基于渗滤液沉积物的甲烷氧化反硝化耦合微生物学机理研究
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摘要
长期处于高浓度有机物和高浓度氨氮胁迫下的渗滤液收集池沉积物是一种极端环境。这种特殊的生境中可能存在着特异性代谢的微生物类群,尤其是耐高浓度有机质和氨氮的碳氮元素转化微生物。近年来,甲烷氧化反硝化耦合(Methane oxidation coupled to denitrification, MOD)过程由于其耗能少,反应器设计简单,受到了研究者的广泛关注,但是其微生物学机理还未有明确定论。本研究以浙江省东阳市生活垃圾填埋场16年龄渗滤液收集池沉积物(0-8cm层)为研究对象,采用现代分子生物学技术,详细分析了高浓度氨氮和有机物胁迫下的渗滤液沉积物原核微生物群落结构、组成多样性,及其潜在的微生物代谢过程；以该渗滤液沉积物为接种体,在微好氧条件下开展了MOD污泥的富集培养及其甲烷氧化与反硝化耦合性能研究；并以功能基因-分子克隆技术探索了富集的MOD功能微生物群落结构与耦合机理。研究结果对开发微生物种质资源以及废水生物处理新工艺具有重要的现实意义。研究主要结论如下：
(1)以东阳市垃圾填埋场16年龄渗滤液收集池沉积物(0-8cm层)为研究对象,采用PCR-分子克隆技术结合16S rRNA基因系统发育分析阐明了渗滤液沉积物中的古菌群落结构与组成多样性,并发现渗滤液沉积物中可能存在氨氧化古菌。通过对随机挑选的425个古菌克隆子的59个基因型系统发育分析,发现渗滤液沉积物中的古菌分属广古菌门(Euryarchaeota)和泉古菌门(Crenarchaeota);其中属于广古菌门基因型45个,代表了397个古菌16SrRNA基因克隆,占库容的93.41%,与产甲烷古菌有较高的同源性,主要为甲烷微菌目(Methanomicrobiales)、甲烷八叠球菌目(Methanosarcinales)和甲烷杆菌目(Methanobacteriales)产甲烷古菌,并以甲烷鬃菌属(Methanosaeta spp.)为优势种群。14个泉古菌门基因型代表了28个古菌16S rRNA基因克隆,与环境样品来源的序列同源性较高。泉古菌门克隆B9与Candidatus 'Nitrosophaera gargensis'同源性高达98.3%。
(2)细菌16S rRNA基因克隆文库揭示了渗滤液沉积物中有机质降解与氮素转化相关微生物的群落结构。多样性指数分析表明,渗滤液沉积物中细菌的多样性明显高于古菌,群落结构也更复杂。代表313个细菌16S rRNA基因克隆的244个基因型,分属于18个细菌分类门。厚壁菌门(Firmicute)和变形菌门(Proteobacteria)细菌是渗滤液沉积物的主要细菌类群,分别占克隆文库库容的21.60%和19.20%。细菌克隆中超过50%的基因型与未培养微生物同源性较高。部分基因型与Genbank中已发表的序列同源性较低,在系统发育学上可能属于新的微生物类群。α-、β-和γ-变形菌亚纲的部分基因型与化能有机营养型反硝化菌同源性较高,推测这些细菌在渗滤液沉积物碳氮元素转化过程中发挥着重要作用。厚壁菌门(Firmicute)梭菌纲(Clostridia)的发酵型细菌、产氢、产乙酸菌等化能有机营养型细菌能够为产甲烷古菌提供H2,CO2,甲基化合物和乙酸等底物,构成了渗滤液沉积物中的产甲烷菌群。氨氧化古菌和氨氮利用型细菌可能具有转化氨氮的功能,并因此形成一个低浓度氨氮小生境,从而减轻或者避免了渗滤液沉积物中高浓度氨氮对其他微生物的抑制或毒害作用。尽管渗滤液沉积物细菌和古菌的群落结构与其他文献报道的渗滤液微生物群落有一定的相似性,但由于渗滤液水质和气候等条件的不同,渗滤液与沉积物理化性质的差别较大,垃圾渗滤液和沉积物中的微生物群落组成与结构多样性存在显著性差异。
(3)以东阳垃圾填埋场16年龄渗滤液收集池沉积物(0-8cm层)为接种体,甲烷为唯一外加碳源,硝酸盐和亚硝酸盐为电子受体,在微好氧条件下,成功富集了以革兰氏阴性菌为主体的MOD污泥。稳定运行阶段含MOD污泥反应器的反硝化速率为4.5mmol N L-1d-1.血清瓶活性试验表明提高反应器配水溶解氧可显著促进富集污泥的反硝化活性,首次证实了反应器中配水硝酸盐与亚硝酸盐的还原是由于好氧反硝化微生物的作用。富集培养与活性试验水质GC-MS分析结果表明,甲醛、柠檬酸盐和乙酸盐是甲烷氧化代谢过程形成的主要有机物。
(4)以甲烷氧化功能基因pmoA和反硝化功能基因nirK分子克隆结合荧光定量PCR技术为研究手段,考察了富集培养的MOD污泥功能微生物群落结构及其基因丰度。结果表明,富集的MOD污泥中存在大量的甲烷氧化菌和反硝化细菌,甲烷氧化pmoA基因拷贝数约为反硝化nirK基因拷贝数的3倍。属于γ-变形菌亚纲(Gammaproteobacteria)甲基球菌科(Methylococcaceae)的TypeⅠ型甲烷氧化菌是富集培养MOD污泥优势的甲烷氧化菌群,占总细菌16SrRNA基因克隆文库库容的37.50%,并以甲基杆菌属(Methylobacter spp.)和甲基暖菌属(Methylocaldum spp.)为优势种群；β-变形菌亚纲(Betaproteobacteria)嗜甲基菌科(Methylophilaceae)的甲基营养型好氧反硝化菌是该富集污泥的主要反硝化微生物类群,占总细菌16S rRNA基因克隆文库库容的36.76%。
综上所述,本研究采用功能基因结合分子克隆技术首次阐明了MOD微生物学机理：Type I型的γ-变形菌亚纲(Gammaproteobacteria)甲基球菌科(Methylococcaceae)甲基杆菌属(Methylobacter spp.)和甲基暖菌属(Methylocaldum spp.)的甲烷氧化菌氧化甲烷,并采用5-磷酸核酮糖途径(RuMP Pathway)同化碳源产生甲醛、柠檬酸盐和乙酸盐等可溶性简单有机物,在微好氧的条件下,为β-变形菌亚纲(Betaproteobacteria)嗜甲基菌科(Methylophilaceae)的好氧反硝化菌提供电子供体,进行硝酸盐或亚硝酸盐的好氧反硝化作用。
Sediment in leachate collection ponds is an extreme environment with considerably high of ammonium and organic matter concentration. Therefore, there might be some specific microognaisms which metabolize in differential pathway in this special habitat, especially carbon and nitrogen transforming microorganisms which could bear high amounts of organic matters and ammonium. Recently, methane oxidation coupled to denitrification (MOD) was attracted much attention due to less energy consumption and simple design reactor. However, the mechanisms and microbial community of this process have not yet been confirmed. In this thesis, sediment (0-8cm) in the16years old leachate collection pond of Dongyang Landfill in Zhejiang Province was taken as the research object. Prokaryotic diversity, composition structure and the potential microbial metabolic processes in leachate sediment ecosystems were analysed by modern molecular biotechnology. With the leachate sediment as inoculum, a consortium involved in MOD was enriched under micro-aerobic condition. Methane oxidation activity and denitrification acitivity of the enrichment reactor were determined.16S rRNA gene phylogeny combined with pmoA gene-based phylogeny of methanotrophs and nirK gene-based phylogeny of denitrifiers were analyzed to reveal the pivotal microbial populations and functional microorganisms. Functional genes combined with molecular cloning technique were performed to identify the primary functional microorganisms and coupling mechanism involved in MOD system. Results of this study would be significant in exploring microbial resources and new technologies for biological wastewater treatment. Main results of the study were summaried as follows:
(1) Sediment (0-8cm) in the16years old leachate collection pond of Dongyang Landfill in Zhejiang Province was taken as the research object. Archeael diversity and community structure was illuminated using PCR (polymerase chain reaction)-molecular cloning technique combined with phylogenetic analysis of16S rRNA gene. It was suggested that ammonium-oxidizing crenarchaeote might exist in leachate sediment. A total of59phylotypes affiliated with two phyla Euryarchaeota and Crenarchaeota were examined among425randomly selected archaeal rDNA clones. Among them,45phylotypes were identified as Euryarhaeota, representing397out of the total425clones, accounting for93.41%of the total archaeal clones. All of the euryarhaeotic clones were closely related to methanogens, mainly belonging to Methanomicrobiales, Methanosarcinales and Methanobacteriales. Methanosaeta spp. was the dominant spcies. Fourteen crenarchaeotic phylotypes, representing28clones, had relatively high level (>95%) of similarity with unclassified environmental clones, except that clone B9was98.3%indentical to a moderately thermophilic ammonium-oxidizing crenarchaeote "Candidatus Nitrososphaera gargensis"
(2) Phylogenetic analysis of the bacterial16S rRNA gene clone library revealed the population of organic matter degrading and ammonium transforming microorganisms. Analysis of the diversity indexes indicated that compared to archaeal community, the bacterial community associated with the landfill leachate sediment was much more diverse and complicated. Two hundred and forty four phylotypes were affiliated with18distinct phyla, representing313bacterial clones. Bacteria belonging to Firmicute and Proteobacteria were the dominant populations, accounting for21.60%and19.20%of the total bacterial clones, respectively. More than50%of bacterial clones had high levels of similarity with unculure bacteria. A substantial fraction of bacterial clones showed low levels of similarity with any previously documented sequences and thus might be taxonomically new. Some phylotypes belonging to Alpha-, Beta-and Gammaproteobacteria were affiliated with chemoorganoheterotroph denitrifiers. It was inferred that these bacteria played an important role in carbon and nitrogen transforming precess in the leachate sediment. Chemoorganotrophy bacteria, such as fermentative bacteria, acetogenic bacteria, and hydrogen producing bacteria, which belonged to phylum Firmicuteand order Clostridia, would provide methanogens with substrates, including acetate, H2/CO2and methylated compounds. These collections of different microbial species were referred to as a methanogenic consortium. Ammonium-oxidizing archaea and ammonium utilizing microorganisms might consume surrounding ammonium to form a relatively low ammonium microenvironment and to alleviate or avoid negative influence on other microorganisms. There were a degree of resemblances in the microbial populations between leachate sediment of current study and leachate of other references. However, distinct landfill circumstances, various climate conditions, and different physicochemical properties would result in discrepant microbial communities in leachate and leachate sediment.
(3) Taking the leachate sediment (0-8cm) of16years old in Dongyang Landfill as inoculum, a consortium which was mainly gram-negative bacteria, involved in MOD was successfully enriched under micro-aerobic condition, with methane as external carbon source, nitrite and nitrate as electron acceptor. The denitrification rate of the MOD reactor was around4.5mmol N L-1d-1at the steady period. The batch experiment suggested that more oxygen providing in the reactor would favor a more efficient denitrification, which indicated that nitrite and nitrate depletions might be associated with aerobic denitrification. GC-MS analysis of the influent and effluent liquid of enrichment and batch experiment cultures demonstrated that methanotrophs produced high amount of formaldehyde, citrate, and acetate during the methane oxidation process.
(4) Composition and abundance of primary functional microbial communities in the MOD ecosystem were investigated by pmoA gene-based phylogeny of methanotrophs and nirK gene-based phylogeny of denitrifiers conbined with real-time PCR. There were amount of methanotrophs and denitrifiers in the enriched sludge, and the copy number of pmoA gene were almost3times more than that of nirK gene. Microbial community in the enrichment culture was dominated by Type I methanotrophs, which belonged to Methylococcaceae, Gammaproteobacteria, comprising37.5%of the total bacterial16S rRNA gene clone library. The Methylobacter spp. and Methylocaldum spp. were the dominant population. Aerobic methylotrophic denitrifiers of Methylophilaceae, Betaproteobacteria, might make great contribution in denitrification in our MOD ecosystems, comprising36.76%of the total bacterial16S rRNA gene clone library.
In conclusion, the microbiological mechanism of the MOD system in this study was that type I methanotrophs, which belonged to Methylobacter spp. and Methylocaldum spp., Methylococcaceae, Gammaproteobacteria, oxidized methane, employed the ribulose monophosphate (RuMP) pathway for assimilation and released organic intermediates (i.e. formaldehyde, citrate, and acetate) under mireo-aerobic condition. Aerobic methylotrophic denitrifiers of Methylophilaceae, Betaproteobacteria, utilizing organic intermediates released from the methanotrophs as electron donor, played a vital role in aerobic denitrification.
(1)以东阳市垃圾填埋场16年龄渗滤液收集池沉积物(0-8cm层)为研究对象,采用PCR-分子克隆技术结合16S rRNA基因系统发育分析阐明了渗滤液沉积物中的古菌群落结构与组成多样性,并发现渗滤液沉积物中可能存在氨氧化古菌。通过对随机挑选的425个古菌克隆子的59个基因型系统发育分析,发现渗滤液沉积物中的古菌分属广古菌门(Euryarchaeota)和泉古菌门(Crenarchaeota);其中属于广古菌门基因型45个,代表了397个古菌16SrRNA基因克隆,占库容的93.41%,与产甲烷古菌有较高的同源性,主要为甲烷微菌目(Methanomicrobiales)、甲烷八叠球菌目(Methanosarcinales)和甲烷杆菌目(Methanobacteriales)产甲烷古菌,并以甲烷鬃菌属(Methanosaeta spp.)为优势种群。14个泉古菌门基因型代表了28个古菌16S rRNA基因克隆,与环境样品来源的序列同源性较高。泉古菌门克隆B9与Candidatus 'Nitrosophaera gargensis'同源性高达98.3%。
(2)细菌16S rRNA基因克隆文库揭示了渗滤液沉积物中有机质降解与氮素转化相关微生物的群落结构。多样性指数分析表明,渗滤液沉积物中细菌的多样性明显高于古菌,群落结构也更复杂。代表313个细菌16S rRNA基因克隆的244个基因型,分属于18个细菌分类门。厚壁菌门(Firmicute)和变形菌门(Proteobacteria)细菌是渗滤液沉积物的主要细菌类群,分别占克隆文库库容的21.60%和19.20%。细菌克隆中超过50%的基因型与未培养微生物同源性较高。部分基因型与Genbank中已发表的序列同源性较低,在系统发育学上可能属于新的微生物类群。α-、β-和γ-变形菌亚纲的部分基因型与化能有机营养型反硝化菌同源性较高,推测这些细菌在渗滤液沉积物碳氮元素转化过程中发挥着重要作用。厚壁菌门(Firmicute)梭菌纲(Clostridia)的发酵型细菌、产氢、产乙酸菌等化能有机营养型细菌能够为产甲烷古菌提供H2,CO2,甲基化合物和乙酸等底物,构成了渗滤液沉积物中的产甲烷菌群。氨氧化古菌和氨氮利用型细菌可能具有转化氨氮的功能,并因此形成一个低浓度氨氮小生境,从而减轻或者避免了渗滤液沉积物中高浓度氨氮对其他微生物的抑制或毒害作用。尽管渗滤液沉积物细菌和古菌的群落结构与其他文献报道的渗滤液微生物群落有一定的相似性,但由于渗滤液水质和气候等条件的不同,渗滤液与沉积物理化性质的差别较大,垃圾渗滤液和沉积物中的微生物群落组成与结构多样性存在显著性差异。
(3)以东阳垃圾填埋场16年龄渗滤液收集池沉积物(0-8cm层)为接种体,甲烷为唯一外加碳源,硝酸盐和亚硝酸盐为电子受体,在微好氧条件下,成功富集了以革兰氏阴性菌为主体的MOD污泥。稳定运行阶段含MOD污泥反应器的反硝化速率为4.5mmol N L-1d-1.血清瓶活性试验表明提高反应器配水溶解氧可显著促进富集污泥的反硝化活性,首次证实了反应器中配水硝酸盐与亚硝酸盐的还原是由于好氧反硝化微生物的作用。富集培养与活性试验水质GC-MS分析结果表明,甲醛、柠檬酸盐和乙酸盐是甲烷氧化代谢过程形成的主要有机物。
(4)以甲烷氧化功能基因pmoA和反硝化功能基因nirK分子克隆结合荧光定量PCR技术为研究手段,考察了富集培养的MOD污泥功能微生物群落结构及其基因丰度。结果表明,富集的MOD污泥中存在大量的甲烷氧化菌和反硝化细菌,甲烷氧化pmoA基因拷贝数约为反硝化nirK基因拷贝数的3倍。属于γ-变形菌亚纲(Gammaproteobacteria)甲基球菌科(Methylococcaceae)的TypeⅠ型甲烷氧化菌是富集培养MOD污泥优势的甲烷氧化菌群,占总细菌16SrRNA基因克隆文库库容的37.50%,并以甲基杆菌属(Methylobacter spp.)和甲基暖菌属(Methylocaldum spp.)为优势种群；β-变形菌亚纲(Betaproteobacteria)嗜甲基菌科(Methylophilaceae)的甲基营养型好氧反硝化菌是该富集污泥的主要反硝化微生物类群,占总细菌16S rRNA基因克隆文库库容的36.76%。
综上所述,本研究采用功能基因结合分子克隆技术首次阐明了MOD微生物学机理：Type I型的γ-变形菌亚纲(Gammaproteobacteria)甲基球菌科(Methylococcaceae)甲基杆菌属(Methylobacter spp.)和甲基暖菌属(Methylocaldum spp.)的甲烷氧化菌氧化甲烷,并采用5-磷酸核酮糖途径(RuMP Pathway)同化碳源产生甲醛、柠檬酸盐和乙酸盐等可溶性简单有机物,在微好氧的条件下,为β-变形菌亚纲(Betaproteobacteria)嗜甲基菌科(Methylophilaceae)的好氧反硝化菌提供电子供体,进行硝酸盐或亚硝酸盐的好氧反硝化作用。
Sediment in leachate collection ponds is an extreme environment with considerably high of ammonium and organic matter concentration. Therefore, there might be some specific microognaisms which metabolize in differential pathway in this special habitat, especially carbon and nitrogen transforming microorganisms which could bear high amounts of organic matters and ammonium. Recently, methane oxidation coupled to denitrification (MOD) was attracted much attention due to less energy consumption and simple design reactor. However, the mechanisms and microbial community of this process have not yet been confirmed. In this thesis, sediment (0-8cm) in the16years old leachate collection pond of Dongyang Landfill in Zhejiang Province was taken as the research object. Prokaryotic diversity, composition structure and the potential microbial metabolic processes in leachate sediment ecosystems were analysed by modern molecular biotechnology. With the leachate sediment as inoculum, a consortium involved in MOD was enriched under micro-aerobic condition. Methane oxidation activity and denitrification acitivity of the enrichment reactor were determined.16S rRNA gene phylogeny combined with pmoA gene-based phylogeny of methanotrophs and nirK gene-based phylogeny of denitrifiers were analyzed to reveal the pivotal microbial populations and functional microorganisms. Functional genes combined with molecular cloning technique were performed to identify the primary functional microorganisms and coupling mechanism involved in MOD system. Results of this study would be significant in exploring microbial resources and new technologies for biological wastewater treatment. Main results of the study were summaried as follows:
(1) Sediment (0-8cm) in the16years old leachate collection pond of Dongyang Landfill in Zhejiang Province was taken as the research object. Archeael diversity and community structure was illuminated using PCR (polymerase chain reaction)-molecular cloning technique combined with phylogenetic analysis of16S rRNA gene. It was suggested that ammonium-oxidizing crenarchaeote might exist in leachate sediment. A total of59phylotypes affiliated with two phyla Euryarchaeota and Crenarchaeota were examined among425randomly selected archaeal rDNA clones. Among them,45phylotypes were identified as Euryarhaeota, representing397out of the total425clones, accounting for93.41%of the total archaeal clones. All of the euryarhaeotic clones were closely related to methanogens, mainly belonging to Methanomicrobiales, Methanosarcinales and Methanobacteriales. Methanosaeta spp. was the dominant spcies. Fourteen crenarchaeotic phylotypes, representing28clones, had relatively high level (>95%) of similarity with unclassified environmental clones, except that clone B9was98.3%indentical to a moderately thermophilic ammonium-oxidizing crenarchaeote "Candidatus Nitrososphaera gargensis"
(2) Phylogenetic analysis of the bacterial16S rRNA gene clone library revealed the population of organic matter degrading and ammonium transforming microorganisms. Analysis of the diversity indexes indicated that compared to archaeal community, the bacterial community associated with the landfill leachate sediment was much more diverse and complicated. Two hundred and forty four phylotypes were affiliated with18distinct phyla, representing313bacterial clones. Bacteria belonging to Firmicute and Proteobacteria were the dominant populations, accounting for21.60%and19.20%of the total bacterial clones, respectively. More than50%of bacterial clones had high levels of similarity with unculure bacteria. A substantial fraction of bacterial clones showed low levels of similarity with any previously documented sequences and thus might be taxonomically new. Some phylotypes belonging to Alpha-, Beta-and Gammaproteobacteria were affiliated with chemoorganoheterotroph denitrifiers. It was inferred that these bacteria played an important role in carbon and nitrogen transforming precess in the leachate sediment. Chemoorganotrophy bacteria, such as fermentative bacteria, acetogenic bacteria, and hydrogen producing bacteria, which belonged to phylum Firmicuteand order Clostridia, would provide methanogens with substrates, including acetate, H2/CO2and methylated compounds. These collections of different microbial species were referred to as a methanogenic consortium. Ammonium-oxidizing archaea and ammonium utilizing microorganisms might consume surrounding ammonium to form a relatively low ammonium microenvironment and to alleviate or avoid negative influence on other microorganisms. There were a degree of resemblances in the microbial populations between leachate sediment of current study and leachate of other references. However, distinct landfill circumstances, various climate conditions, and different physicochemical properties would result in discrepant microbial communities in leachate and leachate sediment.
(3) Taking the leachate sediment (0-8cm) of16years old in Dongyang Landfill as inoculum, a consortium which was mainly gram-negative bacteria, involved in MOD was successfully enriched under micro-aerobic condition, with methane as external carbon source, nitrite and nitrate as electron acceptor. The denitrification rate of the MOD reactor was around4.5mmol N L-1d-1at the steady period. The batch experiment suggested that more oxygen providing in the reactor would favor a more efficient denitrification, which indicated that nitrite and nitrate depletions might be associated with aerobic denitrification. GC-MS analysis of the influent and effluent liquid of enrichment and batch experiment cultures demonstrated that methanotrophs produced high amount of formaldehyde, citrate, and acetate during the methane oxidation process.
(4) Composition and abundance of primary functional microbial communities in the MOD ecosystem were investigated by pmoA gene-based phylogeny of methanotrophs and nirK gene-based phylogeny of denitrifiers conbined with real-time PCR. There were amount of methanotrophs and denitrifiers in the enriched sludge, and the copy number of pmoA gene were almost3times more than that of nirK gene. Microbial community in the enrichment culture was dominated by Type I methanotrophs, which belonged to Methylococcaceae, Gammaproteobacteria, comprising37.5%of the total bacterial16S rRNA gene clone library. The Methylobacter spp. and Methylocaldum spp. were the dominant population. Aerobic methylotrophic denitrifiers of Methylophilaceae, Betaproteobacteria, might make great contribution in denitrification in our MOD ecosystems, comprising36.76%of the total bacterial16S rRNA gene clone library.
In conclusion, the microbiological mechanism of the MOD system in this study was that type I methanotrophs, which belonged to Methylobacter spp. and Methylocaldum spp., Methylococcaceae, Gammaproteobacteria, oxidized methane, employed the ribulose monophosphate (RuMP) pathway for assimilation and released organic intermediates (i.e. formaldehyde, citrate, and acetate) under mireo-aerobic condition. Aerobic methylotrophic denitrifiers of Methylophilaceae, Betaproteobacteria, utilizing organic intermediates released from the methanotrophs as electron donor, played a vital role in aerobic denitrification.
引文
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