黄花蒿内生放线菌资源及其对黄花蒿生长和青蒿素生物合成的影响
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摘要
黄花蒿是一种重要的药用植物,其代谢产物青蒿素不仅是目前有效的抗疟药物,还具有抗病毒、抗肿瘤等其他的药用和农用价值;但由于青蒿素产量极低,严重限制了其应用范围。植物内生菌以其特殊的性质成为我们寻找替代药源和新活性物质的重要来源。本研究以采自昆明的黄花蒿为对象,分析其内生放线菌群落组成,从中发掘有应用潜力的菌种资源和新物种资源;并对内生放线菌与黄花蒿生长及青蒿素生物合成之间的关系进行了初步探讨。
本研究采用了四种方法进行黄花蒿内生放线菌的分离。首次将研磨珠均质器和干热处理运用于内生放线菌的分离。从黄花蒿全株样品中共分离获得内生放线菌228株。结合形态观察和16S rRNA基因序列分析,将全部分离菌株鉴定到属的水平,结果显示它们分别属于链霉菌属、原小单孢菌属、假诺卡氏菌属、诺卡氏菌属、野野村氏菌属、红球菌属、韩国生工菌属、小单孢菌属、马杜拉放线菌属、链孢囊菌属、拟无枝菌酸菌属、指孢囊菌属、芽生球菌属、糖霉菌属、考克氏菌属、微球菌属、戈登氏菌属、游动四孢菌属共18个已知属以及1个潜在新属。分离频率最高的是链霉菌,其次是原小单孢菌。
对其中6个候选新分类单元的代表菌株进行了包括形态与培养特征观察、生理生化特性、细胞化学组分分析、基因组DNA G+C mol%、DNA同源性和基于16S rRNA基因序列系统发育分析等在内的多相分类研究,确定了它们的分类地位。菌株YIM 65646是小单孢菌科的一个新属,被命名为植物单孢菌属(Plantmonospora gen. nov.),典型种为内生植物单孢菌(Plantmonospora endophytica sp. nov.)。菌株YIM 63111是假诺卡氏菌属的一个新种,被命名为珍贵假诺卡氏菌(Pseudonocardia pretiosum sp. nov.)。菌株YIM 65594、YIM 65638、YIM 65642代表了链霉菌属的一个新种,被命名为内生链霉菌(Streptomyces endophytica sp. nov.),典型菌株为YIM 65594。YIM 65601为野野村氏菌属的一个新种,被命名为内生野野村氏菌(Nonomuraea endophytica)。
以上研究结果充分显示黄花蒿体内蕴藏着大量丰富的放线菌菌种资源,其中也包括许多未被发掘的新物种资源。在此基础上,我们对这些内生放线菌的抗菌、酶活、除草活性及产生聚酮类和非核糖体多肽类物质的潜力进行了检测。
采用琼脂扩散法进行抗菌活性检测,在228株内生放线菌中有15.8%～34.6%的菌株分别对指示菌(金黄色葡萄球菌、白色念珠菌、玉蜀黍长蠕孢菌、燕麦镰孢菌、炭疽病菌、苹果腐烂病菌)具有抑制活性,其中有31株菌(13.6%)表现出较强的广谱抗菌活性。
采用PCR扩增法对166株菌进行了PKS-I,PKS-II和NRPS基因的测定,获得35株(21.1%)PKS-I基因阳性的菌株,75株(45.2%)PKS-II基因阳性的菌株,扩增出NRPS基因的有54株(32.5%)。
用平板筛选的方法,对199株菌进行了酶活检测,从中筛选到7株淀粉酶活性较强的菌株,10株蛋白酶活性较强的菌株,1菌株具有较强的脂肪酶活性(菌落边缘至透明圈边缘的距离>0.5cm);7株纤维素酶活性较强的菌株(菌落边缘至透明圈边缘的距离≥1.0cm)。
选取117株代表性菌株,对其发酵液进行稗草萌发的抑制活性检测,其中有19株菌(16.2%)能完全抑制稗草发芽。
首次对黄花蒿内生放线菌资源进行系统的活性评价,研究结果证实了内生放线菌确实是一类具有天然产物开发潜力的重要资源。从中我们也获得了一批值得后续研究的菌株。
通过回接实验发现,32个菌株对黄花蒿幼苗的生长表现出了不同的影响。大多数菌株不影响幼苗的生长;其中6个菌株对幼苗的生长有一定的促进作用;4株菌对黄花蒿幼苗的生长表现出抑制作用,其中菌株YIM 63111的抑制作用最为强烈。
开展了回接处理后,青蒿素合成途径中相关基因表达水平的定量分析,以及青蒿素含量的检测。结果表明在一定回接处理浓度下,菌株YIM 63111能诱导无菌培养条件下和温室培养条件下生长的黄花蒿植株的CYP71AV1和CPR基因表达水平显著上调,使青蒿素含量提高了30%～40%。这是首次发现内生放线菌对青蒿素的生物合成有诱导作用。
首次采用egfp标记内生的假诺卡氏菌YIM 63111,进行回接定殖研究。结果显示在回接14天后,该菌株在黄花蒿幼苗根表面和内部均有定殖。
本研究揭示了黄花蒿内生放线菌的部分生物学和生态学特性,对于开发内生放线菌的活性代谢产物,认识内生菌与植物之间的关系,利用内生放线菌促进黄花蒿的生长、提高青蒿素含量具有一定的指导作用。
The herb Artemisa annua L. is a significant pharmaceutical plant, which is the producer of artemisinin. Besides anti-malaria, artemisinin and its derivatives have been shown to be effective against tumor, a number of viruses, other prokaryotic and eukaryotic agents. They also show the characteristic of allelopathy. Artemisinin is present in exceedingly small amounts, thereby hindering sufficient production for treating malaria let alone any of the other diseases against which it is effective. It is widely accepted that endophyte is a rich source of functional metabolites. The aim of this study was to investigate the composition of endophytic actinobacteria associated with A. annua collected from Kunming, get valuable and (or) novel resources, and the relationship between endophytic actinobacteria and A. annua preliminarily.
Four methods were employed in actinobacterial endophytes isolation. The Mini-Bead Beater and dry-heating were used firstly in actinobacterial endophytes isolation. A total of 228 endophytic actinobacteria were isolated from samples of A. annua. According to the morphological characteristics and the results of 16S rRNA gene sequences analysis, strains were identified to the genus level. The results showed that the most abundant was Streptomyces, and then Promicromonospora. A diverse range of other rare taxa of Actinomycetales were also isolated, including isolates of the genera Pseudonocardia, Nocardia, Nonomuraea, Rhodococcus, Kribbella, Micromonospora, Actinomadura, Streptosporangium, Amycolatopsis, Dactylosporangium, Blastococcus, Glycomyces, Kocuria, Micrococcus, Gordonia, Planotetraspora and an potential novel genus.
Six candidates were subjected to polyphasic taxonomy study including analysis of morphological and cultural characteristics, physiological and biochemical tests, chemotaxonomic properties, phylogenetic analysis based on 16S rRNA gene sequences and DNA-DNA hybridizations. Strain YIM 65646 was identified as a member of the novel genus of the family Micromonosporaceae, the name Plantmonospora gen. nov. was proposed. Plantmonospora endophytica sp. nov. was assigned as the type species of this novel genus. Strain YIM 63111 was a novel species of the genus Pseudonocardia, and it was named as Pseudonocardia pretiosum sp. nov. Strains YIM 65594, YIM 65638 and YIM 65642 belonged to the novel species Streptomyces endophytica sp. nov., and strain YIM 65594 was assigned as the type strain. Strain YIM 65601 was a new member of the genus Nonomuraea, and the name Nonomuraea endophytica was proposed.
Results of isolation and identification work showed that A. annua harbored abundant endophytic actinobacteria including a lot of undescribed novel species. Furthermore, their antimicrobial, enzyme and herbicidal activities and the potential of produing polyketide or non-ribosomal peptide were estimated.
The agar plate diffusion method was used to investigate the antimicrobial activity of endophytic isolates. There were 15.8%～34.6% of tested strains showed inhibition activity to Staphylococcus aureus, Candida albicans, Helminthosporium maydis, Fusarium avenaceum, Colletotrichum sp. and Cytospora mandshurica. Among them, there were thirty-one strains (13.6%) showed strong and broad-spectrum antimicrobial activities.
The presence of PKS-I, PKS-II and NRPS sequences were investigated in total of 166 strains by specific amplification of total DNA with the corresponding primers. High frequencies of positive PCR amplification were obtained for PKS-II (75 strains, 45.2%), NRPS (54 strains, 32.5%) and PKS-I (35 strains, 21.1%) biosynthetic systems.
In the enzyme plate screening experiment, amount of 199 strains were tested. Seven of them showed great amylase activity, ten strains showed great protease activity, one strain showed great lipase activity (R-r >0.5cm), and seven strains showed great cellulase activity(R-r≥1.0cm).
The results of herbicidal activity screening experiment indicated that 19 out of 117 samples of fermentation broth could inhibit the germination of Echinochloa crusgalli completely.
The results of bioactivity evaluation indicated that endophytic actinobacteria are valuable sources of natural products mining. Moreover, we obtained a batch of bioactive strains, which were the objects in continued studies.
There were 32 isolates used for inoculating A. annua seedlings. Most of them didn’t show effect on the growth of seedlings. There were six strains enhanced the growth of seedlings, and four strains inhibited the growth. It was arrestive that strain YIM 63111 showed the strongest inhibition effect.
Both A. annua seedlings grown in the gnotobiotic system and green house were inoculated with strain YIM 63111. The real time RT-PCR determination revealed that the transcription levels of CYP71AV1 (cytochrome P450 monooxygenase) and CPR (cytochrome P450 oxidoreductase) genes were up-regulated after inoculated with strain YIM 63111. Compared with untreated control, the artemisinin content in the treated plants were increased by 30%～40%. This was the first report about that endophytic actinobacterium was able to induce the biosynthesis of artemisinin.
In this study, strain YIM 63111 was tagged with the egfp gene. Endophytic colonization was observed in the sample, which was incubated for 14 days after inoculated with this strain.
The biological and ecological properties of endophytic actinobacteria isolated from A. annua were demonstrated partly in this dissertation. These findings will guide us to explore bioactive metabolites from endophytic actinobacteria, use them to enhance the growth of A. annua and accumulation of artemisinin, and understand the relationship between endophyte and plants.
本研究采用了四种方法进行黄花蒿内生放线菌的分离。首次将研磨珠均质器和干热处理运用于内生放线菌的分离。从黄花蒿全株样品中共分离获得内生放线菌228株。结合形态观察和16S rRNA基因序列分析,将全部分离菌株鉴定到属的水平,结果显示它们分别属于链霉菌属、原小单孢菌属、假诺卡氏菌属、诺卡氏菌属、野野村氏菌属、红球菌属、韩国生工菌属、小单孢菌属、马杜拉放线菌属、链孢囊菌属、拟无枝菌酸菌属、指孢囊菌属、芽生球菌属、糖霉菌属、考克氏菌属、微球菌属、戈登氏菌属、游动四孢菌属共18个已知属以及1个潜在新属。分离频率最高的是链霉菌,其次是原小单孢菌。
对其中6个候选新分类单元的代表菌株进行了包括形态与培养特征观察、生理生化特性、细胞化学组分分析、基因组DNA G+C mol%、DNA同源性和基于16S rRNA基因序列系统发育分析等在内的多相分类研究,确定了它们的分类地位。菌株YIM 65646是小单孢菌科的一个新属,被命名为植物单孢菌属(Plantmonospora gen. nov.),典型种为内生植物单孢菌(Plantmonospora endophytica sp. nov.)。菌株YIM 63111是假诺卡氏菌属的一个新种,被命名为珍贵假诺卡氏菌(Pseudonocardia pretiosum sp. nov.)。菌株YIM 65594、YIM 65638、YIM 65642代表了链霉菌属的一个新种,被命名为内生链霉菌(Streptomyces endophytica sp. nov.),典型菌株为YIM 65594。YIM 65601为野野村氏菌属的一个新种,被命名为内生野野村氏菌(Nonomuraea endophytica)。
以上研究结果充分显示黄花蒿体内蕴藏着大量丰富的放线菌菌种资源,其中也包括许多未被发掘的新物种资源。在此基础上,我们对这些内生放线菌的抗菌、酶活、除草活性及产生聚酮类和非核糖体多肽类物质的潜力进行了检测。
采用琼脂扩散法进行抗菌活性检测,在228株内生放线菌中有15.8%～34.6%的菌株分别对指示菌(金黄色葡萄球菌、白色念珠菌、玉蜀黍长蠕孢菌、燕麦镰孢菌、炭疽病菌、苹果腐烂病菌)具有抑制活性,其中有31株菌(13.6%)表现出较强的广谱抗菌活性。
采用PCR扩增法对166株菌进行了PKS-I,PKS-II和NRPS基因的测定,获得35株(21.1%)PKS-I基因阳性的菌株,75株(45.2%)PKS-II基因阳性的菌株,扩增出NRPS基因的有54株(32.5%)。
用平板筛选的方法,对199株菌进行了酶活检测,从中筛选到7株淀粉酶活性较强的菌株,10株蛋白酶活性较强的菌株,1菌株具有较强的脂肪酶活性(菌落边缘至透明圈边缘的距离>0.5cm);7株纤维素酶活性较强的菌株(菌落边缘至透明圈边缘的距离≥1.0cm)。
选取117株代表性菌株,对其发酵液进行稗草萌发的抑制活性检测,其中有19株菌(16.2%)能完全抑制稗草发芽。
首次对黄花蒿内生放线菌资源进行系统的活性评价,研究结果证实了内生放线菌确实是一类具有天然产物开发潜力的重要资源。从中我们也获得了一批值得后续研究的菌株。
通过回接实验发现,32个菌株对黄花蒿幼苗的生长表现出了不同的影响。大多数菌株不影响幼苗的生长;其中6个菌株对幼苗的生长有一定的促进作用;4株菌对黄花蒿幼苗的生长表现出抑制作用,其中菌株YIM 63111的抑制作用最为强烈。
开展了回接处理后,青蒿素合成途径中相关基因表达水平的定量分析,以及青蒿素含量的检测。结果表明在一定回接处理浓度下,菌株YIM 63111能诱导无菌培养条件下和温室培养条件下生长的黄花蒿植株的CYP71AV1和CPR基因表达水平显著上调,使青蒿素含量提高了30%～40%。这是首次发现内生放线菌对青蒿素的生物合成有诱导作用。
首次采用egfp标记内生的假诺卡氏菌YIM 63111,进行回接定殖研究。结果显示在回接14天后,该菌株在黄花蒿幼苗根表面和内部均有定殖。
本研究揭示了黄花蒿内生放线菌的部分生物学和生态学特性,对于开发内生放线菌的活性代谢产物,认识内生菌与植物之间的关系,利用内生放线菌促进黄花蒿的生长、提高青蒿素含量具有一定的指导作用。
The herb Artemisa annua L. is a significant pharmaceutical plant, which is the producer of artemisinin. Besides anti-malaria, artemisinin and its derivatives have been shown to be effective against tumor, a number of viruses, other prokaryotic and eukaryotic agents. They also show the characteristic of allelopathy. Artemisinin is present in exceedingly small amounts, thereby hindering sufficient production for treating malaria let alone any of the other diseases against which it is effective. It is widely accepted that endophyte is a rich source of functional metabolites. The aim of this study was to investigate the composition of endophytic actinobacteria associated with A. annua collected from Kunming, get valuable and (or) novel resources, and the relationship between endophytic actinobacteria and A. annua preliminarily.
Four methods were employed in actinobacterial endophytes isolation. The Mini-Bead Beater and dry-heating were used firstly in actinobacterial endophytes isolation. A total of 228 endophytic actinobacteria were isolated from samples of A. annua. According to the morphological characteristics and the results of 16S rRNA gene sequences analysis, strains were identified to the genus level. The results showed that the most abundant was Streptomyces, and then Promicromonospora. A diverse range of other rare taxa of Actinomycetales were also isolated, including isolates of the genera Pseudonocardia, Nocardia, Nonomuraea, Rhodococcus, Kribbella, Micromonospora, Actinomadura, Streptosporangium, Amycolatopsis, Dactylosporangium, Blastococcus, Glycomyces, Kocuria, Micrococcus, Gordonia, Planotetraspora and an potential novel genus.
Six candidates were subjected to polyphasic taxonomy study including analysis of morphological and cultural characteristics, physiological and biochemical tests, chemotaxonomic properties, phylogenetic analysis based on 16S rRNA gene sequences and DNA-DNA hybridizations. Strain YIM 65646 was identified as a member of the novel genus of the family Micromonosporaceae, the name Plantmonospora gen. nov. was proposed. Plantmonospora endophytica sp. nov. was assigned as the type species of this novel genus. Strain YIM 63111 was a novel species of the genus Pseudonocardia, and it was named as Pseudonocardia pretiosum sp. nov. Strains YIM 65594, YIM 65638 and YIM 65642 belonged to the novel species Streptomyces endophytica sp. nov., and strain YIM 65594 was assigned as the type strain. Strain YIM 65601 was a new member of the genus Nonomuraea, and the name Nonomuraea endophytica was proposed.
Results of isolation and identification work showed that A. annua harbored abundant endophytic actinobacteria including a lot of undescribed novel species. Furthermore, their antimicrobial, enzyme and herbicidal activities and the potential of produing polyketide or non-ribosomal peptide were estimated.
The agar plate diffusion method was used to investigate the antimicrobial activity of endophytic isolates. There were 15.8%～34.6% of tested strains showed inhibition activity to Staphylococcus aureus, Candida albicans, Helminthosporium maydis, Fusarium avenaceum, Colletotrichum sp. and Cytospora mandshurica. Among them, there were thirty-one strains (13.6%) showed strong and broad-spectrum antimicrobial activities.
The presence of PKS-I, PKS-II and NRPS sequences were investigated in total of 166 strains by specific amplification of total DNA with the corresponding primers. High frequencies of positive PCR amplification were obtained for PKS-II (75 strains, 45.2%), NRPS (54 strains, 32.5%) and PKS-I (35 strains, 21.1%) biosynthetic systems.
In the enzyme plate screening experiment, amount of 199 strains were tested. Seven of them showed great amylase activity, ten strains showed great protease activity, one strain showed great lipase activity (R-r >0.5cm), and seven strains showed great cellulase activity(R-r≥1.0cm).
The results of herbicidal activity screening experiment indicated that 19 out of 117 samples of fermentation broth could inhibit the germination of Echinochloa crusgalli completely.
The results of bioactivity evaluation indicated that endophytic actinobacteria are valuable sources of natural products mining. Moreover, we obtained a batch of bioactive strains, which were the objects in continued studies.
There were 32 isolates used for inoculating A. annua seedlings. Most of them didn’t show effect on the growth of seedlings. There were six strains enhanced the growth of seedlings, and four strains inhibited the growth. It was arrestive that strain YIM 63111 showed the strongest inhibition effect.
Both A. annua seedlings grown in the gnotobiotic system and green house were inoculated with strain YIM 63111. The real time RT-PCR determination revealed that the transcription levels of CYP71AV1 (cytochrome P450 monooxygenase) and CPR (cytochrome P450 oxidoreductase) genes were up-regulated after inoculated with strain YIM 63111. Compared with untreated control, the artemisinin content in the treated plants were increased by 30%～40%. This was the first report about that endophytic actinobacterium was able to induce the biosynthesis of artemisinin.
In this study, strain YIM 63111 was tagged with the egfp gene. Endophytic colonization was observed in the sample, which was incubated for 14 days after inoculated with this strain.
The biological and ecological properties of endophytic actinobacteria isolated from A. annua were demonstrated partly in this dissertation. These findings will guide us to explore bioactive metabolites from endophytic actinobacteria, use them to enhance the growth of A. annua and accumulation of artemisinin, and understand the relationship between endophyte and plants.
引文
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