重金属污染稻田土壤温室气体产生相关的微生物群落结构及活性变化
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摘要
稻田是农业发展的特色土地利用类型,在我国粮食安全和农田土壤碳库保持中占有重要地位；稻田固碳和温室气体减排在应对气候变化的农业可持续发展中具有重要意义。上世纪中后期以来,中国稻田土壤重金属污染日益严重,特别是在珠江、湘江和长江中下游地区。稻田土壤重金属污染除引发日益严峻的稻米食物安全风险外,同时可能影响土壤的生物化学过程,从而可能影响稻田碳氮循环及温室气体产生和排放。因此,探讨重金属污染稻田土壤微生物区系和活性变化,特别是与稻田土壤碳氮循环及温室气体产生相关的功能微生物类群的群落结构多样性、丰度及活性的变化将有助于认识重金属污染的固碳减排效应,为保持和提高稻田土壤碳汇提供科学依据。
为此,本研究选择江苏宜兴、江西德兴和大余以及广东大宝山等4个污染地区的稻田土壤,采集重金属污染和未明显污染的稻田土壤表土,进行土壤微生物区系和群落结构及其活性的多地、多方法比较研究。测定分析了土壤重金属含量及重金属污染程度、土壤基本性质、土壤微生物生物量碳氮等；用稀释平板计数法研究了可培养细菌与可培养真菌的数目；用磷脂脂肪酸分析法(PLFA)分析了土壤的活性微生物区系;用定量PCR (qPCR)和变性梯度凝胶电泳(DGGE)技术分析了细菌、真菌、产甲烷菌、甲烷氧化菌、氨氧化细菌(AOB)、氨氧化古菌(AOA)以及反硝化细菌的基因丰度和群落结构多样性,并挑选重要DGGE条带进行克隆测序及系统发育分析。为了探索微生物区系变化与土壤碳氮代谢过程变化的可能关系,通过实验室培养分析测定了土壤蔗糖酶、淀粉酶、β-葡萄糖苷酶及多酚氧化酶等酶活性,进一步采用化学法分析了土壤基础呼吸、底物诱导呼吸、产甲烷活性、甲烷氧化活性、硝化活性以及反硝化活性。试图从多方面探讨重金属污染稻田土壤中微生物类群的群落结构多样性、丰度以及活性的变化及其与温室气体产生的可能关系,主要研究结果如下：
一重金属污染下土壤微生物生物量、微生物群落结构、酶活性及呼吸活性的变化
1.微生物生物量碳氮在重金属污染稻田土壤中均较其参照有所降低,且微生物商显著降低。真菌的可培养数目、PLFA含量及基因拷贝数在重金属污染土壤中均有不同程度的降低；然而,细菌在各个重金属污染土壤中没有如此一致性的变化。此外,真菌与细菌的PLFA含量之比在所有污染土壤中均较其参照显著降低,其幅度从6%到50%。因而,与细菌相比,真菌可能对稻田土壤重金属污染更为敏感,其相对优势度会下降。并且,重金属污染下微生物商降低程度与真菌/细菌PLFA含量之比的降低程度显著相关。另外,基于基础呼吸的代谢商在污染下显著升高,其幅度从7%到70%。代谢商的升高程度与微生物商的降低程度显著相关；与真菌/细菌PLFA含量之比的降低程度在p=0.10水平上相关,说明可能由于土壤真菌相对优势度下降而引发微生物碳源利用效率降低,致使微生物商降低,造成重金属污染下代谢商增高。
2.脂肪酸18：4ω3c存在于所有重金属污染土壤中,却只在大余参照土壤中被检测到；而18：1ω5c的含量在宜兴污染土壤中较其参照降低,在其它污染土壤中不能被检测到；脂肪酸18：1ω9t(真菌代表性脂肪酸之一)的含量在所有污染土壤中均较其对照而降低。环境胁迫指标：G+菌/G-菌之比以及饱和脂肪酸单不饱和脂肪酸之比在污染土壤中较其参照土壤显著提高。PLFA组分的主成分分析,以及细菌和真菌DGGE图谱的主成分分析均表明,微生物群落结构在重金属污染土壤中有一定程度改变。
3.不同重金属污染土壤中蔗糖酶、淀粉酶、β-葡萄糖苷酶及多酚氧化酶的酶活性变化并不一致：与参照土壤相比,在宜兴和大宝山的污染土壤中四种酶的酶活性均没有显著改变；在大余污染土壤中蔗糖酶和淀粉酶的酶活性显著降低,而多酚氧化酶活性反而提高,β-葡萄糖苷酶活性未明显变化；在德兴污染土壤中β-葡萄糖苷酶和多酚氧化酶的酶活性显著降低,另两种酶的酶活性没有显著变化。
4.氨基葡萄糖、纤维二糖或对羟基苯甲酸三种底物分别诱导的呼吸速率达到最大之前的滞留时间,在重金属污染土壤中均延长,说明重金属污染下微生物代谢多样性降低。在纤维二糖矿化高峰时,重金属污染下总的、细菌的、真菌的PLFA含量以及真菌/细菌之比显著低于参照；微生物群落结构与参照之间的差异程度低于本底土壤,活性细菌群落结构仍有所改变,而真菌群落结构没有显著变化。
二重金属污染下与甲烷产生和氧化相关微生物群落结构、丰度及活性的变化
1.产甲烷菌-mcrA和甲烷氧化菌-pmoA基因DGGE图谱的主成分分析表明,产甲烷菌和甲烷氧化菌群落结构在重金属污染土壤中均较其参照在PC1或PC2上显著变化。
从系统发育分析来看,宜兴、德兴和大宝山污染土壤中分离的产甲烷菌分别属于产甲烷杆菌(Methanobacteriacea)、氢型产甲烷菌Methanocellales (Rice cluster)和甲烷螺菌科(Methanospirillaceae)等不同类群。分离自德兴污染及参照土壤的甲烷氧化菌菌株均属于Ⅰ型甲烷氧化菌,但其分布在两个不同分支上,说明二者亲缘关系较远。大余污染土壤的两株氧化菌分别属于Ⅰ型和Ⅱ型甲烷氧化菌,与其污染土壤的两个菌株相比,这四株菌的亲缘关系均较远。此结果在一定程度上说明德兴和大余重金属污染土壤的甲烷氧化菌在系统发育上均较其参照有所改变。
2.与参照土壤相比,产甲烷菌丰度只在重金属污染程度最高的大余土壤中被显著抑制,在其它样点没有显著变化；而其多样性在大余污染土壤中显著降低,在大宝山无变化,在另两样点显著提高。然而,除德兴样点外,甲烷氧化菌丰度在重金属污染土壤中较其参照显著降低,其幅度从16%到74%；而其多样性在宜兴和德兴污染土壤中显著降低,在大余无显著变化,在污染程度最轻的大宝山显著升高。
3.产甲烷活性只在大余污染土壤中较其参照显著降低,在其它样点没有显著改变。甲烷氧化活性较产甲烷活性可能对重金属污染更为敏感,除德兴样点外,其在污染土壤中均较其参照而显著下降,其幅度从37%到56%。
三重金属污染稻田土壤与N2O产生相关微生物群落结构、丰度及活性的变化
(一)氨氧化细菌(AOB)与古菌(AOA)群落结构、丰度及硝化活性
1. AOB-amoA和AOA-amoA基因DGGE图谱的主成分分析表明,AOB群落结构仅在宜兴和大宝山污染土壤中较其参照有所改变；而AOA群落结构在所有污染土壤中均较其参照在PC1或PC2上显著改变。
从系统发育分析来看,所分离AOB菌株分布在亚硝化螺菌属(Nitrosospira)的多个分支上,而分离自宜兴和大宝山参照土壤的AOB菌株,分别归属于类群3a.1和类群4,其在相应污染土壤中几乎不能被检测到,说明类群3a.1与类群4中某些AOB菌株可能对重金属污染较为敏感。分离自宜兴和大余污染土壤的两个AOA菌株归属于泉古菌门的soil/sediment类群,其它三株菌分类地位尚不明确；而来自于大余参照土壤的AOA菌株归于water column类群。
2.AOB丰度在德兴和大宝山重金属污染土壤中显著降低,在另两样点无显著变化；而其多样性在德兴污染土壤中没有显著变化,在大宝山显著降低,在另两样点却显著升高。AOA丰度及其多样性在宜兴污染土壤中较其参照未显著改变；在德兴污染土壤中均下降；大余污染土壤中其丰度升高但多样性降低；大宝山污染土壤中其丰度无显著变化,而多样性升高。
3.硝化活性在德兴和大宝山重金属污染稻田土壤中较其参照显著降低,其幅度达60%以上,在其它两样点无显著变化。
(二)反硝化细菌群落结构、丰度及反硝化活性
1.反硝化细菌-nirK及-nosZ基因DGGE图谱的主成分分析表明,其群落结构在重金属污染土壤中均较其参照在PC1或PC2上显著变化,仅大宝山污染土壤中nirK群落结构较其参照未明显改变。
从系统发育分析看,所分离nirK克隆不属于α-或β-变形菌；而绝大多数nosZ克隆归属于α-变形菌,但两者均与已知可培养菌株亲缘关系较远。总体分析所有污染土壤或参照土壤的nirK或nosZ克隆,其均分布在细菌的多个不同类群中；但单个研究样点内,分离自污染及参照土壤的nirK或nosZ克隆在系统发育上有一定程度的不同。
2.与参照土壤相比,nirK和nosZ的丰度在宜兴和大余污染土壤中均显著降低,在另外两样点均未显著改变；nirK的多样性在大余污染土壤中显著降低,在其它样点无显著变化；nosZ多样性在德兴和大宝山污染土壤中显著升高,在另外两样点无显著改变。
3.在重金属污染程度最轻的大宝山样点,反硝化活性没有显著变化。而在其它三个样点的污染土壤中,反硝化活性较其参照显著降低；且N20的产生速率也均有所下降。但是N20的还原速率只在德兴污染土壤中显著被抑制,说明在污染较为严重的稻田土壤中,反硝化过程中N20的产生活性比其还原活性受到的抑制程度可能更大。
综上所述,重金属污染稻田土壤中,真菌较细菌相对优势度降低,微生物商降低,而代谢商显著增高,重金属污染下的这些共性变化可能会影响对稻田土壤中与碳素周转相关的生物化学过程及CO2排放。相比产甲烷菌丰度及产甲烷活性,甲烷氧化菌丰度与甲烷氧化活性在重金属污染稻田土壤中所受抑制程度更大,因而可能通过抑制CH4的氧化而加剧了重金属污染稻田的CH4排放,此仍需更多的田间实验验证。而与N20产生相关的氨氧化细菌或古菌与硝化活性、反硝化细菌与反硝化活性在重金属污染下的变化因不同土壤或不同金属污染而有较大差异。
重金属污染稻田土壤中各种微生物活性之变化与其相应功能微生物群落结构多样性变化之间的格局较为复杂。然而,重金属污染下,代谢商增高程度与真菌/细菌PLFA含量之比降低程度在p=0.10水平上相关；产甲烷活性与产甲烷菌丰度、甲烷氧化活性与甲烷氧化菌丰度以及硝化活性与AOB丰度或同时显著降低,或同时无显著变化,说明土壤微生物多样性所维系的一定范围内,微生物活性高低与其丰度变化之间联系可能更为紧密。不过,本研究未得到微生物活性变化与其丰度变化之间的显著相关关系,这提示仍需从微生物本体之外的其它角度探讨重金属污染下温室气体排放发生变化的原因。
Rice paddy is a special land use type in argriculture, which plays an important role in maintaining food safty and soil carbon in China. Carbon sequentation and greenhouse gases (GHGs) mitigation in paddy soils is an important strategy in addressing climatic change. However, rice paddies in China have been increasingly subject to heavy metal pollution since1950s', expecially in the area of Pearl River delta, Xiang river basin and lower Yangtze region. Heavy metal pollution in paddy soils not only threats the food safty, but probably affects soil biochemical processes, which may further influence soil carbon and nitrogen cycling as well as GHGs production and emission. Thus, study in changes of microbial groups and activities in heavy metal polluted rice paddies, especially in variation of soil microbial community structure, abundance and activity related to GHGs production, could be helpful to understand the carbon sequestration and mitigation in heavy metal polluted rice paddies; and could provide the scientific basis for maintaining and enhancing carbon stock in paddy soils.
In the present study, topsoils were collected from heavy metal polluted rice paddies and their counterparts in four sites (Yixing [YX], Dexing [DX], Dayu [DY] and Dabaoshan [DBS]) across South China to conduct a cross-site study, to investigate soil microbial community structure and activity with several methods. Heavy metal contents were determined and the pollution degree was analyzed. Soil basic physicochemical properties and microbial biomass carbon and nitrogen were examined. Culturable colonies of bacteria and fungi were measured with plate counting method; active microbial biomass and community were detected by phospholipids fatty acids (PLFAs) analysis; while the abundance and community structure diversity of bacteria, fungi, methanogens, methanotrophs, ammonia oxidizing bacteria (AOB) and archaea (AOA) as well as denitrifying bacteria were detected with real time PCR (qPCR) and denaturing gradient gel electrophoresis (DGGE) respectively, and some important bands retrieved from DGGE gel were sequenced for phylogenetic analysis. Moreover, the parallel studies of four enzymes (Invertase, Amylase, β-Glucosidase and Polyphenol oxidase) relating to carbon turnover in soil, of soil basal respiration, substrate induced respiration, methanogenic activity, methane oxidation activity, nitrifying activity and denitrifying activity were also conducted. Compared to the corresponding background soil, changes under pollution in the microbial communities, abundances and activities, as well as the relationship among them were investigated. The main results were as follows:
1. Changes in soil microbial biomass, community structure, enzyme activity and soil respiration under heavy metal pollution
1) Compared with the corresponding background soils, soil microbial biomass carbon (SMBC) and nitrogen (SMBN) had a decreased trendy in all the polluted soils, and microbial quotient reduced significantly. Cultural population size, PLFA content and gene copies of fungi simultaneously showed a consistent decreace in all the polluted soils at different degrees. However, bacteria did not reveal so consistent change in the different polluted soils. Moreover, the ratio of fungal-to-bacterial PLFA contents decreased significantly in all the polluted soils, at a degree of6%to50%. Thus, fungi appeared to be more sensitive than bacteria in heavy metal polluted paddy soils, and fungal dominance decreased. And the decrease of microbial quotient under pollution was significantly connected to the decrease of fungal-to-bacterial ratio. Furthermore, there did occur a significantly increase in metabolic quotient (qCO2)(at a degree of7%to70%) under pollution across the sites. And the increase of qCO2was sharply related to the decrease of microbial quotient; and slightly related (p=0.10) to the decrease of fungal-to-bacterial PLFAs ratio. These observations supported a shift of microbial community with decreased fungal dominance and thus C utilization efficiency under pollution in rice paddies, which may caused the decrease of microbial quotient and increase in qCO2.
2) Fatty acid18:4w3c was detected in all polluted soils, while only in the background soils of DY; whereas, the18:1w5c was not detected in the polluted soils, except in that of YX where its content decreased. The concentration of fatty acid18:1w9t (one of fungal biomarkers) reduced in all the polluted soils. Moreover, the ratio of G+to G-bacteria and of saturated to monounsaturated fatty acids (indexes of environmental stress) increased significantly in all the polluted soils compared with their counterparts. Comparison of microbial community structure by principal component analysis (PCA) of PLFA composition and bacterial and fungal DGGE profiles revealed difference between the polluted soils and their counterparts.
3) The four studied enzymes (Invertase, Amylase, β-Glucosidase and Polyphenol oxidase) responded differently to heavy metal pollution across the studied sites. Compared with their counterparts, the activities of all the four enzymes did not change significantly in the polluted soils of YX and DBS. In the polluted soils of DY, the activities of invertase and amylase decreased significantly,β-Glucosidase activity did not change, while polyphenol oxidase activity increased. In the polluted soils of DX, β-Glucosidase and polyphenol oxidase activities reduced significantly, yet the activities of other two enzymes did not change clearly.
4) Lag time before the priming CO2flush induced by glucosamine, cellobiose or4-hydroxybenzoate in all the polluted soils was longer than that in their counterparts, indicating decreased catabolic versatilities in heavy metal polluted soils. Furthermore, when cellobiose was decomposed actively, total, bacterial and fungal PLFA contents as well as fungal-to-bacterial ratio decreased significantly under pollution; difference of microbial community between polluted and background soils was smaller than that in soils without substrate amended, and the active community of bacteria shifted, yet that of fungi did not change under pollution.
2. Changes in soil microbial community structure, abundance and activity with special reference to CH4production and oxidation under heavy metal pollution
1) Comparison of the community structures of both methanogens and methanotrophs by PCA of DGGE profiles revealed difference along PC1or PC2between the polluted soils and their counterparts.
Phylogenetic analysis showed that the retrieved species of methanogens from the polluted soils of YX, DX and DBS affiliated with Methanobacteriacea, Methanocellales (Rice cluster) and Methanospirillaceae, respectively. The methanotrophs'clones from the polluted and background soils in DX affiliated with type I methanotrophs, while they grouped into two different clusters. Two clones from DY polluted soils, belonging to type I and typeⅡ methanotrophs respectively, did not grouped into the same cluster with that from their counterparts. These indicated that, to an extent, the methanothrophs in the polluted soils of DX or DY differed in phylogenesis from that in their counterparts.
2) In the polluted soils, the abundances of methanogens decreased significantly in DY, yet did not change clearly in other sites; while its diversities reduced in DY, did not change in DBS, increased significantly in YX and DX. However, the abundances of methanotrophs reduced significantly in the polluted soils, at a degree of16%to74%, except in DX, while its diversities decreased clearly in the polluted soils of YX and DX, did not change in that of DY, but increased significantly in that of DBS.
3) The methanogenic activity decreased significantly in the polluted soils of DY, yet did not change clearly in those of other sites; while the methane oxidation activity appeared to be more sensitive to metal pollution, the activity decreased significantly in the polluted soils, at a degree of37%to56%, except in DX.
3. Changes in soil microbial community structure, abundance and activity with special reference to N2O production under heavy metal pollution
(1) Ammonia oxidizers'community structure and abundance as well as nitrifying activity
1) Comparison of the community structures of AOB and AOA by PC A of DGGE profiles revealed that the difference of AOB community between the polluted and background soils was only found in YX and DBS, while the AOA community differed along PC1or PC2in all the polluted soils from their counterparts.
Phylogenetic analysis showed that all the retrieved AOB sequences in this study fell into different clusters in the genus Nitrosospira. Clones retrived from the background soils in YX and DBS respectively grouped into Cluster3a.1and Cluster4, which almost can not be detected in the polluted soils. These indicated some species in Cluster3a.1and Cluster4were more sensitive to heavy metal pollution. Two AOA sequences from the polluted soils in YX and DY distributed in soil/sediment cluster of phylum Crenarchaeote, while other three clones fall outside of all of the known three clusters; whereas, clones from the background soils in DY affiliated with water column cluster.
2) AOB abundances decreased significantly in the heavy metal polluted soils of DX and DBS, did not change clearly in other two sites; while it diversities did not change in DX polluted soils, decreased clearly in DBS, increased in other two sites. While AOA abundances and diversities did not change significantly in the polluted soils of YX, decreased in that of DX, but changed inconsistent in that of DY or DBS.
3) Nitrifying activity was inhibited significantly in the polluted soils of DX and DBS, at a degree more than60%, but did not change clearly in other two sites.
(2) Denitrifers'community structure and abundance as well as denitrifying activity
1) Comparison of the community structures of nirK-and nosZ-denitrifiers by PCA of DGGE profiles revealed difference along PC1or PC2between the polluted soils and their counterparts, except the nirK community in DBS.
All the retrived nirK clones did not belong to either α-or β-proteobacteria, while most of the nosZ species affiliated with a-proteobacteria. All the nirK and nosZ clones were not closely related to known cultural species in phylogenesis, and were widespread among different bacterial genera. While in a single site, the nirK-or nosZ-denitrifers from the polluted and background soils were different in phylogenesis to an extent.
2) Abundances of nirK and nosZ decreased significantly in the metal polluted soils in YX and DY, did not change clearly in other sites. Diversities of nirK reduced significantly in DY polluted soils, did not change in other soils; while that of nosZ increased clearly in the polluted soils in DX and DBS, yet not change significantly in other sites.
3) Denitrifying activity reduced significantly in polluted soils in YX, DX and DY, and N2O production rate also reduced more or less under pollution in the three sites, yet N2O reduction rate decreased significantly in DX site only. These suggested that comparing with N2O reduction activity, N2O production activity may be more inhibited in the relatively seriously polluted paddy soils.
In a word, in the four heavy metal polluted rice paddies, there did occur a decline in fungal dominance, in microbial quotient and an increase in metabolic quotient, which were the common change and may exert an impact on soil biogeochemical process related to C metabolism and CO2evolution in polluted rice paddies. Compared with methanogens and methanogenic activity, methanotrophs and methane oxidation activity seemed to be more sensitive to heavy metal pollution in paddy soils, which probably enhance CH4emission from paddy soils and deserve more field studies to examine. However, the changes of ammonia oxidizers and nitrifying activity, as well as denitrifers and denitrifying activity varied in different soils or due to different heavy metal elements or contents.
The changes in the several microbial activities detemined in this study had ambiguous relationships with the changes in community structures or diversities of the related functional microorganisms. However, under heavy metal pollution, increase in qCO2was related to decrease in fungal-to-bacterial PLFAs ratio (p=0.10); methanogenic activity and methanogenes'abundance, methane oxidation activity and methanotrophs'abundance, as well as nitrifying activity and AOB abundance reduced significantly and consistently or unchanged simultaneously. These indicated that, when soil microbial diversities maintained stability in a certain extent, microbial activities appeared to be more related to their abundances. However, no significant relationship between the change in microbial activity and in its abundance were observed in this study, which indicated that other aspects except for microorganisms probably should be concerned to explore the changes in GHGs emission under heavy metal pollution.
为此,本研究选择江苏宜兴、江西德兴和大余以及广东大宝山等4个污染地区的稻田土壤,采集重金属污染和未明显污染的稻田土壤表土,进行土壤微生物区系和群落结构及其活性的多地、多方法比较研究。测定分析了土壤重金属含量及重金属污染程度、土壤基本性质、土壤微生物生物量碳氮等；用稀释平板计数法研究了可培养细菌与可培养真菌的数目；用磷脂脂肪酸分析法(PLFA)分析了土壤的活性微生物区系;用定量PCR (qPCR)和变性梯度凝胶电泳(DGGE)技术分析了细菌、真菌、产甲烷菌、甲烷氧化菌、氨氧化细菌(AOB)、氨氧化古菌(AOA)以及反硝化细菌的基因丰度和群落结构多样性,并挑选重要DGGE条带进行克隆测序及系统发育分析。为了探索微生物区系变化与土壤碳氮代谢过程变化的可能关系,通过实验室培养分析测定了土壤蔗糖酶、淀粉酶、β-葡萄糖苷酶及多酚氧化酶等酶活性,进一步采用化学法分析了土壤基础呼吸、底物诱导呼吸、产甲烷活性、甲烷氧化活性、硝化活性以及反硝化活性。试图从多方面探讨重金属污染稻田土壤中微生物类群的群落结构多样性、丰度以及活性的变化及其与温室气体产生的可能关系,主要研究结果如下：
一重金属污染下土壤微生物生物量、微生物群落结构、酶活性及呼吸活性的变化
1.微生物生物量碳氮在重金属污染稻田土壤中均较其参照有所降低,且微生物商显著降低。真菌的可培养数目、PLFA含量及基因拷贝数在重金属污染土壤中均有不同程度的降低；然而,细菌在各个重金属污染土壤中没有如此一致性的变化。此外,真菌与细菌的PLFA含量之比在所有污染土壤中均较其参照显著降低,其幅度从6%到50%。因而,与细菌相比,真菌可能对稻田土壤重金属污染更为敏感,其相对优势度会下降。并且,重金属污染下微生物商降低程度与真菌/细菌PLFA含量之比的降低程度显著相关。另外,基于基础呼吸的代谢商在污染下显著升高,其幅度从7%到70%。代谢商的升高程度与微生物商的降低程度显著相关；与真菌/细菌PLFA含量之比的降低程度在p=0.10水平上相关,说明可能由于土壤真菌相对优势度下降而引发微生物碳源利用效率降低,致使微生物商降低,造成重金属污染下代谢商增高。
2.脂肪酸18：4ω3c存在于所有重金属污染土壤中,却只在大余参照土壤中被检测到；而18：1ω5c的含量在宜兴污染土壤中较其参照降低,在其它污染土壤中不能被检测到；脂肪酸18：1ω9t(真菌代表性脂肪酸之一)的含量在所有污染土壤中均较其对照而降低。环境胁迫指标：G+菌/G-菌之比以及饱和脂肪酸单不饱和脂肪酸之比在污染土壤中较其参照土壤显著提高。PLFA组分的主成分分析,以及细菌和真菌DGGE图谱的主成分分析均表明,微生物群落结构在重金属污染土壤中有一定程度改变。
3.不同重金属污染土壤中蔗糖酶、淀粉酶、β-葡萄糖苷酶及多酚氧化酶的酶活性变化并不一致：与参照土壤相比,在宜兴和大宝山的污染土壤中四种酶的酶活性均没有显著改变；在大余污染土壤中蔗糖酶和淀粉酶的酶活性显著降低,而多酚氧化酶活性反而提高,β-葡萄糖苷酶活性未明显变化；在德兴污染土壤中β-葡萄糖苷酶和多酚氧化酶的酶活性显著降低,另两种酶的酶活性没有显著变化。
4.氨基葡萄糖、纤维二糖或对羟基苯甲酸三种底物分别诱导的呼吸速率达到最大之前的滞留时间,在重金属污染土壤中均延长,说明重金属污染下微生物代谢多样性降低。在纤维二糖矿化高峰时,重金属污染下总的、细菌的、真菌的PLFA含量以及真菌/细菌之比显著低于参照；微生物群落结构与参照之间的差异程度低于本底土壤,活性细菌群落结构仍有所改变,而真菌群落结构没有显著变化。
二重金属污染下与甲烷产生和氧化相关微生物群落结构、丰度及活性的变化
1.产甲烷菌-mcrA和甲烷氧化菌-pmoA基因DGGE图谱的主成分分析表明,产甲烷菌和甲烷氧化菌群落结构在重金属污染土壤中均较其参照在PC1或PC2上显著变化。
从系统发育分析来看,宜兴、德兴和大宝山污染土壤中分离的产甲烷菌分别属于产甲烷杆菌(Methanobacteriacea)、氢型产甲烷菌Methanocellales (Rice cluster)和甲烷螺菌科(Methanospirillaceae)等不同类群。分离自德兴污染及参照土壤的甲烷氧化菌菌株均属于Ⅰ型甲烷氧化菌,但其分布在两个不同分支上,说明二者亲缘关系较远。大余污染土壤的两株氧化菌分别属于Ⅰ型和Ⅱ型甲烷氧化菌,与其污染土壤的两个菌株相比,这四株菌的亲缘关系均较远。此结果在一定程度上说明德兴和大余重金属污染土壤的甲烷氧化菌在系统发育上均较其参照有所改变。
2.与参照土壤相比,产甲烷菌丰度只在重金属污染程度最高的大余土壤中被显著抑制,在其它样点没有显著变化；而其多样性在大余污染土壤中显著降低,在大宝山无变化,在另两样点显著提高。然而,除德兴样点外,甲烷氧化菌丰度在重金属污染土壤中较其参照显著降低,其幅度从16%到74%；而其多样性在宜兴和德兴污染土壤中显著降低,在大余无显著变化,在污染程度最轻的大宝山显著升高。
3.产甲烷活性只在大余污染土壤中较其参照显著降低,在其它样点没有显著改变。甲烷氧化活性较产甲烷活性可能对重金属污染更为敏感,除德兴样点外,其在污染土壤中均较其参照而显著下降,其幅度从37%到56%。
三重金属污染稻田土壤与N2O产生相关微生物群落结构、丰度及活性的变化
(一)氨氧化细菌(AOB)与古菌(AOA)群落结构、丰度及硝化活性
1. AOB-amoA和AOA-amoA基因DGGE图谱的主成分分析表明,AOB群落结构仅在宜兴和大宝山污染土壤中较其参照有所改变；而AOA群落结构在所有污染土壤中均较其参照在PC1或PC2上显著改变。
从系统发育分析来看,所分离AOB菌株分布在亚硝化螺菌属(Nitrosospira)的多个分支上,而分离自宜兴和大宝山参照土壤的AOB菌株,分别归属于类群3a.1和类群4,其在相应污染土壤中几乎不能被检测到,说明类群3a.1与类群4中某些AOB菌株可能对重金属污染较为敏感。分离自宜兴和大余污染土壤的两个AOA菌株归属于泉古菌门的soil/sediment类群,其它三株菌分类地位尚不明确；而来自于大余参照土壤的AOA菌株归于water column类群。
2.AOB丰度在德兴和大宝山重金属污染土壤中显著降低,在另两样点无显著变化；而其多样性在德兴污染土壤中没有显著变化,在大宝山显著降低,在另两样点却显著升高。AOA丰度及其多样性在宜兴污染土壤中较其参照未显著改变；在德兴污染土壤中均下降；大余污染土壤中其丰度升高但多样性降低；大宝山污染土壤中其丰度无显著变化,而多样性升高。
3.硝化活性在德兴和大宝山重金属污染稻田土壤中较其参照显著降低,其幅度达60%以上,在其它两样点无显著变化。
(二)反硝化细菌群落结构、丰度及反硝化活性
1.反硝化细菌-nirK及-nosZ基因DGGE图谱的主成分分析表明,其群落结构在重金属污染土壤中均较其参照在PC1或PC2上显著变化,仅大宝山污染土壤中nirK群落结构较其参照未明显改变。
从系统发育分析看,所分离nirK克隆不属于α-或β-变形菌；而绝大多数nosZ克隆归属于α-变形菌,但两者均与已知可培养菌株亲缘关系较远。总体分析所有污染土壤或参照土壤的nirK或nosZ克隆,其均分布在细菌的多个不同类群中；但单个研究样点内,分离自污染及参照土壤的nirK或nosZ克隆在系统发育上有一定程度的不同。
2.与参照土壤相比,nirK和nosZ的丰度在宜兴和大余污染土壤中均显著降低,在另外两样点均未显著改变；nirK的多样性在大余污染土壤中显著降低,在其它样点无显著变化；nosZ多样性在德兴和大宝山污染土壤中显著升高,在另外两样点无显著改变。
3.在重金属污染程度最轻的大宝山样点,反硝化活性没有显著变化。而在其它三个样点的污染土壤中,反硝化活性较其参照显著降低；且N20的产生速率也均有所下降。但是N20的还原速率只在德兴污染土壤中显著被抑制,说明在污染较为严重的稻田土壤中,反硝化过程中N20的产生活性比其还原活性受到的抑制程度可能更大。
综上所述,重金属污染稻田土壤中,真菌较细菌相对优势度降低,微生物商降低,而代谢商显著增高,重金属污染下的这些共性变化可能会影响对稻田土壤中与碳素周转相关的生物化学过程及CO2排放。相比产甲烷菌丰度及产甲烷活性,甲烷氧化菌丰度与甲烷氧化活性在重金属污染稻田土壤中所受抑制程度更大,因而可能通过抑制CH4的氧化而加剧了重金属污染稻田的CH4排放,此仍需更多的田间实验验证。而与N20产生相关的氨氧化细菌或古菌与硝化活性、反硝化细菌与反硝化活性在重金属污染下的变化因不同土壤或不同金属污染而有较大差异。
重金属污染稻田土壤中各种微生物活性之变化与其相应功能微生物群落结构多样性变化之间的格局较为复杂。然而,重金属污染下,代谢商增高程度与真菌/细菌PLFA含量之比降低程度在p=0.10水平上相关；产甲烷活性与产甲烷菌丰度、甲烷氧化活性与甲烷氧化菌丰度以及硝化活性与AOB丰度或同时显著降低,或同时无显著变化,说明土壤微生物多样性所维系的一定范围内,微生物活性高低与其丰度变化之间联系可能更为紧密。不过,本研究未得到微生物活性变化与其丰度变化之间的显著相关关系,这提示仍需从微生物本体之外的其它角度探讨重金属污染下温室气体排放发生变化的原因。
Rice paddy is a special land use type in argriculture, which plays an important role in maintaining food safty and soil carbon in China. Carbon sequentation and greenhouse gases (GHGs) mitigation in paddy soils is an important strategy in addressing climatic change. However, rice paddies in China have been increasingly subject to heavy metal pollution since1950s', expecially in the area of Pearl River delta, Xiang river basin and lower Yangtze region. Heavy metal pollution in paddy soils not only threats the food safty, but probably affects soil biochemical processes, which may further influence soil carbon and nitrogen cycling as well as GHGs production and emission. Thus, study in changes of microbial groups and activities in heavy metal polluted rice paddies, especially in variation of soil microbial community structure, abundance and activity related to GHGs production, could be helpful to understand the carbon sequestration and mitigation in heavy metal polluted rice paddies; and could provide the scientific basis for maintaining and enhancing carbon stock in paddy soils.
In the present study, topsoils were collected from heavy metal polluted rice paddies and their counterparts in four sites (Yixing [YX], Dexing [DX], Dayu [DY] and Dabaoshan [DBS]) across South China to conduct a cross-site study, to investigate soil microbial community structure and activity with several methods. Heavy metal contents were determined and the pollution degree was analyzed. Soil basic physicochemical properties and microbial biomass carbon and nitrogen were examined. Culturable colonies of bacteria and fungi were measured with plate counting method; active microbial biomass and community were detected by phospholipids fatty acids (PLFAs) analysis; while the abundance and community structure diversity of bacteria, fungi, methanogens, methanotrophs, ammonia oxidizing bacteria (AOB) and archaea (AOA) as well as denitrifying bacteria were detected with real time PCR (qPCR) and denaturing gradient gel electrophoresis (DGGE) respectively, and some important bands retrieved from DGGE gel were sequenced for phylogenetic analysis. Moreover, the parallel studies of four enzymes (Invertase, Amylase, β-Glucosidase and Polyphenol oxidase) relating to carbon turnover in soil, of soil basal respiration, substrate induced respiration, methanogenic activity, methane oxidation activity, nitrifying activity and denitrifying activity were also conducted. Compared to the corresponding background soil, changes under pollution in the microbial communities, abundances and activities, as well as the relationship among them were investigated. The main results were as follows:
1. Changes in soil microbial biomass, community structure, enzyme activity and soil respiration under heavy metal pollution
1) Compared with the corresponding background soils, soil microbial biomass carbon (SMBC) and nitrogen (SMBN) had a decreased trendy in all the polluted soils, and microbial quotient reduced significantly. Cultural population size, PLFA content and gene copies of fungi simultaneously showed a consistent decreace in all the polluted soils at different degrees. However, bacteria did not reveal so consistent change in the different polluted soils. Moreover, the ratio of fungal-to-bacterial PLFA contents decreased significantly in all the polluted soils, at a degree of6%to50%. Thus, fungi appeared to be more sensitive than bacteria in heavy metal polluted paddy soils, and fungal dominance decreased. And the decrease of microbial quotient under pollution was significantly connected to the decrease of fungal-to-bacterial ratio. Furthermore, there did occur a significantly increase in metabolic quotient (qCO2)(at a degree of7%to70%) under pollution across the sites. And the increase of qCO2was sharply related to the decrease of microbial quotient; and slightly related (p=0.10) to the decrease of fungal-to-bacterial PLFAs ratio. These observations supported a shift of microbial community with decreased fungal dominance and thus C utilization efficiency under pollution in rice paddies, which may caused the decrease of microbial quotient and increase in qCO2.
2) Fatty acid18:4w3c was detected in all polluted soils, while only in the background soils of DY; whereas, the18:1w5c was not detected in the polluted soils, except in that of YX where its content decreased. The concentration of fatty acid18:1w9t (one of fungal biomarkers) reduced in all the polluted soils. Moreover, the ratio of G+to G-bacteria and of saturated to monounsaturated fatty acids (indexes of environmental stress) increased significantly in all the polluted soils compared with their counterparts. Comparison of microbial community structure by principal component analysis (PCA) of PLFA composition and bacterial and fungal DGGE profiles revealed difference between the polluted soils and their counterparts.
3) The four studied enzymes (Invertase, Amylase, β-Glucosidase and Polyphenol oxidase) responded differently to heavy metal pollution across the studied sites. Compared with their counterparts, the activities of all the four enzymes did not change significantly in the polluted soils of YX and DBS. In the polluted soils of DY, the activities of invertase and amylase decreased significantly,β-Glucosidase activity did not change, while polyphenol oxidase activity increased. In the polluted soils of DX, β-Glucosidase and polyphenol oxidase activities reduced significantly, yet the activities of other two enzymes did not change clearly.
4) Lag time before the priming CO2flush induced by glucosamine, cellobiose or4-hydroxybenzoate in all the polluted soils was longer than that in their counterparts, indicating decreased catabolic versatilities in heavy metal polluted soils. Furthermore, when cellobiose was decomposed actively, total, bacterial and fungal PLFA contents as well as fungal-to-bacterial ratio decreased significantly under pollution; difference of microbial community between polluted and background soils was smaller than that in soils without substrate amended, and the active community of bacteria shifted, yet that of fungi did not change under pollution.
2. Changes in soil microbial community structure, abundance and activity with special reference to CH4production and oxidation under heavy metal pollution
1) Comparison of the community structures of both methanogens and methanotrophs by PCA of DGGE profiles revealed difference along PC1or PC2between the polluted soils and their counterparts.
Phylogenetic analysis showed that the retrieved species of methanogens from the polluted soils of YX, DX and DBS affiliated with Methanobacteriacea, Methanocellales (Rice cluster) and Methanospirillaceae, respectively. The methanotrophs'clones from the polluted and background soils in DX affiliated with type I methanotrophs, while they grouped into two different clusters. Two clones from DY polluted soils, belonging to type I and typeⅡ methanotrophs respectively, did not grouped into the same cluster with that from their counterparts. These indicated that, to an extent, the methanothrophs in the polluted soils of DX or DY differed in phylogenesis from that in their counterparts.
2) In the polluted soils, the abundances of methanogens decreased significantly in DY, yet did not change clearly in other sites; while its diversities reduced in DY, did not change in DBS, increased significantly in YX and DX. However, the abundances of methanotrophs reduced significantly in the polluted soils, at a degree of16%to74%, except in DX, while its diversities decreased clearly in the polluted soils of YX and DX, did not change in that of DY, but increased significantly in that of DBS.
3) The methanogenic activity decreased significantly in the polluted soils of DY, yet did not change clearly in those of other sites; while the methane oxidation activity appeared to be more sensitive to metal pollution, the activity decreased significantly in the polluted soils, at a degree of37%to56%, except in DX.
3. Changes in soil microbial community structure, abundance and activity with special reference to N2O production under heavy metal pollution
(1) Ammonia oxidizers'community structure and abundance as well as nitrifying activity
1) Comparison of the community structures of AOB and AOA by PC A of DGGE profiles revealed that the difference of AOB community between the polluted and background soils was only found in YX and DBS, while the AOA community differed along PC1or PC2in all the polluted soils from their counterparts.
Phylogenetic analysis showed that all the retrieved AOB sequences in this study fell into different clusters in the genus Nitrosospira. Clones retrived from the background soils in YX and DBS respectively grouped into Cluster3a.1and Cluster4, which almost can not be detected in the polluted soils. These indicated some species in Cluster3a.1and Cluster4were more sensitive to heavy metal pollution. Two AOA sequences from the polluted soils in YX and DY distributed in soil/sediment cluster of phylum Crenarchaeote, while other three clones fall outside of all of the known three clusters; whereas, clones from the background soils in DY affiliated with water column cluster.
2) AOB abundances decreased significantly in the heavy metal polluted soils of DX and DBS, did not change clearly in other two sites; while it diversities did not change in DX polluted soils, decreased clearly in DBS, increased in other two sites. While AOA abundances and diversities did not change significantly in the polluted soils of YX, decreased in that of DX, but changed inconsistent in that of DY or DBS.
3) Nitrifying activity was inhibited significantly in the polluted soils of DX and DBS, at a degree more than60%, but did not change clearly in other two sites.
(2) Denitrifers'community structure and abundance as well as denitrifying activity
1) Comparison of the community structures of nirK-and nosZ-denitrifiers by PCA of DGGE profiles revealed difference along PC1or PC2between the polluted soils and their counterparts, except the nirK community in DBS.
All the retrived nirK clones did not belong to either α-or β-proteobacteria, while most of the nosZ species affiliated with a-proteobacteria. All the nirK and nosZ clones were not closely related to known cultural species in phylogenesis, and were widespread among different bacterial genera. While in a single site, the nirK-or nosZ-denitrifers from the polluted and background soils were different in phylogenesis to an extent.
2) Abundances of nirK and nosZ decreased significantly in the metal polluted soils in YX and DY, did not change clearly in other sites. Diversities of nirK reduced significantly in DY polluted soils, did not change in other soils; while that of nosZ increased clearly in the polluted soils in DX and DBS, yet not change significantly in other sites.
3) Denitrifying activity reduced significantly in polluted soils in YX, DX and DY, and N2O production rate also reduced more or less under pollution in the three sites, yet N2O reduction rate decreased significantly in DX site only. These suggested that comparing with N2O reduction activity, N2O production activity may be more inhibited in the relatively seriously polluted paddy soils.
In a word, in the four heavy metal polluted rice paddies, there did occur a decline in fungal dominance, in microbial quotient and an increase in metabolic quotient, which were the common change and may exert an impact on soil biogeochemical process related to C metabolism and CO2evolution in polluted rice paddies. Compared with methanogens and methanogenic activity, methanotrophs and methane oxidation activity seemed to be more sensitive to heavy metal pollution in paddy soils, which probably enhance CH4emission from paddy soils and deserve more field studies to examine. However, the changes of ammonia oxidizers and nitrifying activity, as well as denitrifers and denitrifying activity varied in different soils or due to different heavy metal elements or contents.
The changes in the several microbial activities detemined in this study had ambiguous relationships with the changes in community structures or diversities of the related functional microorganisms. However, under heavy metal pollution, increase in qCO2was related to decrease in fungal-to-bacterial PLFAs ratio (p=0.10); methanogenic activity and methanogenes'abundance, methane oxidation activity and methanotrophs'abundance, as well as nitrifying activity and AOB abundance reduced significantly and consistently or unchanged simultaneously. These indicated that, when soil microbial diversities maintained stability in a certain extent, microbial activities appeared to be more related to their abundances. However, no significant relationship between the change in microbial activity and in its abundance were observed in this study, which indicated that other aspects except for microorganisms probably should be concerned to explore the changes in GHGs emission under heavy metal pollution.
引文
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