capability 78
Chapter 4 New Insight into Plasmid-Driven T7 RNA Polymerase (PDT7) in Escherichia coli and Used as Genetic Amplifier for Biosensor 79
1 Background 79
2 Plasmid Construction 81
3 Results and Discussion 87
3.1 Development of constitutive PDT7 system in E. coli 87
3.2 Constitutive PDT7 proofs the toxicity caused by orthogonal T7RNAP and T7 promoter 90
3.3 Central dogma analysis of constitutive PDT7 in E. coli 97
3.4 Protein analysis provides new insight into the stability of PDT7 system. 99
3.5 Pathway engineering using PDT7 106
3.6 Apply PDT7 system to enhance the sensitivity of cell-based biosensors. 109
3.7 Identify the promoter strength in non-canonical E. coli strain and organism 112
4 Conclusion 115
Chapter 5 CRISPRi-Mediated NIMPLY Logic Gate for Fine-Tuning the Whole-cell Sensing Toward Simple Urine Glucose Detection 116
1 Background 116
2 Plasmid Construction 118
3 Results and Discussion 122
3.1 Determine medium for whole-cell glucose sensing 122
3.2 Enhanced the glucose sensing efficacy by ribozyme regulator RiboJ 125
3.3 Used CRISPRi system to elevate S/N value of glucose sensing 128
3.4 PDT7 and CRISPRi to boost glucose sensing performance 132
3.5 Adapted synthetic bacteria into a portable urine glucose sensing system 134
4 Conclusion 138
Chapter 6 CRISPRi-Mediated Programing Essential Gene can as a Direct Enzymatic Performance Evaluation & Determination (DEPEND) System 139
1 Background 139
2 Plasmid Construction and DEPEND System 142
3 Results and Discussion 146
3.1 Controlled cell growth by CRISPRi of the essential gene can 146
3.2 CRISPRi::CA serves as a CO2 whole-cell biosensor 151
3.3 CRISPRi::CA serves as a CO2 whole-cell biosensor screening CA performance by CRISPRi::CA 153
3.4 Characterization of CO2-evolving enzymatic reaction by CRISPRi::CA 156
4 Conclusion 159
Chapter 7 Design and Optimization of Bioreactor to Boost Carbon Dioxide Assimilation in RuBisCO-Equipped Escherichia coli 160
1 Background 160
2 Plasmid Construction 163
3 Results and Discussion 165
3.1 Calculation of CO2 assimilation by mass balance 165
3.2 Effect of bioreactors on the CO2 assimilation 168
3.3 Optimization of CO2 utilization by RuBisCO-equipped E. coli 170
3.4 Enhance the CO2 assimilation by inducer and chaperone 173
3.5 New insight of the toxicity and evolution in the RuBisCO-equipped E. coli 177
4 Conclusion 181
Chapter 8 Stepwise Optimization of Genetic RuBisCO-Equipped Escherichia coli for Low Carbon-Footprint Protein and Chemical Production 182
1 Background 182
2 Plasmid Construction 184
3 Results and Discussion 189
3.1 Selection of RuBisCO genes from the green and red algae 189
3.2 Selection of PRK genes from the green and red algae 192
3.3 Stepwise integration of genetic element to obtain a robust chassis 195
3.4 Enhance carbon flux toward RuBioCO pathway by CRISPRi 197
3.5 Coupling the CO2 assimilation and high-value chemical production 202
3.6 Low carbon-footprint protein over-expression in GREEN strain 206
4 Conclusion 209
Chapter 9 Prospectives and Challenges 210
References 216
Appendix 250
                                    

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