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研究生:Novaria Sari Dewi Panjaitan
研究生(外文):NOVARIA SARI DEWI PANJAITAN
論文名稱:The Study of the Novel PTS Regulation in Klebsiella pneumoniae: -EtcA Negatively Affects the 1,3-Propanediol Production -EtcABC Positively Regulates Type III Fimbriae through cAMP-CRP
論文名稱(外文):The Study of the Novel PTS Regulation in Klebsiella pneumoniae:-EtcA Negatively Affects the 1,3-Propanediol Production-EtcABC Positively Regulates Type III Fimbriae through cAMP-CRP
指導教授:蘇伯琦
指導教授(外文):PO-CHI SOO
口試委員:李惠春邱浩傑鄭文義賴信志蘇伯琦
口試委員(外文):HUI-CHUN LIHAO-CHIEH CHIUWEN-YIH JENGHSIN-CHIH LAIPO-CHI SOO
口試日期:2020-03-02
學位類別:博士
校院名稱:慈濟大學
系所名稱:醫學科學研究所
學門:醫藥衛生學門
學類:醫學學類
論文種類:學術論文
論文出版年:2020
畢業學年度:108
語文別:英文
論文頁數:179
外文關鍵詞:Klebsiella pneumoniae
IG URL:@novariasari
Facebook:Novaria Sari Dewi Panjaitan
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Klebsiella pneumoniae was found as a normal flora in human and an opportunistic pathogen. Despite its pathogenesis, K. pneumoniae was regularly used in the production of several valuable intermediates. 1,3-propanediol recently has been used in various industry field, such as the synthesis of biodegradable polyesters, polyurethanes and polyethers. Besides the chemical methods, 1,3-PD can be produced through fermentation processes of glycerol in certain bacteria, including K. pneumoniae. In this study, we found a novel putative enzyme II complex of the phosphoenolpyruvate:carbohydrate phosphotransferase system, EtcA-EtcB-EtcC in K. pneumoniae STU1. Initially, we observed that the overexpression of EtcABC in K. pneumoniae STU1 decreased the 1,3-PD production due to the interaction of EtcA and glycerol kinase of K. pneumoniae (KpGlpK). From the interface residues determined by PDBePISA, the 65th and 110th histidine residues of EtcA were predicted as the important residues for the binding of EtcA-KpGlpK. By several point mutations in etcA, we eventually proved that His-65 residue is important for the interaction of EtcA-KpGlpK. We also provided evidences that the stronger the binding of EtcA-KpGlpK, the less 1,3-PD produced in K. pneumoniae STU1. The overexpression of EtcABC was not only decreasing the 1,3-PD production, but also enhancing the biofilm formation of K. pneumoniae STU1. Both type I and type III fimbriae play an important role in biofilm formation of K. pneumoniae. We found that the overexpression of EtcABC increased the production of type III, but not type I fimbriae. Type III fimbriae is encoded by mrkABCDF operon, where mrkA encodes the major subunit of this fimbrial adhesin in K. pneumoniae. The expression of mrkA was significantly increased in the EtcABC-overexpressing K. pneumoniae strains. We found that the overexpression of EtcABC could increase cAMP production. The high level of intracellular cAMP then activated cyclic-AMP receptor protein (CRP). Our results showed that the locus of etcABC was common in K. pneumoniae strains. We proved that mrkA is positively regulated by CRP in K. pneumoniae STU1 and two clinical isolates. In this study, we unraveled the role of EtcABC in 1,3-PD production and biofilm formation by K. pneumoniae.
Contents
Abstract…………………………………………………………………………... I

Chapter 1
General Introduction
1.1 Klebsiella pneumoniae is a multi-featured bacterium…………………. 1
1.2 Intermediates produced in K. pneumoniae…………………………….. 1
1.3 The properties and production of 1,3-propanediol……………………. 2
1.4 Pathogenesis of K. pneumoniae…………………………………………. 5
1.5 Virulence factors of K. pneumoniae…………………………………….. 6
1.6 Type I fimbriae (encoded by fim operon)……………………………… 7
1.7 Bacterial type I fimbriae regulation……………………………………. 8
1.8 Type III fimbriae (encoded by mrk operon) in Klebsiella pneumoniae…………………………10
1.9 Type III fimbriae regulation in Klebsiella pneumoniae……..................10
1.10 Bacterial biofilm formation……………………………………............... 13
1.11 The regulation of biofilm production in K. pneumoniae……................ 16
1.12 Phosphoemolpyruvate Phosphotransferase System (PTS) in bacteria………………………………………………………17
1.13 Glucose-specific PTS in bacteria………………………………………18
1.14 Regulatory function of the glucose-specific PTS………………………19
1.15 Bacterial PTS and 1,3-propanediol production regulation…………… 21
1.16 Bacterial PTS and virulence factors regulation…………………………………. 21
1.17 The transposon (Tn5) mutagenesis in K. pneumoniae STU1…………. 22
1.18 The main works in this dissertation……………………………………. 23

Chapter 2
Materials and Methods
2.1 Materials used in this study…………………………………………... 32
2.2 Chemical reagents……………………………………………………... 38
2.3 Kits……………………………………………………………………... 40
2.4 Enzymes………………………………………………………………... 41
2.5 Media……………………………………………………………............ 41
2.6 Antibiotics……………………………………………………................ 43
2.7 DNA Electrophoresis Reagents……………………………………….. 43
2.8 Purification of bacterial chromosomal DNA…………………............ 43
2.9 Plasmid purification…………………………………………………... 44
2.10 Gel electrophoresis of DNA……………………………………............ 45
2.11 Purification of DNA from low melting agarose gel …………………. 45
2.12 Preparation of vector and insert DNA……………………………….. 46
2.13 DNA ligation……………………………………………………............ 46
2.14 Cloning of PCR products……………………………………………... 46
2.15 Amplification of DNA by PCR……………………………………….. 46
2.16 Site directed mutagenesis for constructing etcA variants…………... 47
2.17 Heat shock-based DNA transformation………………………............ 48
2.17.1 Preparation of E. coli – competent cells for heat shock transformation………………………………………………48
2.17.2 Heat shock transformation of plasmid DNA………………………… 48
2.18 Electroporation-based transformation………………………………. 48
2.18.1 Preparation of competent cells for electroporation…………..49
2.18.2 Transformation with DNA by electroporation.……………… 49
2.19 Plasmid DNA transfer by conjugation……………………………….. 50
2.20 Blue-white colony screening for colonies containing the recombinant plasmid………………………………………………… 50
2.21 Selection of recombinant plasmids…………………………………… 51
2.22 Sequence analaysis and databank comparison……………………. 51
2.23 Bacterial RNA extraction…………………………………………….. 51
2.24 RNA gel electrophoresis (Agarose/Formaldehyde in MOPS buffer system)………………………………………………………………52
2.24.1 Gel preparation………………………………………………............... 52
2.24.2 Bacterial RNA sample preparation…………………….…….............. 53
2.24.3 Gel running system………………………………..…………………... 53
2.25 Reverse transcription qPCR…………………………………………. 53
2.26 Northern blotting……………………………………………………… 54
2.27 Expression of His-tagged recombinant proteins…………………….. 55
2.27.1 Protein induction……………………………………………................. 55
2.27.2 SDS-PAGE……………………………………………………………... 56
2.27.3 Solubility test of the expressed protein………………………………. 56
2.28 Construction of mutants from Klebsiella pneumoniae……………..... 57
2.28.1 Maintenance of suicide plasmid(s)…………………………………… 57
2.28.2 Selection of in-frame deletion mutants constructed by using the pW18mobsacB suicide plasmid………………………………….......58
2.28.3 Selection of crr mutant of K. pneumoniae STU1 by using the pKO-Kmr suicide plasmid……………………………………..............58
2.29 Complementation of the deleted gene(s)……………………………... 59
2.30 His-tagged proteins purification……………………………………… 59
2.31 Site-directed mutagenesis of etcA…………………………………….60
2.32 GST-tagged protein expression……………………………………… 60
2.33 Protein pull-down assay……………………………………………… 60
2.34 Quantification of biofilm formation…………………………………62
2.35 Antibody preparation…………………………………………………. 62
2.36 Western blot analysis………………………………………………… 62
2.37 Analysis of 1,3-propanediol by high-performance liquid chromatography (HPLC)……………………………………………63
2.38 Quantification of intracellular glycerol 3-phosphate (G3P)……….. 64
2.39 Transmission electron microscopy…………………………………… 65
2.40 Quantification of cyclic AMP………………………………………… 66
2.41 Sugar specificity of EtcABC………………………………………….. 66
2.42 Quantification of crp promoter activity by luxCDABE as reporter... 66
2.43 Statistical methods…………………………………………………….. 67
2.44 Nucleotide sequence accession number…………………………….. 67

Chapter 3
The activity of glycerol kinase and 1,3-propanediol production were negatively affected by EtcA in Klebsiella pneumoniae
3.1 Significance and aim ……………………….…………………………. 70
3.2 Locus of etcABC (KPN0353-KPN00352-KPN00351) is common among K. pneumoniae isolates……………………………………70
3.3 The overexpression of etcA represses the 1,3-PD production in K. pneumoniae………………………………………………………71
3.4 EtcA could interact with glycerol kinase (GlpK) in K. pneumoniae.. 72
3.5 The interaction of EtcA and GlpK inhibits enzymatic function of GlpK…………………………………………………………………73
3.6 Residue His-65 of EtcA is important for binding to GlpK and 1,3-PD production…………………………………………74
3.7 Discussion……………………………………………………………… 76

Chapter 4
The role of EtcABC in regulating type III fimbriae is cyclic AMP receptor protein (CRP)-dependent in Klebsiella pneumoniae
4.1 Significance and aim …………………………………………........... 87
4.2 Overexpression of EtcABC enhanced type III fimbriae production and biofilm formation in Klebsiella pneumoniae……... 89
4.3 cAMP-CRP regulated lac operon and tightly controlled lactose uptake in K. pneumoniae ……………………………………92
4.4 MrkA expression is regulated by cyclic-AMP receptor protein (CRP) in K. pneumoniae…………………………………………93
4.5 The role of EtcABC in enhancing MrkA protein expression is cAMP-CRP pathway dependent…………………………………94
4.6 The overexpression of EtcABC enhanced crp promoter activity in
ΔcrrΔetcABC double genes deletion in K. pneumoniae STU1………..94
4.7 The overexpression of EtcABC increased cAMP level in K. pneumoniae STU1…………………………………………………… 96
4.8 MrkH transcriptional level was affected by crp deletion and EtcABC overexpression……………………………………………...98
4.9 The expression of MrkA is dependent on both cAMP-CRP and MrkH regulations…………………………………………………… 99
4.10 The crp deletion negatively affected the expression of ORF X, the KPN03280 homologue, in K. pneumoniae STU1…………………... 101
4.11 Discussion……………………………………………………………. 102

Chapter 5
General Discussion

Reference list………………………………………………………………… 128







Figure Contents

Figure 1.1 The metabolic pathway of glycerol and glucose in bacteria.. 25
Figure 1.2 Schematic structure of type I fimbrial adhesin…………….. 26
Figure 1.3 Escherichia coli expresses type I fimbriae…………………... 26
Figure 1.4 Locus of mrk operon in the genome of K. pneumoniae…….. 27
Figure 1.5 Locus of mrk operon regulator, mrkHIJ in K. pneumoniae IApc35…………………………27
Figure 1.6 Five important stages in bacterial biofilm formation……… 28
Figure 1.7 Common mechanism of phosphoenolpyruvate (PEP): carbohydrate phosphotransferase system (PTS) in bacteria....28
Figure 1.8 The HPLC chromatograph of filtrate of bacterial culture in glycerol medium……………………………………………


Figure 1.9 Transposon insertion map in D17 mutant…………………..30
Figure 1.10 The Northern blot analysis for the transcription of the etcABCDE and the gene homologue of KPN0348 according to the genomic databse of K. pneumoniae MGH 78578…….31

Figure 2.1 Strategy of in-frame deletion by usng pW18mobsacB suicide plasmid………………………………………………... 68
Figure 2.2 Strategy of constructing the gene deletion and antibiotic cassette insertion mutant by pKO3-Kmr……………………. 69

Figure 3.1 Locus of KPN00353-KPN00352-KPN00351 (etcABC) is common among K. pneumoniae isolates……………………81
Figure 3.2 The quantification of 1,3-PD production, residual glycerol, and bacterial cell density…………………………………….. 82
Figure 3.3 EtcA could interact specifically with KpGlpK…………….... 83
Figure 3.4 BLASTP alignment of etcA shows high homology to the PTS EIIAs in fructose superfamily………………………….. 83
Figure 3.5 The role of overexpression of EtcA and its derivative mutated proteins………………………………………………84
Figure 3.6 Structure and interface residues of GlpK-Crr complex in E. coli and GlpK-EtcA complex in K. pneumoniae………… 85
Figure 3.7 The hypothetical role of EtcA in affecting glycerol metabolism in K. pneumoniae…………………………….…..86
Figure 3.8 Comparison of the contacts surrounding 65th and 110th residues of EtcA variants interacting with KpGlpK……….. 86

Figure 4.1
Overexpression of etcABC increased biofilm formation of K. pneumoniae STU1…………………………………………. 107
Figure 4.2 CRP may regulate mrkA in K. pneumoniae STU1………….. 107
Figure 4.3 Effects of EtcABC overexpression on bacterial biofilm formation…………………………………………………….... 108
Figure 4.4 Overexpression of etcABC enhanced the production of fimbriae in K. pneumoniae……………………………………109
Figure 4.5 Overexpression of etcABC enhanced the production of type III fimbriae in K. pneumoniae……………………………….. 110
Figure 4.6 Overexpression of EtcABC decreased type I production in K. pneumoniae STU1………………………………………….111
Figure 4.7 Strategy used to construct crp deletion strain and the phenotypes of crp mutants observation……………………... 112
Figure 4.8 CRP positively regulates MrkA expression, biofilm formation and adhesion ability of K. pneumoniae………….. 113
Figure 4.9 The role of EtcABC overexpression in enhancing MrkA expression is CRP dependent………………………………...114
Figure 4.10 Exogenous cAMP and overexpression of EtcABC enhanced crp promoter activity………………………………………….115
Figure 4.11 Effect of exogenous cAMP and EtcABC overexpression on K. pneumoniae STU1 and its derivatives on MacConkey plate with or without cAMP…………………………………. 116
Figure 4.12 Overexpression of EtcABC increased cAMP level in K. pneumoniae STU1…………………………………………….. 117
Figure 4.13 crp deletion and EtcABC overexpression affected mrkH trasncripts level in K. pneumoniae…………………………... 118
Figure 4.14 The role of both crp and etcABC overexpression in regulating mrkA expression are dependent on mrkHI……... 119
Figure 4.15 Effects of crp deletion (A) and EtcABC overexpression (B) on transcriptional level of ORF X in K. pneumoniae STU1... 120
Figure 4.16 Model of the role of EtcABC in regulation of type III fimbriae……………………………………………………….. 121
Figure 5.1 Model of the role of EtcABC in K. pneumoniae…………….. 126


Table Contents

Table 1. List of strains and plasmids used in the experiments in this study……………………………………………………………32
Table 2. List of primers used in the experiments of this study……… 35
Table 3. Chemical reagents used in this study………………………... 38
Table 4. Kits used in this study………………………………………... 40
Table 5. Antibiotics used in this study………………………………… 43



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