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系統識別號 U0026-0302201517004900
論文名稱(中文) 土壤微生物體與生物刺激掩埋反應槽促進多氯戴奧辛污染土壤生物復育
論文名稱(英文) Soil Microbiome Approach and Biostimulating Landfill Reactor for Enhancing Bioremediation of Polychlorinated Dioxin-Contaminated Soil
校院名稱 成功大學
系所名稱(中) 環境工程學系
系所名稱(英) Department of Environmental Engineering
學年度 103
學期 1
出版年 104
研究生(中文) 陳薇羽
研究生(英文) Wei-Yu Chen
電子信箱 weiuie.chen@gmail.com
學號 P58961041
學位類別 博士
語文別 英文
論文頁數 197頁
口試委員 指導教授-張祖恩
指導教授-吳哲宏
口試委員-胡苔莉
口試委員-高志明
口試委員-童心欣
口試委員-曾怡禎
中文關鍵字 多氯二聯苯戴奧辛  土壤微生物體  生物復育  高通量定序  功能性基因 
英文關鍵字 Polychlorinated dibenzofurans and polychlorinated dibenzo-p-dioxins  soil microbiome  bioremediation  high-throughput sequencing  functional gene 
學科別分類
中文摘要 含氯戴奧辛同源物有210種同源物,是自然或人為的燃燒程序產生,也是許多工業製程的不純物。因強烈的疏水性與頑固性,不斷地在土壤環境中累積,其中以八氯同源物濃度最高。含氯戴奧辛透過生物鏈濃縮放大效應,會造成嚴重的生態威脅與健康風險的問題。土壤與堆肥中含多樣而特殊微生物菌群,可分解戴奧辛同源物,利用這些關鍵的微生物以及含有的基因與代謝活性,可發展出有效、成本可負擔且對環境友善的生物復育整治方法,減少戴奧辛對環境生態的危害。但是,目前有關降解高氯數戴奧辛同源物的微生物種類、數量、分佈,以及分解戴奧辛的生化代謝機制的瞭解仍然相當有限。本論文主要目的為研究高氯數戴奧辛生物降解的土壤微生物多樣性與功能,並發展一套污染土壤生物處理系統,提供未來處理污染場址戴奧辛污染之參考方案。
首先,將戴奧辛污染土壤與營養鹽植入血清瓶,進行好氧共代謝降解批次試驗。經過6個星期,土壤中八氯二聯苯呋喃與七氯二聯苯呋喃的濃度由912.7 μmol/kg與88.8 μmol/kg降至0.28 μmol/kg和0.24 μmol/kg,降解速率分別為20.3 μmol/kg/day和2.0 μmol/kg/day,並觀察到脫氯同源物短暫累積。隨後,將批次試驗的泥水轉植至含50 mg八氯二聯苯呋喃粉末的基礎培養基中,培養3個星期後,發現八氯二聯苯呋喃由5,096 μmol/kg減少至913 μmol/kg,去除率高達82.1%,降解速率為199 μmolkg/day。批次試驗結果指出八氯二聯苯呋喃可生物分解。以選殖分子生物技術分析微生物菌群結構,結果顯示98.3%的微生物菌群屬於Proteobacteria。進一步,配合階層寡核苷酸引子延伸定性定量技術發現,當批次試驗的八氯二聯苯呋喃濃度減少時,Micrococcus、Rhizobium、Pseudoxanthomonas和Brevudimonas菌群相對豐富度顯著地增加。另一方面,利用聚合酵素鏈鎖反應篩選從戴奧辛污染土壤分離具戴奧辛雙氧氧化酵素基因的菌株,且經過21天降解測試,Bacillus sp. B2、Rhodococcus erythropolis B11、Micrococcus sp. B43、Sphingomonadaceae sp. M2_1及Mesorhizobium sp. M3對八氯二聯苯呋喃的平均降解率為26%-43%,此結果指出污染土壤中存在複雜多樣化具有降解高氯數戴奧辛同源物能力的菌種。
接著,利用次世代高通量定序技術分析戴奧辛污染土壤菌群結構。結果顯示戴奧辛原始污染土壤菌群結構與批次試驗的菌群結構有很大的差異。戴奧辛原始污染土壤以Proteobacteria為主;而批次試驗降解初期,Firmicutes分別佔總菌群的33.6%及80.5%,批次試驗降解末期,豐富度最高的菌群為Proteobacteria,佔總菌群的56.7%與41.9%。進一步透過主成份分析結果指出,厭氧菌Sedimentibacter與好氧菌Brevundimonas、Pseudoxanthomonas與Lysobacter分別在八氯二聯苯呋喃降解前後期扮演重要角色。綜合本研究結果推測,雖然有供氧,血清瓶中實際呈現缺氧環境,在好氧性與厭氧性微生物同時存活下,促進八氯二聯苯呋喃脫氯與氧化分解反應。本研究透過次世代高通量定序技術發現污染土壤中微生物多樣性極為豐富,且存在可有效降解戴奧辛的關鍵菌株。
從污染場址分離出的Rhodococcus erythropolis B11對於八氯二聯苯呋喃與其他苯環化合物有不錯的降解能力。B11 菌株全基因體定序分析結果顯示,獲得的染色體序列為6,838,862 bp,G+C值為62.5%,鑑定到的蛋白質與基因數量分別高達6,332及6,748個。依照蛋白質相鄰同源簇功能類型的註解,代謝相關 (Metabolism) 的蛋白質數量的比例最多,佔總基因體的35.0 %。訊息儲存與處理、細胞程序與信號傳遞相關蛋白質的數量比例分別是12.4 %和9.2 %,而大約有14.0 -29.4%的蛋白質功能是不清楚或尚無法註解。
B11基因體至少含有10種不同環狀化合物的雙加氧酵素,顯示此菌株具有多樣化降解苯環化合物的能力。B11菌株可透過四種途徑 (TreS、OtsA-OtsB、TreP與TreY-TreZ) 產生生物界面活性劑-海藻糖,環境污染物的增溶能力改變而更容易被利用。除此之外,首次發現Rhodococcus erythropolisB11具有調節與還原汞能力的汞操縱子相關基因-merR與merA。親緣分析顯示汞操縱子可能是經由Janibacter hoylei水平基因轉移至B11。這些功能性基因分析指出此菌株具有運用在環境有機與無機污染物生物復育的潛力。
最後,本研究設計一套掩埋反應槽,添加堆肥後,控制氧化還原電位於缺氧的環境下 (好氧/厭氧條件交替循環),測試實際污染土壤的處理效率。經過280天的操作,R6 (添加10% 污泥堆肥) 與R7 (添加5% 污泥堆肥和5%牛糞堆肥) 反應槽的戴奧辛總毒性當量去除率分別達53%及79 %,遠高於控制組無堆肥添加的反應槽 (27 %),顯示添加堆肥生物復育程序成功地促進多氯戴奧辛的脫氯與氧化裂環反應。同時,結合高通量定序技術分析掩埋反應槽菌群結構變化,除了數種好氧性的戴奧辛分解菌群,發現戴奧辛毒性當量的降低與厭氧菌群Clostridium菌群豐富度增加有相當高的關聯性,且堆肥添加增加反應槽微生物多樣性,有助於戴奧辛毒性當量穩定地的降低。本研究成功地展示生物強化土壤掩埋反應槽系統處理多氯戴奧辛污染土壤的可行性。這項生物復育技術與操控參數已具實際應用的雛型,可提供未來污染場址如安順廠址整治之參考。
英文摘要 Polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs), collectively called “dioxins”, comprise 210 congeners and are by-products of combustion and industrial manufacturing processes. Because of their strong hydrophobicity and xenobiotic nature, a high concentration of PCDD/Fs has accumulated in the soil environment. Octachloro DD/Fs are among the most abundant congeners distributed. Through bioaccumulation in the food chain, it already poses a serious ecological threat and health risk. Soil and compost are inhabited by diverse microbial populations that reportedly can decompose chlorinated dioxins. Potentially, these microorganisms with relevant genes and metabolic activities can be used to develop an efficient, cost-effective, and environmentally friendly bioremediation method for reducing the concentration of PCDD/Fs in soil. However, understanding of the microbial population quantity, distribution, and role in PCDD/F biodegradation remains limited. The aim of this thesis was to examine the soil microbiome (i.e., microbial community structure and functionality) associated with PCDD/F contamination and develop a biological treatment system for removing PCDD/F toxicants from a contaminated site.
To study the feasibility of bioremediation, closed microcosms were constructed with PCDD/Fs-contaminated soil in oxygen-stimulating conditions. After incubation for 6 weeks, octachlorodibenzofuran (OCDF) decreased by 330 mg/kg, whereas heptachlorodibenzofuran (HpCDF) concentration decreased from 88.8 to 0.24 μmol/kg. To further validate the degradation of OCDFs, microbial consortia from the first-batch experiment were transferred to serum bottles containing fresh minimal medium and 50 mg of OCDF powder. The results showed that the OCDF decreased from 5096 to 913 μmol/kg after 3 weeks, which corresponded to an efficiency of 82.1% and a degradation rate of 199 μmol/kg/day. Clone library analysis of a polymerase chain reaction-amplified 16S rRNA gene from the OCDF-degrading consortia determined that 98.3% of the detected sequences were affiliated with Proteobacteria. Hierarchical oligonucleotide primer extension analysis revealed that Micrococcus, Rhizobium, Pseudoxanthomonas, and Brevudimonas-related populations increased sharply when high concentrations of OCDF decreased. Furthermore, the obtained strains with putative aromatic dioxygenase genes were closely related to the members of Actinobacteria, Firmicutes, and Proteobacteria. Among the members of Actinobacteria, Firmicutes, and Proteobacteria, certain Rhodococcus, Micrococcus, Mesorhizobium, and Bacillus strains degrade OCDF with efficiencies of 26% to 43% within 21 days. This study determined that the contaminated soil evolved diverse bacterial populations able to degrade highly chlorinated dioxins.
Next-generation high-throughput sequencing technology was used to determine the microbial composition and population dynamics transited from the original soil to the OCDF microcosms. The results of 16S rRNA gene analysis showed complex microbial diversity in the PCDD/F-contaminated soil and revealed that the community composition changed considerably, becoming concomitant with the OCDF degradation; thus, the distinctive population structure developed rapidly in the OCDF microcosm. Anaerobic Sedimentibacter (within Firmicutes) emerged first, and several aerobic participants, such as Brevudimonas (within Alphaproteobacteria), Pseudoxanthomonas, and Lysobacter (within Gammaproteobacteria) increased considerably within the timeframe. The results revealed a temporal population dynamic and collaborative contributions to OCDF degradation under hypoxic conditions.
Rhodococcus erythropolis effectively degraded PCDD/Fs and aromatic compounds. To study microbial functionality, strain B11 was isolated from the PCDD/F-contaminated soil and decoded. Genome sequencing yielded a draft genome of 6 838 862 bp, with a guanine-cytosine content of 62.5%. The draft genome contained 6748 genes and 6332 protein-coding sequences (CDSs; 94% of the entire genome). These CDSs exhibited a distinct distribution pattern in the functional categories of the Clusters of Orthologous Groups database, reflecting the unique niche of Rhodococcus erythropolis in the contaminated environment. The annotation identified various genetic features that contribute to its lifestyle and the degradation of xenobiotics, indicating the potential of using ring-hydroxylation oxygenase (RHOs) systems to metabolise these xenobiotics. The B11 genome comprises several gene segments that can produce trehalose as a biosurfactant via 4 biosynthetic pathways (i.e., TreS, OtsA-OtsB, TreP, and TreY-TreZ), elucidating its ability to enhance substrate availability for microbial degradation in soil. In addition, merA and merR genes were identified in the B11 genome, suggesting that B11 may regulate mercury resistance and reduce Hg (II) to Hg (0). Phylogenetic analysis revealed a horizontal gene transfer from Janibacter hoylei and genomic analysis showed that the lifestyle of the B11 strain has valuable applications in removing organic and inorganic environmental pollutants.
Lastly, a novel landfill reactor system with compost amendment was developed in this study. Intermittent aeration and leachate recirculation were applied in the reactor to establish hypoxic conditions. After 280 days, the average removal efficiencies of total dioxin toxicity in the R6 (10% sewage sludge compost) and R7 (5% sewage sludge compost and 5% cow manure compost) bioreactors were 53% and 79%, respectively, both higher than that recorded by the control bioreactor (27%). This result suggests that adding compost effectively enhanced the degradation of PCDD/Fs in the landfill reactor operated under hypoxic conditions. In such conditions, the microbial community inside the reactors was dominated by the groups associated with the classes Gammaproteobacteria, Alphaproteobacteria, Actinobacteria, and Clostridia, changing markedly. In particular, the removal of PCDD/Fs strongly correlated with an increase in the population of anaerobic Clostridium. The compost amendment increased the complexity of microbial composition and aided in stably reducing the toxicity equivalence of PCDD/Fs. The stimulating landfill reactor developed in this thesis has field applications, such as the bioremediation of An-shun, the site of a former chemical plant in Southern Taiwan. In conclusion, this thesis study affords insight into the association of the soil microbiome with PCDD/Fs-contaminated soil, microcosms, and landfill reactors developed, and indicates a new direction for future studies on the bioremediation of PCDD/Fs.
論文目次 摘 要 i
Abstract iv
Acknowledgments vii
Table of Contents viii
List of Tables xii
List of Figures xiv
List of Supplementary Tables xvii
List of Supplementary Figures xviii
Abbreviations xix
Chapter 1 Introduction 1
1.1 Background and problem statement 1
1.2 Objectives of this thesis 4
1.3 Outline of thesis infrastructure 5
Chapter 2 Literature Review 7
2.1 Dioxin feature 7
2.2 Microbiology and biochemistry of PCDD/Fs 12
2.2.1 Biodiversity of aerobic bacteria involved 12
2.2.2 Biodiversity of anaerobic bacteria involved 14
2.2.3 Aerobic degradation process 17
2.2.4 Anaerobic degradation process 24
2.3 High-throughput molecular techniques 26
2.3.1 Hierarchical oligonucleotide primer extension 26
2.3.2 High-throughput sequencing 29
Chapter 3 Bioremediation Potential of Soil Contaminated with Highly Substituted Polychlorinated Dibenzo-p-dioxins and Dibenzofurans: Microcosm Study and Microbial Community Analysis 36
3.1 Introduction 36
3.2 Materials and Methods 38
3.2.1. Soil samples 38
3.2.2 Batch microcosm assays 38
3.2.3. PCDD/Fs analysis 39
3.2.4. Soil DNA preparation and microbial composition analysis 40
3.2.5. Hierarchical oligonucleotide primer extension analysis 41
3.2.6. Bacterial isolation, identification and OCDF-degrading ability 42
3.2.7. PCR detection of aromatic dioxygenase-coding genes 43
3.2.8. Nucleotide sequence accession numbers 43
3.3 Results and discussion 46
3.3.1. Degradation of PCDD/Fs in soil microcosms 46
3.3.2. Microbial community structure of PCDD/F-degrading consortium 50
3.3.3. Isolation and identification of OCDF-growing bacterial isolates 53
3.3.4 Characterization of OCDF-growing bacterial isolates 57
3.3.5. Relative abundance of microbial populations as revealed by HOPE analysis 60
3.4. Conclusions 63
Chapter 4 Pyrosequencing Analysis Reveals High Population Dynamics of Soil Microcosm Degrading Octachlorodibenzofuran 64
4.1 Introduction 64
4.2 Materials and methods 65
4.2.1 Soil samples 65
4.2.2 Constructions of AS-G and OCDF microcosms 66
4.2.3 PCDD/Fs analysis 67
4.2.4 DNA recovery and quantitative PCR analysis of 16S rRNA gene 68
4.2.5 Barcoded PCR and 454 pyrosequencing of 16S rRNA gene 68
4.2.6 Pyrosequencing data analysis 69
4.2.7 Nucleotide sequence accession numbers 71
4.3 Results 71
4.3.1 Microbial communities of uncultivated soil with low and high concentrations of PCDD/Fs 71
4.3.2 PCDD/Fs degradation and microbial community in the AS-G microcosm 76
4.3.3 OCDF degradation and microbial community in the OCDF microcosm 76
4.3.4 Comparison of bacterial community structure 79
4.3.5 In silico screening of yet-isolated PCDD/Fs degrader 83
4.4 Discussion 85
Chapter 5 The genome analysis of Rhodococcus erythropolis illuminates the metabolic diversity and potential of environmental pollutants 90
5.1 Introduction 90
5.2 Materials and Methods 91
5.2.1 Bacteria isolation, identification and phylogenetic analysis 91
5.2.2 Biolog GN2 and ECO assays 92
5.2.3 Illumina library construction 92
5.2.4 Illumina Sequencing 93
5.2.5 Cluster of orthologous group of proteins database construction 93
5.3 Results and Discussion 94
5.3.1 Classification and feature 94
5.3.2 Growth in Biolog GN2 well after inoculation with Rhodococcus erythropolis B11 97
5.3.3 Growth in Biolog ECO well after inoculation with Rhodococcus erythropolis B11 97
5.3.4 Growth in Biolog GN2 well after inoculation with Rhodococcus erythropolis B51 97
5.3.5 Growth in Biolog ECO well after inoculation with Rhodococcus erythropolis B51 98
5.3.6 High-quality genomic DNA extraction 98
5.3.7 The sequencing summary for R. erythropolis B11 99
5.3.8 De Novo Assembly 100
5.3.9 Functional categories of coding sequences 102
5.3.10 Genome anatomy and comparative genomics 104
5.3.11 Functional gene similarity between genomes 115
5.3.12 Catabolism of xenobiotics 117
5.3.13 Microbial ring-hydroxylating oxygenases (RHO) 119
5.3.14 Biosurfactant synthesis 123
5.3.15 Functional component of Hg resistance 125
5.4 Conclusion 129
Chapter 6 Microbial Community Structure Change and Process Performance in the Compost Augmented Landfill Reactor Remediating PCDD/Fs-Contaminated Soil 130
6.1 Introduction 130
6.2 Materials and Methods 132
6.2.1 Contaminated soil 132
6.2.2 Landfill reactor setup 132
6.2.3 PCDD/Fs analysis 135
6.2.4 Microbial Community as revealed by pyrosequencing 135
6.3 Result 136
6.3.1 ORP profile 136
6.3.2 PCDD/Fs toxicity removal 137
6.3.3 Overall soil bacterial community structure 140
6.3.4 Bacterial diversity 145
6.3.5 Bacterial community structure 148
6.3.6 Impact of bioreactor on known dioxin degraders 153
6.4 Discussion 155
Chapter 7 Conclusions and Recommendations 159
7.1 Conclusions 159
7.2 Recommendations 162
References 164
Appendix 188
Resume 198
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