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研究生：	王昱仁 Wang, Yu-Jen
論文名稱：	棘阿米巴與眼部共生菌之交互作用研究解析 The interaction of Acanthamoeba and ocular commensals
指導教授：	林威辰 Lin, Wei-Chen
學位類別：	博士 Doctor
系所名稱：	醫學院 - 基礎醫學研究所 Institute of Basic Medical Sciences
論文出版年：	2022
畢業學年度：	110
語文別：	英文
論文頁數：	118
中文關鍵詞：	棘阿米巴、吞噬作用、眼表共生菌、細胞毒性
外文關鍵詞：	Acanthamoeba, Phagocytosis, Ocular commensal, Cytotoxicity
相關次數：	點閱：89 下載：11
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棘阿米巴是一種常見於環境中並可伺機性感染人類產生致盲性角膜炎的自營性原
蟲。根據過往的研究指出，細菌在被棘阿米巴攝食進入細胞內後，細菌可逃脫消化作
用形成棘阿米巴細胞內共生菌或被消化分解成為食物營養來源。然而，在棘阿米巴入
侵人類眼角膜時，棘阿米巴攝食眼表共生菌對於阿米巴性角膜炎的影響並不清楚。本
研究發現，棘阿米巴透過吞噬作用與眼表共生菌產生的交互作用和阿米巴性角膜炎的
病程具有高度相關性。此外，棘阿米巴引發的細胞外微量元素變化亦可刺激環境常在
菌的致病力提升。首先，我們透過免疫螢光染色與核酸放大實驗證明棘阿米巴可透過
肌動蛋白與SBDS細胞骨架相關蛋白參與的吞噬作用，進而將可做為食物來源的大腸
桿菌吞噬進入細胞體內。在利用16S核醣體RNA定序分析比較不同棘阿米巴分離株的
胞內共生菌組成與含量，發現格蘭氏陽性厭氧菌中的黏液真杆菌含量與阿米巴性角膜
炎的疾病進程有正相關性。再來，我們以細胞毒殺試驗、西方墨點法與小鼠眼球體外
模型，證實在可被消化分解的細菌存在之下，棘阿米巴對上皮細胞連接蛋白和角膜上
皮細胞的破壞都會降低。另外，我們將環境常在的克雷伯氏肺炎菌與棘阿米巴共同培
養後，發現棘阿米巴可在改變環境離子濃度之下，使得克雷伯氏肺炎菌轉型成為高毒
力菌株。此研究成果不僅提供眼表菌相影響阿米巴性角膜炎病程之證據；往後，我們
也將持續探索環境與人體中寄生蟲與細菌之間交互作用對於微生物伺機性感染的影
響。

Acanthamoeba is a free-living protozoa to be found in a wide environment and leading to blindness keratitis in humans. Previous studies indicated that bacteria ingested by Acanthamoeba would escape digestion and become endosymbionts or as a food source to be broken down in the vacuole. However, whether Acanthamoeba hunting the ocular commensals affected Acanthamoeba keratitis progression is still unclear. We demonstrated that ocular microbiota was highly correlated with the severity of Acanthamoeba keratitis based on amoeba’s phagocytosis. Besides, the amoeba could also affect the pathogenicity of environmental flora by changing extracellular ions. First, Escherichia coli as a food source could be ingested by Acanthamoeba through the phagocytosis of actin and SBDS protein. The comparison of endosymbionts between Acanthamoeba isolates by 16S rRNA sequencing showed the relative abundance of Blautia producta is related to the keratitis progression. Afterward, using the cytotoxicity assay, western blotting and mice eyeball ex vivo model demonstrated that microbiota existing could reduce the disruption of epithelial cell junctions and corneal epithelium by Acanthamoeba. In addition, after co-culture of Klebsiella pneumoniae with Acanthamoeba revealed a microenvironmental electrolytes alteration by Acanthamoeba and resulting bacteria transformation into high virulence. Based
on the results, suggest that dysbiosis recovery be used in Acanthamoeba keratitis prevention, and in the future, we will continue to study the interaction between parasites and bacteria in the environment and human body.

論文口試合格證明 I
摘要 II
Abstract III
致謝 IV
Abbreviation V
Contents VI
Table list VII
Figure list VIII
CHAPTER 1 Introduction 1
1 Acanthamoeba 1
1.1 Characterization of Acanthamoeba 1
1.2 Virulence factors of Acanthamoeba 2
2 Endosymbionts of Acanthamoeba 2
2.1 Endosymbionts 2
2.2 Microorganism evolution 3
3 Acanthamoeba phagocytosis 4
3.1 Motility associated cytoskeletons 4
3.2 Shwachman-Bodian-Diamond (SBDS) gene and motility 5
4 Commensals and Acanthamoeba 5
4.1 Human body surface commensals 5
4.2 Dysbiosis and Acanthamoeba infection 6
4.3 Opportunistic parasite infection 7
5 Klebsiella pneumoniae and Acanthamoeba 8
5.1 Opportunistic infections in nosocomial infection 8
5.2 The capsule of Klebsiella pneumoniae 8
5.3 Ions regulation in Acanthamoeba and environmental effects 9
CHAPTER 2 Rationale and experimental designs 11
1 Rationale 11
2 Experimental design 12
CHAPTER 3 Materials and methods 14
1 Culture of Acanthamoeba Protozoa 14
1.1 Peptone-Yeast Extract-Glucose (PYG) medium 14
1.2 Page's modified Neff's amoeba saline (PAS) buffer 14
1.3 Passaging Acanthamoeba Cells 14
1.4 Acanthamoeba freezing and thawing 15
2 Culture of C6 glioma rat cell line and A549 non-small lung cancer human cell line 16
2.1 Dulbecco's modified eagle medium (DMEM) with high glucose 16
2.2 Phosphate buffered saline (PBS) buffer 16
2.3 Passaging cell line 16
2.4 Cell freezing and thawing 17
3 Culture conditions and serotyping of Klebsiella pneumoniae 17
4 Acanthamoeba genomic DNA extraction. 18
5 Acanthamoeba RNA extraction. 19
6 Reverse transcription polymerase chain reaction (RT-PCR) 19
7 Phagocytosis and encystation tests 20
8 PCR products sequencing and bioinformatic analysis 20
9 Immunofluorescence staining 20
10 Endosymbionts DNA extraction 21
11 Bacterial 16S Ribosomal RNA (16S rRNA) Sequencing 21
12 Metagenomics analysis 22
13 Gene Abundance Comparison 22
14 Bacteria processing 23
15 Adhesion assays 23
16 Analysis of secreted proteins neutralization 24
17 Cytopathic effect (CPE) analysis 24
18 Lactate dehydrogenase (LDH) assay 24
19 Time-course and image capture 25
20 Western blotting 25
21 Ex vivo mouse model 26
22 Sampling of dominant commensals on the ocular surface 26
23 Klebsiella pneumoniae stimulation by Acanthamoeba 27
24 India ink staining 27
25 String test 28
26 Hypermucoviscosity assay 28
27 Serum resistance assay 28
28 Klebsiella pneumoniae cytotoxicity assay 28
29 Phenol-sulfuric acid assay 29
30 Sedimentation assay 29
31 Quantitative of capsule associated genes 29
32 Extracellular proteins separation 30
33 External ions analysis 30
34 Statistical analysis 30
CHAPTER 4 Results 32
1 Acanthamoeba Shwachman-Diamond syndrome (AcSBDS) interacts with bacteria during phagocytosis 32
2 The AcSBDS specific primers were evaluated and reliable 32
3 AcSBDS247 was mainly expressed in the Acanthamoeba phagocytosis and encystation 33
4 The stimulations triggered AcSBDS alternative splicing result in two isoforms 33
5 The AcSBDS and actin involved in Acanthamoeba phagocytosis of bacteria 34
6 Collecting the Acanthamoeba isolates from various disease progression 35
7 The designed 16S rRNA primers were used in endosymbionts analysis 35
8 Clostridiales and Bacteroidales are the major endosymbionts of isolates 36
9 Blautia product showed abundance in the isolates of severe Acanthamoeba keratitis 36
10 heat-killed bacteria reduced Acanthamoeba pathogenicity in C6 cells 37
11 The intact bacteria interfered with amoeba crawling in position 38
12 The bacteria affected Acanthamoeba cytotoxicity but not adhesion and secreted proteins 38
13 The presence of bacteria interfered with the phagocytic ability of Acanthamoeba 38
14 The preservation of epithelial cell junctions by bacteria 39
15 The integrity of corneal epithelium is preserved by ocular commensals during the Acanthamoeba invasion 39
16 Food source bacteria were dominant commensals on the human ocular surface 40
CHAPTER 5 Discussion and future perspective 41
1 The first report of AcSBDS in Acanthamoeba and its association with phagocytosis 41
2 The anaerobic gram-positive bacillus abundance may be associated with Acanthamoeba pathogenicity 41
3 The ocular surface dysbiosis might result from Acanthamoeba ingestion of ocular commensals 42
4 Endosymbionts analysis could be a target for diagnosis of Acanthamoeba keratitis progression 43
5 The commensals interfere Acanthamoeba phagocytosis during infection 44
6 Cell junction proteins were preserved in the presence of the commensals 44
7 Healthy microbiota serve as a natural barrier against Acanthamoeba invasion 45
8 The immune resistance and cytotoxicity of Klebsiella pneumoniae were elevated after co-culture with Acanthamoeba 46
9 The capsule of K. pneumoniae becomes thickened and maintained after three-times passage 46
10 Co-cultured K. pneumoniae possessed abundant polysaccharides and were
transformed into a hypermucoviscosity strain 47
11 The enhancement of K. pneumoniae capsule biosynthesis resulted from the ions alteration by Acanthamoeba 48
12 Acanthamoeba enhanced the capsule biosynthesis of K. pneumoniae in various serotypes and clinical isolates 49
13 Investigation of the source of hypervirulence of Klebsiella pneumoniae is a critical issue 50
14 Acanthamoeba microenvironment alteration impacts surrounding bacteria 51
15 Acanthamoeba provide a microenvironmental stimulation to a wide variety of K. pneumoniae serotypes 51
16 Conclusions and future perspectives 52
CHAPTER 6 References 54
APPENDIX I Acanthamoeba SBDS proteins, including the rRNA metabolism protein (ACA1_142090) 109
APPENDIX II Acanthamoeba Shwachman-Bodian-Diamond syndrome (SBDS) protein (ACA1_204560) 110
APPENDIX III Comparison of endosymbionts' relative expression between keratitis and environmental isolates 111
APPENDIX IV Comparison of endosymbionts' relative expression between late and early keratitis 115
APPENDIX V Quantification measurement of corneal epithelium viability 117
APPENDIX VI The journal publication 118
                                    

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