嗜鱼外瓶霉（Exophiala pisciphila ACCC32496）镉耐性机制研究
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摘要
铅锌矿产资源的开采导致铅锌矿区镉(Cd)严重污染,是云南省重大环境问题之一。在Cd严重污染的铅锌矿区自然生长的野生植物根部普遍定殖着深色有隔内生真菌(Dark septate endophytes, DSE),提示着DSE在铅锌矿区野生植物适应重金属胁迫中可能发挥着重要作用。研究分离自铅锌矿区的DSE对Cd的耐性及其机理,有助于阐明DSE在重金属严重污染的铅锌矿区这一特殊生态系统中的功能地位,解释铅锌矿区DSE与野生植物重金属耐性的关系；对于探索利用植物根部定殖的DSE,提高植物耐受重金属能力,重建重金属污染环境植被具有重要的理论和实践意义。
本研究以分离自重金属严重污染的云南省会泽铅锌矿区自然生长的密序野古草(Arundinella bengalensis (Spreng.) Druce)根内的1株DSE真菌—嗜鱼外瓶霉(Exophiala pisciphila ACCC32496)为研究对象,浓度为0-400mg/L的Cd胁迫处理下,研究菌丝Cd富集量、Cd化学形态与亚细胞分布、细胞壁Cd吸附能力与特征、Cd吸附基团、菌丝黑色素性质与特征、低分子量有机酸分泌、矿质营养、抗氧化系统等方面的内容,分析该菌株耐受Cd的胞外与胞内机制,得到以下主要结果：
(1) E. pisciphila ACCC32496有很强的Cd耐性和富集能力。固体和液体培养情况下,采用直线内插法计算Cd对E. pisciphila ACCC32496的半数生长抑制浓度值(EC50),分别为332.2和111.2mg/L。Cd浓度为400mg/L时,E. pisciphila ACCC32496菌丝的Cd含量达到51.43mg/g干菌丝。
(2)采用扫描电镜—能谱、透射电镜和透射电镜—能谱分析,结合差速离心法分离E. pisciphila ACCC32496菌丝亚细胞组分(细胞壁、细胞器和可溶性组分),发现Cd主要分布在菌丝细胞壁上。采用化学试剂逐步提取法,研究表明菌丝Cd的化学形态主要为醋酸提取态(FHAc)和氯化钠提取态(FNaCl)。
(3)0.1M HCl和Na2EDTA从E. pisciphila ACCC32496菌丝解吸出来的Cd占菌丝Cd含量的63.0%-83.5%,0.1M CaCl2能够解吸8.3%-43.8%,0.1M NaOH能够解吸0.9%-5.6%。
(4)在初始Cd浓度为25～400mg/L, pH值5.0,转速120rpm和30℃条件下, E. pisciphila ACCC32496菌丝吸附Cd的过程符合Langmuir吸附等温模型,吸附Cd的动力学实验数据符合准二级速率方程。傅里叶红外光谱(FTIR)分析表明,吸附Cd的化学基团涉及氨基、酰氨基、羧基、羟基和磷酰基等。
(5) E. pisciphila ACCC32496菌丝黑色素属于典型的DHN型黑色素。三环唑能特异性抑制E. pisciphila ACCC32496菌丝黑色素合成,浓度不高于10μg/ml的三环唑对E. pisciphila ACCC32496菌丝生长与孢子产生量没有明显影响。Cd浓度在50-350mg/L, E. pisciphila ACCC32496菌丝黑色素含量有显著增加。50～200mg/L Cd胁迫下,采用三环唑抑制E. pisciphila ACCC32496菌丝黑色素合成,该菌丝生物量显著小于正常菌丝,Cd富集量大于正常菌丝,表明黑色素在该菌株Cd耐性中有作用。
(6)Cd胁迫导致E. pisciphila ACCC32496菌丝N、K和Fe含量显著下降,P、Mg和Ca含量显著增加,S含量在Cd浓度为100mg/L时显著增加。Cd胁迫促进E. pisciphila ACCC32496菌丝产酸,培养液pH值下降。采用高效液相色谱法(HPLC)分析培养液中的低分子量有机酸,表明E. pisciphila ACCC32496菌丝主要产生草酸,培养液中菌丝草酸分泌量随Cd处理浓度增加而显著增加。
(7)Cd胁迫导致E. pisciphila ACCC32496菌丝超氧阴离子生成速率、MDA和H2O2含量显著增加。SOD酶与CAT酶活性、GSH与-SH化合物含量以及T-AOC在一定Cd浓度范围内,随着Cd浓度增加而增强。
以上结果表明,分离自重金属污染严重的铅锌矿区的DSE菌株E. pisciphila ACCC32496对Cd有很强的耐性与富集能力。E. pisciphila ACCC32496对Cd的耐性机制：①胞外机制包括：增加低分子量有机酸的分泌,尤其是草酸的分泌；通过菌丝细胞壁对的Cd吸附作用,以及增加细胞壁上的特殊组分—黑色素的合成。②胞内机制包括：通过增强菌丝细胞内SOD, CAT等抗氧化酶的活性,增加GSH等巯基化合物的合成,以及提高菌丝中P, S、Mg和Ca等矿质元素的含量,提高E. pisciphila ACCC32496对Cd的耐受能力。
本文通过铅锌矿区典型DSE菌株对Cd的富集特征和耐性机制的初步研究,有助于理解特殊生境—重金属严重污染的铅锌矿区中特殊生物类群—DSE的生态学功能,并为进一步研究DSE在重金属污染环境的植被重建与修复可能应用打下了一定的基础。
Cadmium (Cd) pollution caused by mining of Lead (Pb) and Zinc (Zn) in Pb-Zn mine area is one of the most serious environmental problems in Yunnan. The roots of plants naturally growing in Pb-Zn mine areas are commonly colonized by dark septate endophytes (DSE) suggestes that DSE may play an important role in adaptation to heavy metal stress of these plants. Based on these facts, to relise the Cd tolerance and mechanisms of DSE from Pb-Zn mine area may help us to elucidate biological functions of DSE in the special ecosystem and to explain the relationship between DSE and heavy metal tolerance of their host plants in Pb-Zn mine area. Meanwhile, this research work is also theoretically and practically significance for making use of DSE-plants association to improve the heavy metal tolerance of plants to restore vegetation in Cd polluted environment.
Exophiala pisciphila ACCC32496, a fungus of DSE isolated from the roots of Arundinella bengalensis (Spreng.) Druce which is wild plant grown on Pb-Zn mine area with serious heavy metals pollution in Huze County, Yunnan Province was selected in this thesis. The extracellular and intracellular tolerance mechanisms to Cd of Exophiala pisciphila ACCC32496are analyzed by studies on Cd accumulation of mycelium, Cd chemical forms and subcellular distribution, Cd adsorption capacity and characteristics of cell wall, chemical groups for Cd adsorption, physical and chemical characteristics of melanin from mycelium, secretion of low molecular weight organic acid, mineral nutrition, antioxidant system and so on which are responses to Cd stress with concentration of0～400mg/L.
The main results are as follows:
(1) A relative high Cd tolerance and accumulation ability of E. pisciphila ACCC32496was founded. The50%effective inhibiting concentration (EC50) of Cd to E. pisciphila ACCC32496was calculated by linear interpolation and the result was332.2and111.2mg/L by solid and liquid culture respectively.89.02mg Cd per g dry mycelium was accumulated by E. pisciphila ACCC32496when the concentration of Cd was400mg/L in liquid medium.
(2) The mycelium of E. pisciphila ACCC32496were analyzed by SEM-EDS, TEM and TEM-EDS, and the subcellular fractions, ie cell wall, organelles and soluble fraction, were separated by differential centrifugation. The results showed that Cd was mainly distributed in the cell wall of E. pisciphila ACCC32496. Cd associated with different chemical forms was successively extracted by designated solutions in the following order,80%ethanol, deionized water,1M NaCl,2%acetic acid and0.6M HCl. Acetic acid extractable (FHAc) and sodium chloride extractable (FNaCl) was the main chemical form of Cd.
(2) About63.0%～83.5%of the total Cd in the mycelium of E. pisciphila ACCC32496could be desorbed by0.1M HCl or0.1M Na2EDTA,8.3%-43.8%by0.1M CaCl2, and0.9%-5.6%by0.1M NaOH.
(3) Cd adsorption process of E. pisciphila ACCC32496mycelium can be well described by Langmuir adsorption isotherm model. Kinetics data for the adsorption of Cd from aqueous solutions by E. pisciphila ACCC32496mycelium were in good agreement with the pseudo-second rate equation within an initial concentration range of25-400mg/L, pH value of5.0, an agitation speed range of120rpm and an experimental temperature of30℃. The chemical groups of E. pisciphila ACCC32496mycelium involving in adsorption of Cd involved amino, amido, carboxyl, hydroxyl, and phosphoryl and so on.
(4) The melanin isolated from E. pisciphila ACCC32496mycelium is typical of DHN melanin. The melanin synthesis of E. pisciphila ACCC32496mycelium could be specifically inhibited by tricyclazole. There was no significant effect of tricyclazole on the mycelial growth and spore production of E. pisciphila ACCC32496when the concentration of tricyclazole was not higher than10μg/ml. The melanin content of E. pisciphila ACCC32496mycelium was increased significantly when the range of Cd concentration in liquid medium was50-350mg/L. Biomass of the mycelium in which the melanin synthesis was inhibited by tricyclazole was significantly smaller than normal mycelium under50-200mg/L Cd stress, which indicated the melanin had a role in the Cd tolerance of E. pisciphila ACCC32496.
(5) The content of N, K and Fe was decreased significantly, that of P, Mg and Ca was increased significantly in the mycelium of E. pisciphila ACCC32496under Cd stress. The content of S was increased significantly when the concentration of Cd in liquid medium was100mg/L. The production of organic acids by E. pisciphila ACCC32496mycelium was promoted by Cd stress, and the pH value in liquid medium was decreased. Oxalic acid was the main organic acid produced by E. pisciphila ACCC32496mycelium. The content of oxalic acid was increased significantly with the increase of Cd concentration in liquid medium.
(6) The rate of superoxide anion formation, content of MDA and H2O2was increased significantly in the mycelium of E. pisciphila ACCC32496under Cd stress. The activity of SOD and CAT, content of GSH and-SH compounds, and the T-AOC was increased with the increase of Cd concentration within the certain range.
These results suggested that E. pisciphila ACCC32496, a DSE strain isolated from Pb-Zn mine area with serious heavy metal pollution, had a strong tolerance and accumulation ability for Cd. The tolerance mechanisms to Cd of E. pisciphila ACCC32496included:①Extracellular mechanisms included increased secretion of extracellular low molecular weight organic acids, especially oxalic acid; the adsorption of Cd by cell wall; and increased synthesis of the special components-melanin in the mycelium.②Intracellular mechanisms included enhanced activity of antioxidant enzymes such as SOD and CAT in the mycelium; increased synthesis of GSH and other thiol compounds; and increased contents of mineral elements (P, S, Mg and Ca) in mycelium. So the tolerance of E. pisciphila ACCC32496was enhanced.
本研究以分离自重金属严重污染的云南省会泽铅锌矿区自然生长的密序野古草(Arundinella bengalensis (Spreng.) Druce)根内的1株DSE真菌—嗜鱼外瓶霉(Exophiala pisciphila ACCC32496)为研究对象,浓度为0-400mg/L的Cd胁迫处理下,研究菌丝Cd富集量、Cd化学形态与亚细胞分布、细胞壁Cd吸附能力与特征、Cd吸附基团、菌丝黑色素性质与特征、低分子量有机酸分泌、矿质营养、抗氧化系统等方面的内容,分析该菌株耐受Cd的胞外与胞内机制,得到以下主要结果：
(1) E. pisciphila ACCC32496有很强的Cd耐性和富集能力。固体和液体培养情况下,采用直线内插法计算Cd对E. pisciphila ACCC32496的半数生长抑制浓度值(EC50),分别为332.2和111.2mg/L。Cd浓度为400mg/L时,E. pisciphila ACCC32496菌丝的Cd含量达到51.43mg/g干菌丝。
(2)采用扫描电镜—能谱、透射电镜和透射电镜—能谱分析,结合差速离心法分离E. pisciphila ACCC32496菌丝亚细胞组分(细胞壁、细胞器和可溶性组分),发现Cd主要分布在菌丝细胞壁上。采用化学试剂逐步提取法,研究表明菌丝Cd的化学形态主要为醋酸提取态(FHAc)和氯化钠提取态(FNaCl)。
(3)0.1M HCl和Na2EDTA从E. pisciphila ACCC32496菌丝解吸出来的Cd占菌丝Cd含量的63.0%-83.5%,0.1M CaCl2能够解吸8.3%-43.8%,0.1M NaOH能够解吸0.9%-5.6%。
(4)在初始Cd浓度为25～400mg/L, pH值5.0,转速120rpm和30℃条件下, E. pisciphila ACCC32496菌丝吸附Cd的过程符合Langmuir吸附等温模型,吸附Cd的动力学实验数据符合准二级速率方程。傅里叶红外光谱(FTIR)分析表明,吸附Cd的化学基团涉及氨基、酰氨基、羧基、羟基和磷酰基等。
(5) E. pisciphila ACCC32496菌丝黑色素属于典型的DHN型黑色素。三环唑能特异性抑制E. pisciphila ACCC32496菌丝黑色素合成,浓度不高于10μg/ml的三环唑对E. pisciphila ACCC32496菌丝生长与孢子产生量没有明显影响。Cd浓度在50-350mg/L, E. pisciphila ACCC32496菌丝黑色素含量有显著增加。50～200mg/L Cd胁迫下,采用三环唑抑制E. pisciphila ACCC32496菌丝黑色素合成,该菌丝生物量显著小于正常菌丝,Cd富集量大于正常菌丝,表明黑色素在该菌株Cd耐性中有作用。
(6)Cd胁迫导致E. pisciphila ACCC32496菌丝N、K和Fe含量显著下降,P、Mg和Ca含量显著增加,S含量在Cd浓度为100mg/L时显著增加。Cd胁迫促进E. pisciphila ACCC32496菌丝产酸,培养液pH值下降。采用高效液相色谱法(HPLC)分析培养液中的低分子量有机酸,表明E. pisciphila ACCC32496菌丝主要产生草酸,培养液中菌丝草酸分泌量随Cd处理浓度增加而显著增加。
(7)Cd胁迫导致E. pisciphila ACCC32496菌丝超氧阴离子生成速率、MDA和H2O2含量显著增加。SOD酶与CAT酶活性、GSH与-SH化合物含量以及T-AOC在一定Cd浓度范围内,随着Cd浓度增加而增强。
以上结果表明,分离自重金属污染严重的铅锌矿区的DSE菌株E. pisciphila ACCC32496对Cd有很强的耐性与富集能力。E. pisciphila ACCC32496对Cd的耐性机制：①胞外机制包括：增加低分子量有机酸的分泌,尤其是草酸的分泌；通过菌丝细胞壁对的Cd吸附作用,以及增加细胞壁上的特殊组分—黑色素的合成。②胞内机制包括：通过增强菌丝细胞内SOD, CAT等抗氧化酶的活性,增加GSH等巯基化合物的合成,以及提高菌丝中P, S、Mg和Ca等矿质元素的含量,提高E. pisciphila ACCC32496对Cd的耐受能力。
本文通过铅锌矿区典型DSE菌株对Cd的富集特征和耐性机制的初步研究,有助于理解特殊生境—重金属严重污染的铅锌矿区中特殊生物类群—DSE的生态学功能,并为进一步研究DSE在重金属污染环境的植被重建与修复可能应用打下了一定的基础。
Cadmium (Cd) pollution caused by mining of Lead (Pb) and Zinc (Zn) in Pb-Zn mine area is one of the most serious environmental problems in Yunnan. The roots of plants naturally growing in Pb-Zn mine areas are commonly colonized by dark septate endophytes (DSE) suggestes that DSE may play an important role in adaptation to heavy metal stress of these plants. Based on these facts, to relise the Cd tolerance and mechanisms of DSE from Pb-Zn mine area may help us to elucidate biological functions of DSE in the special ecosystem and to explain the relationship between DSE and heavy metal tolerance of their host plants in Pb-Zn mine area. Meanwhile, this research work is also theoretically and practically significance for making use of DSE-plants association to improve the heavy metal tolerance of plants to restore vegetation in Cd polluted environment.
Exophiala pisciphila ACCC32496, a fungus of DSE isolated from the roots of Arundinella bengalensis (Spreng.) Druce which is wild plant grown on Pb-Zn mine area with serious heavy metals pollution in Huze County, Yunnan Province was selected in this thesis. The extracellular and intracellular tolerance mechanisms to Cd of Exophiala pisciphila ACCC32496are analyzed by studies on Cd accumulation of mycelium, Cd chemical forms and subcellular distribution, Cd adsorption capacity and characteristics of cell wall, chemical groups for Cd adsorption, physical and chemical characteristics of melanin from mycelium, secretion of low molecular weight organic acid, mineral nutrition, antioxidant system and so on which are responses to Cd stress with concentration of0～400mg/L.
The main results are as follows:
(1) A relative high Cd tolerance and accumulation ability of E. pisciphila ACCC32496was founded. The50%effective inhibiting concentration (EC50) of Cd to E. pisciphila ACCC32496was calculated by linear interpolation and the result was332.2and111.2mg/L by solid and liquid culture respectively.89.02mg Cd per g dry mycelium was accumulated by E. pisciphila ACCC32496when the concentration of Cd was400mg/L in liquid medium.
(2) The mycelium of E. pisciphila ACCC32496were analyzed by SEM-EDS, TEM and TEM-EDS, and the subcellular fractions, ie cell wall, organelles and soluble fraction, were separated by differential centrifugation. The results showed that Cd was mainly distributed in the cell wall of E. pisciphila ACCC32496. Cd associated with different chemical forms was successively extracted by designated solutions in the following order,80%ethanol, deionized water,1M NaCl,2%acetic acid and0.6M HCl. Acetic acid extractable (FHAc) and sodium chloride extractable (FNaCl) was the main chemical form of Cd.
(2) About63.0%～83.5%of the total Cd in the mycelium of E. pisciphila ACCC32496could be desorbed by0.1M HCl or0.1M Na2EDTA,8.3%-43.8%by0.1M CaCl2, and0.9%-5.6%by0.1M NaOH.
(3) Cd adsorption process of E. pisciphila ACCC32496mycelium can be well described by Langmuir adsorption isotherm model. Kinetics data for the adsorption of Cd from aqueous solutions by E. pisciphila ACCC32496mycelium were in good agreement with the pseudo-second rate equation within an initial concentration range of25-400mg/L, pH value of5.0, an agitation speed range of120rpm and an experimental temperature of30℃. The chemical groups of E. pisciphila ACCC32496mycelium involving in adsorption of Cd involved amino, amido, carboxyl, hydroxyl, and phosphoryl and so on.
(4) The melanin isolated from E. pisciphila ACCC32496mycelium is typical of DHN melanin. The melanin synthesis of E. pisciphila ACCC32496mycelium could be specifically inhibited by tricyclazole. There was no significant effect of tricyclazole on the mycelial growth and spore production of E. pisciphila ACCC32496when the concentration of tricyclazole was not higher than10μg/ml. The melanin content of E. pisciphila ACCC32496mycelium was increased significantly when the range of Cd concentration in liquid medium was50-350mg/L. Biomass of the mycelium in which the melanin synthesis was inhibited by tricyclazole was significantly smaller than normal mycelium under50-200mg/L Cd stress, which indicated the melanin had a role in the Cd tolerance of E. pisciphila ACCC32496.
(5) The content of N, K and Fe was decreased significantly, that of P, Mg and Ca was increased significantly in the mycelium of E. pisciphila ACCC32496under Cd stress. The content of S was increased significantly when the concentration of Cd in liquid medium was100mg/L. The production of organic acids by E. pisciphila ACCC32496mycelium was promoted by Cd stress, and the pH value in liquid medium was decreased. Oxalic acid was the main organic acid produced by E. pisciphila ACCC32496mycelium. The content of oxalic acid was increased significantly with the increase of Cd concentration in liquid medium.
(6) The rate of superoxide anion formation, content of MDA and H2O2was increased significantly in the mycelium of E. pisciphila ACCC32496under Cd stress. The activity of SOD and CAT, content of GSH and-SH compounds, and the T-AOC was increased with the increase of Cd concentration within the certain range.
These results suggested that E. pisciphila ACCC32496, a DSE strain isolated from Pb-Zn mine area with serious heavy metal pollution, had a strong tolerance and accumulation ability for Cd. The tolerance mechanisms to Cd of E. pisciphila ACCC32496included:①Extracellular mechanisms included increased secretion of extracellular low molecular weight organic acids, especially oxalic acid; the adsorption of Cd by cell wall; and increased synthesis of the special components-melanin in the mycelium.②Intracellular mechanisms included enhanced activity of antioxidant enzymes such as SOD and CAT in the mycelium; increased synthesis of GSH and other thiol compounds; and increased contents of mineral elements (P, S, Mg and Ca) in mycelium. So the tolerance of E. pisciphila ACCC32496was enhanced.
引文
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