臺灣博碩士論文加值系統

探討從反覆復發菌血症患者分離出的八株抗藥性金黃色葡萄球菌的演化路徑

摘 要

在2008年，一個病人被抗甲氧苯青黴素金黃色葡萄球菌(Methicillin-resistant Staphylococcus aureus，簡稱MRSA)感染，在其治療期間使用了多種抗生素，但是MRSA所引起的菌血症還是反覆發作。醫院在八個月期間從病人身上分離出8株MRSA菌株(命名為CGK1到CGK8)。這8株菌的脈衝場凝膠電泳結果無區分，分生檢測結果亦是同一型，但每株菌有幾種抗生素的最小抑制濃度測試結果卻不相同也不規律，無法指出這8株菌的演化方向。
因此，本研究的目的是要藉由全基因體定序找出這8株菌的演化路徑。本研究使用Nanopre結合Illumina的定序方法大幅提高組裝細菌基因體的完整性以及準確性。CGK1的序列經過組裝和校正後，其他7株菌株的Illumina資料被用來比對並找出單核苷酸多態性(SNPs)，藉由SNPs 在染色體上的位置，我們推測出4條演化路徑，分別為: (1) CGK1-> CGK2-> CGK3; (2) CGK1-> CGK4-> CGK6-> CGK8; (3) CGK1-> CGK5以及 (4) CGK1-> CGK7。
此外，我們也想要探討這些SNPs對抗藥性的影響。扼煞西林是一種乙內醯胺類抗生素，從CGK1及CGK2的扼煞西林耐受性的改變來看，prs基因上的A304V點突變是唯一差異，然而，並沒有研究指出prs基因對抗藥性會造成的影響，因此對這個突變點進行實驗。結果顯示prs基因的A304V點突變會使MRSA對扼煞西林的耐受度提高超過8倍，而對另一種乙內醯胺類抗生素亞胺培南也有超過32倍的提高，因此我們認為prs基因上的A304V點突變會提高MRSA對乙內醯胺類抗生素的耐受度。
在此研究中，我們提供了新的方法來追蹤病人體內細菌的演化方向，而藉由SNPs對抗生素耐受性的深入研究，未來在臨床上可以更精準的使用抗生素治療。


比較不同來源的clonal complex (CC) 9家畜相關型抗藥性金黃色葡萄球菌

摘 要

金黃色葡萄球菌通常共生在皮膚表面及鼻腔中，也是臨床上最常見的革蘭氏陽性菌，可引起皮膚傷口膿腫、肺炎、菌血症等各種感染。隨著抗生素的大量使用，臨床分離金黃色葡萄球菌中大約60%屬於抗甲氧苯青黴素金黃色葡萄球菌 (Methicillin-resistant Staphylococcus aureus，簡稱MRSA)，是臨床治療的挑戰，因為除了對幾乎所有乙內醯胺(β-lactam)抗生素具抗藥性，MRSA對多種非乙內醯胺抗生素也具抗藥性。早年MRSA感染個案大多跟醫療機構有關，隨著MRSA持續擴大生態，1990年代以後，社區型MRSA的感染開始增加，近年來更發現與家畜相關的MRSA 感染個案(livestock-associated MRSA, LA-MRSA)。在亞洲地區，LA-MRSA主要屬於clonal complex (CC) 9型，然而台灣LA-MRSA在牲畜及人類之間傳染的資料目前很少，因此本研究的主要目的是進行全基因體的比較基因體學分析，以探討台灣各地區的CC9 LA-MRSA在牲畜、肉品以及人類之間的傳播關係。
此研究首先比較市場肉品(42株)及臨床病人(16株)分離出的CC9 MRSA菌的抗藥性及基本基因型，CC9 LA-MRSA普遍帶有多重抗藥性，多數菌對臨床使用多年的幾種抗生素皆具抗藥性。這些菌的基因型大多相同，包括Staphylococcal cassette chromosome mec (SCCmec) XII型及Staphylococcal protein A (spa) t899型，脈衝場凝膠電泳(pulsed field gel electrophoresis, PFGE)也顯示CC9 LA-MRSA菌株有很高的相似度。為進一步探討環境中CC9 MRSA菌跟人類感染CC9 MRSA菌的親緣性，本研究再從不同PFGE分群中挑選20株不同來源的CC9 LAMRSA菌(豬鼻腔-1株、市場肉品-12株、臨床病人檢體-8株)，使用Nanopore次世代定序平台，完成全基因體序列之組裝然後進行比較基因組學分析。除台灣菌株間比較，也與公共數據庫中取得的4株中國CC9 MRSA全基因體序列比較，首先，經過抗藥基因資料庫比對，台灣CC9 LA-MRSA菌株所攜帶的抗藥基因跟其抗藥性表現型大多一致，最主要的發現是，大多數的CC9 LA-MRSA菌株染色體上都帶有特定的原噬菌體序列，雖然菌株攜帶的原噬菌體有差異，但這些菌株在台灣的分布沒有區域性的差異。另發現一些CC9 LA-MRSA菌株的基因序列中，有大片段或小片段的倒置現象，此現象目前沒有研究指出發生原因及對菌株可能造成的影響。親緣關係則顯示這些菌可被歸為三個分支: 分支一在動物、肉品及人類都有偵測到; 分支二主要為人類分離菌; 分支三則主要是肉品分離菌。此研究顯示，CC9 LA-MRSA是可在不同宿主及國家互傳的多重抗藥菌，須提高民眾警覺，如有接觸家畜或生肉品時，應採取適當衛生措施，以避免CC9 LA-MRSA在人體寄生及引發感染。

Evolution pathway of 8 sequential methicillin-resistant Staphylococcus aureus (MRSA) isolates from a patient with persistent bacteremia


ABSTRACT

In 2008, a patient was infected by methicillin-resistant Staphylococcus aureus (MRSA) that led to persistent bacteremia and 8 sequential strains (named CGK1 to CGK8) were isolated during the therapy. These 8 isolates had indistinguishable pulsed-field gel electrophoresis patterns and all belong to the same clonatype. However, the minimum inhibitory concentrations (MICs) of oxacillin fluctuated among these 8 isolates without consistent pattern.
In this study, the objective is to find out the evolution pathways by using whole-genome sequencing and the application of Nanopore with Illumina can generate a genome with high accuracy and completeness. CGK1 genome was successfully assembled and considered the reference. Single nucleotide polymorphisms (SNPs) were detected in the other 7 strains compared to CGK1. A total of 4 evolution pathways were determined based on location of the SNPs on CGK1 chromosome: (1) CGK1-> CGK2-> CGK3; (2) CGK1-> CGK4-> CGK6-> CGK8; (3) CGK1-> CGK5; (4) CGK1-> CGK7.
In addition to the findings of the 4 pathways, we would like to study the influence of specific SNPs on antibiotic susceptibility. A point mutation A304V on prs gene was selected as a target that may increase the level of oxacillin resistance due to the change of MIC for CGK1 and CGK2. However, there are few studies for prs gene and its ability of antibiotic resistance. The result showed that the A304V mutation on prs gene increased the resistance levels of MRSA to oxacillin and imipenem which are β-lactams. Therefore, the A304V prs mutation was considered to make MRSA more resistant to β-lactam antibiotics.
In this study, we provide a new method to track evolution of bacteria in a patient. Furthermore, as more and more researches on SNPs, treatment of antibiotics in clinical can be more precise in the future.


Comparison of clonal complex (CC) 9 livestock-associated MRSA from different sources


ABSTRACT

Staphylococcus aureus is the most common Gram-positive pathogen and usually exists on skin and in nasal cavities as a commensal. It can cause a spectrum of diseases such as skin abscess, pneumonia, bacteremia, etc. Due to the overuse of antibiotics, about 60% of clinical S. aureus isolates are methicillin-resistant. Treatment of methicillin-resistant S. aureus (MRSA) infections can be challenging because resistance to methicillin indicates resistance to almost all β-lactam antibiotics, and MRSA are also often resistant to several non-β-lactam antibiotics. MRSA used to be mostly associated with healthcare facilities but community-associated MRSA infections have increased since 1990s. In addition, livestock-associated MRSA (LA-MRSA) infections emerged in recent years. In Asia, the predominant LA-MRSA belong to clonal complex (CC) 9. However, studies linking transmission between livestock and humans in Taiwan are scarce. Hence, the main objective of this study was to determine the relatedness of CC9 LA-MRSA isolates from livestock, meat, and humans in Taiwan using comparative genomics analysis.
Comparison of antibiotic susceptibility and fundamental genotypes was performed on CC9 MRSA isolates from meat (n = 42) and patients (n = 16) initially. Almost all isolates are multi-drug resistant, especially to antibiotics that have been used clinically for decades. Most of their genotypes were identical, including SCCmec type XII and spa type t899. PFGE also showed high similarity between these isolates, although they separate into several sub-pulsotypes. To further investigate the phylogeny of the CC9 MRSA isolates from the environment and humans, 20 isolates (meat-12; patients-8) from different pulsotypes were submitted to Nanopore whole genome sequencing followed by assembly and comparative genomics analysis. In addition, 4 complete sequences of CC9 MRSA strains from China obtained from the NCBI database were used for comparison. Through cross referencing with an online antibiotic resistance database, the resistance genes carried by the 20 CC9 MRSA isolates matched the majority of their resistance phenotypes. Of noteworthy was that most CC9 LA-MRSA isolates carried specific prophage sequences on their chromosomes. Although they acquired the different prophages, their distribution was random in isolates from different sources. In addition, sequence reversion of large or small fragments was observed in several isolates, and no studies have reported the causes and effects on this phenomenon. The phylogenetic tree shows that the isolates can be classified into 3 clades: clade I includes isolates from livestock, meat and humans; clade II consists of isolates from humans predominantly and; clade III comprises isolates only from meat. This study shows that CC9 LA-MRSA isolates in Taiwan are multi-drug resistant and can transmit between different hosts. Therefore, people who come into contact with livestock and retail meats should take proper hygiene precautions to prevent being colonized by CC9 MRSA and possible subsequent infections.

Chinese Abstract……………………………………………………. i
English Abstract……………………………………………………. iv
Contents…………………………………………………………….. viii
List of Tables……………………………………………………….. xii
List of Figures………………………………………………………. xiii

I. Overall Introduction…………………………………………… 1
1.1 Microbiology and characteristics of Staphylococcus aureus………………………………………………………… 1
1.2 Role in disease……………………………………………....... 1
1.3 Treatment for S. aureus infections………………………......... 1
1.4 Methicillin (Oxacillin)-resistant S. aureus (MRSA)…….......... 2
1.5 MRSA epidemiology…………………………………………. 2
1.6 Classical diagnosis and typing methods…………………........ 3
1.6.1 SCCmec typing……………………………………….. 3
1.6.2 Pulsed-field gel electrophoresis (PFGE)………………4
1.6.3 Multi-locus sequence typing (MLST)…………………5
1.6.4 Staphylococcal protein A (spa) typing………………… 5
1.7 Whole-genome sequencing (WGS)………………………....... 6
Project I…………………………………………………………...... 7
I. Introduction……………………………………………………. 7
1.1 The progress of researches for antibiotic resistance……...........7
1.2 Introduction of 8 sequential isolates………………………......7
1.2.1 High similarity of 8 isolates…………………………...7
1.2.2 Point mutations in 8 isolates…………………………...8
1.3 A novel application of WGS for bacteria…………………….8
1.4 Application and importance of SNPs in bacteria……………...9
II. Materials and methods……………………………………….....9
2.1 Bacterial strains, culture conditions and plasmids……….........9
2.2 Primers and restriction enzymes………………………………10
2.3 MICs of 8 isolates……………………………………………..10
2.4 Whole-genome sequencing…………………………………...11
2.4.1 DNA extraction for Nanopore sequencing……….........11
2.4.2 Nanopore sequencing………………………………….11
2.5 Assembly and correction of CGK1 genome…………………12
2.5.1 Albacore 2.0.1…………………………………………12
2.5.2 Canu-1.6………………………………………………12
2.5.3 Racon………………………………………………….13
2.5.4 Nanopolish-0.8.5…………………………………….13..
2.5.5 Pilon-1.22……………………………………………..13
2.6 Detection of variation…………………………………………13
2.7 Cloning………………………………………………………..14
2.8 Construction of prs mutant derivatives………………………..15
2.9 Antimicrobial susceptibility test……………………………....16
III. Result…………………………………………………………...17
3.1 Detection of SNPs from CGK2 to CGK8……………………..17
3.2 Determination of evolution pathways……………………........17
3.3 Enhanced level of oxacillin and imipenem resistance due to the point mutation A304V on prs gene…………………..........18
IV. Discussion……………………………………………………... 19
V. Reference………………………………………………………. 44

Project II……………………………………………………………. 22
I. Introduction…………………………………………………….22
1.1 Classification of MRSA………………………………………22
1.2 HA-MRSA……………………………………………………22
1.3 CA-MRSA……………………………………………………23
1.4 LA-MRSA…………………………………………………….23
1.5 Transmission of LA-MRSA………………………………….. 24
II. Materials and methods……………………………………….....25
2.1 Culture conditions…………………………………………….25
2.2 Isolate sources………………………………………………...25
2.2.1 Isolates from meat……………………………………..26
2.2.2 Isolates from humans………………………………….26
2.2.3 Sequences for comparative genomics analysis………...27
2.3 Antimicrobial susceptibility test……………………………....27
2.4 Molecular characterization of MRSA…………………………28
2.4.1 DNA extraction & PCR conditions…………………....28
2.4.2 nuc, coa and mecA detection…………………………..28
2.4.3 pvl detection…………………………………………...28
2.4.4 SCCmec typing………………………………………..28
2.4.5 spa typing……………………………………………...29
2.4.6 PFGE (Pulsed-field gel electrophoresis)………………29
2.4.7 MLST………………………………………………….30
2.5 Whole-genome sequencing (WGS)……………………….......31
2.6 Genome assembly and correction……………………………..32
2.7 Detection of antibiotic resistance genes……………………….32
2.8 BLAST ring image generator (BRIG) ………………………...32
2.9 Construction of phylogenetic trees……………………………33
III. Result………………………………………………………...…33
3.1 Molecular typing of CC9 LA-MRSA…………………………33
3.2 Phenotypic antibiotic susceptibility analysis………………….34
3.3 Genotypic resistance profiling………………………………...34
3.4 The relationships of CC9 LA-MRSA between NTU08 and other isolates from meat and patients are close…………..........35
3.5 Whole-genome phylogenetic tree……………………………..36
IV. Discussion……………………………………………………... 37
V. Reference……………………………………………………..... 44

List of Tables

Table 1. Bacterial strains used in this study……………….................56
Table 2. Primers used in this study……………………………...........57
Table 3. The MICs of 8 CGK isolates……………………………...... 58
Table 4. SNPs detected in CGK2 to CGK8 isolates compared to CGK1……………………………………………………….59
Table 5. Primers used in this study………...........................................62
Table 6. Summary of the population, the source of isolates, clonal complex (CC) and resistance genes…………………………64
Table 7. Relationship between antibiotic resistance phenotype and resistance genes in CC9 MRSA…………………………….67
Table 8. Detection of bacteriophages in CC9 LA-MRSA……............68

List of Figures
Figure 1. SCCmec types…………………………………………69
Figure 2. The insert and vector used for cloning………………...70
Figure 3. CGK1 genome………………………………………...71
Figure 4. Determination of evolution pathways of CGK1 to CGK8…………………………………………………72
Figure 5. Map of CGK2 Illumina short-reads to CGK1 chromosome…………………………………………..73
Figure 6. Antibiotic susceptibility test results using Etest……….74
Figure 7. Dendrogram of CC9 MRSA isolates from humans and retail meat in Taiwan……………………………..........75
Figure 8. Consistent loss of DNA fragments in most CC9 MRSA when compared to NTU08…………………………….76
Figure 9. Genome comparison of NTU08 to the 24 CC9 LA-MRSA………………………………………………...77
Figure 10. Classification of prophages detected in CC9 LA-MRSA………………………………………………...78
Figure 11. Sequence dot plot analysis between 24 CC9 LA-MRSA and NTU08……………………………………79
Figure 12. The whole-genome phylogenetic tree and metadata of CC9 LA-MRSA……………………………………….80
Figure S1. Loss of the plasmid in CGK5 genome…………………81
Figure S2. Detection of mecA gene……………………………….82
Figure S3. Comparison of ST398 LA-MRSA to NTU08 sequence..……………………………………………..83

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