两种药用植物内生真菌次生代谢产物及其生物活性的研究
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摘要
植物内生真菌是具有高度多样性的微生物资源，代谢产物多种多样，目前被认为是抗菌、抗病毒、抗肿瘤、抗氧化、杀虫等天然活性物质的重要资源。为了寻找更多的生物活性物质，本论文采用活性追踪的方法，研究了4株来源于药用植物的内生真菌的活性代谢产物。内容包括：药用植物（杜仲和无花果）内生真菌的分离的初步鉴定；抗菌活性菌株的分级组合筛选；活性菌株的鉴定和发酵条件考察；活性成分的追踪分离；单体化合物的结构解析；单体化合物生物活性的初步评价。概括如下:
（1）以杜仲和无花果为研究对象，共获得了119株内生真菌。从杜仲根、茎、叶中分离得到62株内生真菌，初步形态学鉴定，这些内生真菌分属于7目，9科，15属，其中曲霉属Aspergillus sp.，镰孢霉属Fusrium sp.，链格孢属Alternaria sp.是杜仲内生真菌的优势种群。从无花果根、茎、叶中分离得到57株内生真菌，初步形态学鉴定，分属于7目，10科，21属。其中镰孢霉属Fusrium sp.，青霉属Penicillium sp.，曲霉属Aspergillus sp.是无花果内生真菌的优势种属。不同部位分离内生真菌的数量、种类和分布不尽相同，这就表明这两种药用植物的不同部位内生真菌的数量、分布和种群存在差异。
（2）采用抗菌活性筛选为主、代谢产物化学成分筛选为辅的二级组合筛选模式，得到如下结果：抗菌活性初筛确定活性菌株共有20株（杜仲内生真菌11株，无花果内生真菌9株），筛选率为16.8%；抗菌活性复筛筛选到12株高抗菌活性的内生真菌，筛选率为10.1%；结合化学成分复筛最后确定了ER12、EL09、FR02、FL10这4株具有高抗菌活性，并且代谢产物种类丰富的内生真菌作为本论文的研究对象。
（3）根据菌株的形态、培养特征、18S rDNA以及ITS序列分析结果，对活性菌株ER12、EL09、FR02和FL10进行菌种鉴定，分别鉴定为刀孢蜡蚧菌、黑曲霉、溜曲霉以及三线镰孢。以菌丝体生物量、发酵产物重量、抗菌活性、薄层色谱分析以及高效液相色谱分析为评价依据，对4株活性内生真菌进行了发酵产物稳定性试验，培养基选择试验，发酵时间试验，萃取实验，确定了4株活性内生真菌的扩大培养条件以及提取条件。
（4）经过扩大培养，采用常规的硅胶柱层析、反相硅胶柱层析，凝胶Sephadex LH-20柱层析、制备薄层层析以及重结晶等分离手段，从4株活性内生真菌分离到90个单体化合物。利用各种现代波谱技术（EI-MS、HR-ESI-MS、1H-NMR、13C-NMR、DEPT、1H-1HCOSY、HSQC、HMBC等）并结合化学方法鉴定了这90个化合物的结构，其中新化合物3个，分别是malformin E（19）、cyclo-(N-methyl-Trp-Leu)（62）和helovlic acid ester（83）。
从ER12中分离到34个化合物，其代谢产物的结构类型是12个环二肽类化合物（3-10，13-16），1个新的环五肽化合物（19），4个fumiquinazoline生物碱类化合物（17，18，22，23），2个二苯酮类化合物（20，21），1个咪唑类化合物（12），2个甾体化合物（1，2），8个苯的衍生物（11，24-28，31，32）及4个核酸苷（29，30，33，34）。从EL09中分离到18个化合物，其代谢产物的结构类型是9个甾体类化合物（38-44,1,2），3个脂肪酸（35-37），2个呋喃类化合物（45，46），2个多羟基醇化合物（47，48）及2个吲哚类化合物（49，50）。从FR02中分离到22个化合物，其代谢产物的结构类型是13个吲哚二酮哌嗪类化合物（53-65，其中62为新化合物，65为新天然产物），2个萜类化合物（51，52），2个甾体化合物（1，39），2个多元羧酸（67，68）和1个多元醇（66）。从FL10中分离到33个化合物，其代谢产物的结构类型是7个gliotoxin类化合物（74-80），3个烟曲霉酸的衍生物（81-83），3个环二肽化合物（13，14，84），5个脂肪酸（69-71，36，37），4个甾体化合物（1，39，72，73），3个苯的衍生物（87-89），4个碱基或核酸苷（29，30，85，86）及4个多元羧酸或多元醇（47，48，68，90）。
（5）采用MIC法，以11种指示菌（4个细菌和7个植物病原真菌）为模型，对4株活性内生真菌产生的90个单体化合物进行抑菌活性评价，结果表明有26个化合物对指示菌显示了较强的抑制作用。新化合物19（malformin E）和83（helovlic acid ester）对多种指示菌表现了很强的抗菌作用。综合分析抗菌活性测试的结果，明确了4株活性内生真菌生物活性物质的类别，ER12Lecanicillium psalliotae的活性物质主要是fumiquinazoline类生物碱和环肽类化合物；EL09Aspergillus niger的活性物质主要是甾醇类和呋喃类化合物；FR02Aspergillus tamarii的活性物质主要是吲哚二酮哌嗪生物碱类化合物；FL10Fusarium tricinctumi的活性物质主要是gliotoxin类生物碱和烟曲霉酸类化合物。
采用MTT法，以3个肿瘤细胞株（MCF-7人乳腺癌细胞、HepG2人肝癌细胞、A549人肺癌细胞）为模型，对分离得到的新化合物和生物碱类代谢产物的抗肿瘤活性进行了初步评价，结果表明这些化合物对不同肿瘤细胞系表现出不同程度的增殖抑制活性。其中新化合物malformin E（19）MCF-7和HepG2系表现出很好的细胞毒活性，IC50分别是0.65和2.42μM；fumiquinazoline C（18）和fumiquinazoline J（23）对HepG2和A549肿瘤细胞的增殖有抑制作用，verruculogen（56）对HepG2和A549肿瘤细胞表现出很强的细胞毒性，IC50分别是1.95和2.56μM。
总之，本文经过筛选获得4株活性内生真菌，通过分离鉴定阐明了4株内生真菌中90个化合物的结构，其中包括3个新化合物。评价了这些单体化合物的抗菌活性和抗肿瘤活性，发现了26个单体化合物具有较强抗菌活性和4个单体化合物具有较强抗肿瘤活性。上述研究结果证明植物内生真菌作为植物生态一个重要的组成部分，是新结构和新活性物质的主要来源，是寻找药物先导化合物的重要资源。
Endophytic fungi are a special and important group of microorganisms withtaxonomic diversity, which show high potential as sources of antimicrobial,antiviral, anticancer, antioxidant, and insecticidal compounds. In order toinvestigate the potential bioactive compounds derived from endophytic fungi,this dissertation described the discovery of several antimicrobial compoundsisolated from four endophytic fungi of medicinal plants by bioassay-guidedfractionation. Studies include isolating of endophytic fungi, seleeting aimedstrains, fermentation studies, bioassay-guided fractionation, structural elucidation,preliminary evaluation of antimicrobial and anti-tumor activities of purecompounds. The results are concluded as follows:
Sixty-two strains isolated from roots, stems and leaves of Eucommiaulmoides, were classified, identified, and belonged to fifteen genera, ninefamilies, and seven orders according to their morphological and micro-structurecharacters. Alternaria sp., Fusrium sp. and Alternaria sp. are dominantendophytic fungi population in Eucommia ulmoides. Fifty-seven strains fromFicus carice were classified, identified, and belonged to twenty-one genera, tenfamilies, and seven orders while Fusrium sp., Penicillium sp. and Alternaria sp.are dominant endophytic fungi population. It showed that the quantities, species,and distribution of the endophytic fungus varied in different parts of Eucommiaulmoides and Ficus carice.
The endophytic fungi isolated from Eucommia ulmoides and Ficus carice,were first screened by antimicrobial assay to obtain20strains which showedstrong antimicrobial activities, and possessed16.8%of total119strains tested.The20strains were subjected to the flow antimicrobial secondary screening and10strains were found to have more strong activities, which possessed10.1%oftotal119strains tested. On the basis of antimicrobial activities, the results of TLC and HPLC analysis, four ested strains, ER12, EL09, FR02and FL10, werechosen as the aimed strains to investigate their bioactive metabolites in thisstudy.
According to their morphology, cultural characteristics,18S rDNA and ITSsequences, the strains ER12, EL09, FR02and FL10were indentified asLecanicillium psalliotae, Aspergillus niger, Aspergillus tamari and Fusariumtricinctum, respectively. On the basis of mycelia biomass, weight of fermentationextracts, antimicrobial activities, the results of TLC and HPLC analysis,stability-tests for the bioactive components and fermentation studies perfomredon the aimed strains. The time course experiments for the fermentation of fourstrains were then carried out, followed by solvent extraction tests for the activecomponents. Then, large-scale fermentation and preparation of the activefractions were perfomred to obtain the active fractions of the four strains.
Ninety compounds were isolated from the four active strains by repeatedcolumn chromatography on silica gel, Sephadex LH-20, preparative thin layerchromatography (PTLC) and recrystallization. The structures of thesecompounds were elucidated by means of spectroscopic methods includingESI-MS, HR-ESI-MS,1D-NMR (1H NMR,13C NMR, DEPT) and2D-NMR(1H-1H COSY, HSQC, HMBC) as well as chemical method. Among them therewere three new compounds, malformin E (19), cyclo-(N-methyl-Trp-Leu)(62)and helovlic acid ester (83).
Thirty-four compounds were isolated from fungus ER12, and the chemicalstructure types of compounds were involved in cyclic dipeptides (3-10,13-16),malformin E (19), fumiquinazolines (17,18,22,23), diphenyl ketones (20,21),imidazoles (12), sterols (1,2), benzene derivatives (11,24-28,31,32) andnucleosides (29,30,33,34). Eighteen compounds were isolated from fungusEL09, and the structure types of compounds were involved in sterols (38-44,1,2), fatty acids (35-37), furan derivatives (45,46), polyhydric alcohols (47,48)and indole derivatives (49,50). Twenty-two compounds were isolated fromfungus FR02, and the structure types of compounds were involved in indolyldiketopiperazine analogs (53-65), terpenes (51,52), sterols (1,39),polycarboxylic acids (67,68) and polyhydric alcohols (66). Thirty-threecompounds were isolated from fungus Fl10, and the structure types of compounds were involved in gliotoxins (74-80), helvolic acid derivatives(81-83), cyclic dipeptides (13,14,84), fatty acids (69-71,36,37), sterols (1,39,72,73), benzene derivatives (87-89), nucleosides (29,30,85,86), polyhydricalcohols and polycarboxylic acids (47,48,68,90).
Ninety compounds were evaluated for their antimicrobial activities againseleven tested strains. The results indicated that twenty-six compounds showedstrong antimicrobial activities and the structure types of bioactive compoundswere involved in indolyl diketopiperazines, gliotoxins, quinazoline alkaloids,cyclic dipeptides and sterols. Remarkably, malformin E and helovlic acid estershow strong antimicrobial activities against different tested strains. The results ofantibacterial activity test indicated bioactive substances of four active fungi.Active substances of ER12were mainly fumiquinazoline alkaloids and cyclicpeptide compounds. Active substances of EL09were sterols and furans. Activesubstances of FR02were indolyl diketopiperazines. Active substances of FL10were gliotoxins and helvolic acid derivatives. Three new compounds and isolatedalkaloids were evaluated for their cytotoxicities against three cancer cell lines,MCF-7, HepG2and A549, by the MTT method. The results indicated that four ofthem showed significant cytotoxicities against different cancer cell lines andothers were weak. Among them, new compond, malformin E, showed significantinhibitory activities against MCF-7and HepG2cell lines with IC500.65,2.42μMrespectively. Fumiquinazoline C and fumiquinazoline J exhibited moderateactivities against HepG2and A549. Verruculogen showed significant inhibitoryactivities against HepG2and A549with IC501.95,2.56μM.
Summarily, this work obtained four active fungi from two medicinal plantsand ninety compounds, including three new compounds and a new naturalproduct, were isolated from the fungi. The bioactivities results indicated thattwenty-six compounds showed significant antimicrobial activities and fourcompounds showed significant cytotoxicities against different cancer cell lines.This thesis indieated that endophytic fungi, as an important part of plant system,which contain novel and bioactive compounds in its secondary metabolisms, isan important source for searching lead compounds for drugs.
（1）以杜仲和无花果为研究对象，共获得了119株内生真菌。从杜仲根、茎、叶中分离得到62株内生真菌，初步形态学鉴定，这些内生真菌分属于7目，9科，15属，其中曲霉属Aspergillus sp.，镰孢霉属Fusrium sp.，链格孢属Alternaria sp.是杜仲内生真菌的优势种群。从无花果根、茎、叶中分离得到57株内生真菌，初步形态学鉴定，分属于7目，10科，21属。其中镰孢霉属Fusrium sp.，青霉属Penicillium sp.，曲霉属Aspergillus sp.是无花果内生真菌的优势种属。不同部位分离内生真菌的数量、种类和分布不尽相同，这就表明这两种药用植物的不同部位内生真菌的数量、分布和种群存在差异。
（2）采用抗菌活性筛选为主、代谢产物化学成分筛选为辅的二级组合筛选模式，得到如下结果：抗菌活性初筛确定活性菌株共有20株（杜仲内生真菌11株，无花果内生真菌9株），筛选率为16.8%；抗菌活性复筛筛选到12株高抗菌活性的内生真菌，筛选率为10.1%；结合化学成分复筛最后确定了ER12、EL09、FR02、FL10这4株具有高抗菌活性，并且代谢产物种类丰富的内生真菌作为本论文的研究对象。
（3）根据菌株的形态、培养特征、18S rDNA以及ITS序列分析结果，对活性菌株ER12、EL09、FR02和FL10进行菌种鉴定，分别鉴定为刀孢蜡蚧菌、黑曲霉、溜曲霉以及三线镰孢。以菌丝体生物量、发酵产物重量、抗菌活性、薄层色谱分析以及高效液相色谱分析为评价依据，对4株活性内生真菌进行了发酵产物稳定性试验，培养基选择试验，发酵时间试验，萃取实验，确定了4株活性内生真菌的扩大培养条件以及提取条件。
（4）经过扩大培养，采用常规的硅胶柱层析、反相硅胶柱层析，凝胶Sephadex LH-20柱层析、制备薄层层析以及重结晶等分离手段，从4株活性内生真菌分离到90个单体化合物。利用各种现代波谱技术（EI-MS、HR-ESI-MS、1H-NMR、13C-NMR、DEPT、1H-1HCOSY、HSQC、HMBC等）并结合化学方法鉴定了这90个化合物的结构，其中新化合物3个，分别是malformin E（19）、cyclo-(N-methyl-Trp-Leu)（62）和helovlic acid ester（83）。
从ER12中分离到34个化合物，其代谢产物的结构类型是12个环二肽类化合物（3-10，13-16），1个新的环五肽化合物（19），4个fumiquinazoline生物碱类化合物（17，18，22，23），2个二苯酮类化合物（20，21），1个咪唑类化合物（12），2个甾体化合物（1，2），8个苯的衍生物（11，24-28，31，32）及4个核酸苷（29，30，33，34）。从EL09中分离到18个化合物，其代谢产物的结构类型是9个甾体类化合物（38-44,1,2），3个脂肪酸（35-37），2个呋喃类化合物（45，46），2个多羟基醇化合物（47，48）及2个吲哚类化合物（49，50）。从FR02中分离到22个化合物，其代谢产物的结构类型是13个吲哚二酮哌嗪类化合物（53-65，其中62为新化合物，65为新天然产物），2个萜类化合物（51，52），2个甾体化合物（1，39），2个多元羧酸（67，68）和1个多元醇（66）。从FL10中分离到33个化合物，其代谢产物的结构类型是7个gliotoxin类化合物（74-80），3个烟曲霉酸的衍生物（81-83），3个环二肽化合物（13，14，84），5个脂肪酸（69-71，36，37），4个甾体化合物（1，39，72，73），3个苯的衍生物（87-89），4个碱基或核酸苷（29，30，85，86）及4个多元羧酸或多元醇（47，48，68，90）。
（5）采用MIC法，以11种指示菌（4个细菌和7个植物病原真菌）为模型，对4株活性内生真菌产生的90个单体化合物进行抑菌活性评价，结果表明有26个化合物对指示菌显示了较强的抑制作用。新化合物19（malformin E）和83（helovlic acid ester）对多种指示菌表现了很强的抗菌作用。综合分析抗菌活性测试的结果，明确了4株活性内生真菌生物活性物质的类别，ER12Lecanicillium psalliotae的活性物质主要是fumiquinazoline类生物碱和环肽类化合物；EL09Aspergillus niger的活性物质主要是甾醇类和呋喃类化合物；FR02Aspergillus tamarii的活性物质主要是吲哚二酮哌嗪生物碱类化合物；FL10Fusarium tricinctumi的活性物质主要是gliotoxin类生物碱和烟曲霉酸类化合物。
采用MTT法，以3个肿瘤细胞株（MCF-7人乳腺癌细胞、HepG2人肝癌细胞、A549人肺癌细胞）为模型，对分离得到的新化合物和生物碱类代谢产物的抗肿瘤活性进行了初步评价，结果表明这些化合物对不同肿瘤细胞系表现出不同程度的增殖抑制活性。其中新化合物malformin E（19）MCF-7和HepG2系表现出很好的细胞毒活性，IC50分别是0.65和2.42μM；fumiquinazoline C（18）和fumiquinazoline J（23）对HepG2和A549肿瘤细胞的增殖有抑制作用，verruculogen（56）对HepG2和A549肿瘤细胞表现出很强的细胞毒性，IC50分别是1.95和2.56μM。
总之，本文经过筛选获得4株活性内生真菌，通过分离鉴定阐明了4株内生真菌中90个化合物的结构，其中包括3个新化合物。评价了这些单体化合物的抗菌活性和抗肿瘤活性，发现了26个单体化合物具有较强抗菌活性和4个单体化合物具有较强抗肿瘤活性。上述研究结果证明植物内生真菌作为植物生态一个重要的组成部分，是新结构和新活性物质的主要来源，是寻找药物先导化合物的重要资源。
Endophytic fungi are a special and important group of microorganisms withtaxonomic diversity, which show high potential as sources of antimicrobial,antiviral, anticancer, antioxidant, and insecticidal compounds. In order toinvestigate the potential bioactive compounds derived from endophytic fungi,this dissertation described the discovery of several antimicrobial compoundsisolated from four endophytic fungi of medicinal plants by bioassay-guidedfractionation. Studies include isolating of endophytic fungi, seleeting aimedstrains, fermentation studies, bioassay-guided fractionation, structural elucidation,preliminary evaluation of antimicrobial and anti-tumor activities of purecompounds. The results are concluded as follows:
Sixty-two strains isolated from roots, stems and leaves of Eucommiaulmoides, were classified, identified, and belonged to fifteen genera, ninefamilies, and seven orders according to their morphological and micro-structurecharacters. Alternaria sp., Fusrium sp. and Alternaria sp. are dominantendophytic fungi population in Eucommia ulmoides. Fifty-seven strains fromFicus carice were classified, identified, and belonged to twenty-one genera, tenfamilies, and seven orders while Fusrium sp., Penicillium sp. and Alternaria sp.are dominant endophytic fungi population. It showed that the quantities, species,and distribution of the endophytic fungus varied in different parts of Eucommiaulmoides and Ficus carice.
The endophytic fungi isolated from Eucommia ulmoides and Ficus carice,were first screened by antimicrobial assay to obtain20strains which showedstrong antimicrobial activities, and possessed16.8%of total119strains tested.The20strains were subjected to the flow antimicrobial secondary screening and10strains were found to have more strong activities, which possessed10.1%oftotal119strains tested. On the basis of antimicrobial activities, the results of TLC and HPLC analysis, four ested strains, ER12, EL09, FR02and FL10, werechosen as the aimed strains to investigate their bioactive metabolites in thisstudy.
According to their morphology, cultural characteristics,18S rDNA and ITSsequences, the strains ER12, EL09, FR02and FL10were indentified asLecanicillium psalliotae, Aspergillus niger, Aspergillus tamari and Fusariumtricinctum, respectively. On the basis of mycelia biomass, weight of fermentationextracts, antimicrobial activities, the results of TLC and HPLC analysis,stability-tests for the bioactive components and fermentation studies perfomredon the aimed strains. The time course experiments for the fermentation of fourstrains were then carried out, followed by solvent extraction tests for the activecomponents. Then, large-scale fermentation and preparation of the activefractions were perfomred to obtain the active fractions of the four strains.
Ninety compounds were isolated from the four active strains by repeatedcolumn chromatography on silica gel, Sephadex LH-20, preparative thin layerchromatography (PTLC) and recrystallization. The structures of thesecompounds were elucidated by means of spectroscopic methods includingESI-MS, HR-ESI-MS,1D-NMR (1H NMR,13C NMR, DEPT) and2D-NMR(1H-1H COSY, HSQC, HMBC) as well as chemical method. Among them therewere three new compounds, malformin E (19), cyclo-(N-methyl-Trp-Leu)(62)and helovlic acid ester (83).
Thirty-four compounds were isolated from fungus ER12, and the chemicalstructure types of compounds were involved in cyclic dipeptides (3-10,13-16),malformin E (19), fumiquinazolines (17,18,22,23), diphenyl ketones (20,21),imidazoles (12), sterols (1,2), benzene derivatives (11,24-28,31,32) andnucleosides (29,30,33,34). Eighteen compounds were isolated from fungusEL09, and the structure types of compounds were involved in sterols (38-44,1,2), fatty acids (35-37), furan derivatives (45,46), polyhydric alcohols (47,48)and indole derivatives (49,50). Twenty-two compounds were isolated fromfungus FR02, and the structure types of compounds were involved in indolyldiketopiperazine analogs (53-65), terpenes (51,52), sterols (1,39),polycarboxylic acids (67,68) and polyhydric alcohols (66). Thirty-threecompounds were isolated from fungus Fl10, and the structure types of compounds were involved in gliotoxins (74-80), helvolic acid derivatives(81-83), cyclic dipeptides (13,14,84), fatty acids (69-71,36,37), sterols (1,39,72,73), benzene derivatives (87-89), nucleosides (29,30,85,86), polyhydricalcohols and polycarboxylic acids (47,48,68,90).
Ninety compounds were evaluated for their antimicrobial activities againseleven tested strains. The results indicated that twenty-six compounds showedstrong antimicrobial activities and the structure types of bioactive compoundswere involved in indolyl diketopiperazines, gliotoxins, quinazoline alkaloids,cyclic dipeptides and sterols. Remarkably, malformin E and helovlic acid estershow strong antimicrobial activities against different tested strains. The results ofantibacterial activity test indicated bioactive substances of four active fungi.Active substances of ER12were mainly fumiquinazoline alkaloids and cyclicpeptide compounds. Active substances of EL09were sterols and furans. Activesubstances of FR02were indolyl diketopiperazines. Active substances of FL10were gliotoxins and helvolic acid derivatives. Three new compounds and isolatedalkaloids were evaluated for their cytotoxicities against three cancer cell lines,MCF-7, HepG2and A549, by the MTT method. The results indicated that four ofthem showed significant cytotoxicities against different cancer cell lines andothers were weak. Among them, new compond, malformin E, showed significantinhibitory activities against MCF-7and HepG2cell lines with IC500.65,2.42μMrespectively. Fumiquinazoline C and fumiquinazoline J exhibited moderateactivities against HepG2and A549. Verruculogen showed significant inhibitoryactivities against HepG2and A549with IC501.95,2.56μM.
Summarily, this work obtained four active fungi from two medicinal plantsand ninety compounds, including three new compounds and a new naturalproduct, were isolated from the fungi. The bioactivities results indicated thattwenty-six compounds showed significant antimicrobial activities and fourcompounds showed significant cytotoxicities against different cancer cell lines.This thesis indieated that endophytic fungi, as an important part of plant system,which contain novel and bioactive compounds in its secondary metabolisms, isan important source for searching lead compounds for drugs.
引文
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