Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis

Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis
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DOI:
10.1073/pnas.0812082106
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发表时间:
2009-03-24
影响因子:
11.1
通讯作者:
Spiteller, Dieter
Spiteller, Dieter
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Haeder, Susanne;Wirth, Rainer;Spiteller, Dieter

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切叶蚁如刺顶蚁生活在专性共生与真菌属的Leucoagaricus,他们种植收获的树叶材料。共生真菌反过来又是蚂蚁的主要食物来源。这种互惠关系受到专门的病原真菌Escovopsis sp.的干扰,其可以克服Leucoagaricus sp.并因此破坏蚁群。已经提出切叶蚁的微生物共生体通过产生抗真菌化合物来保护真菌花园免受Escovopsis的侵害[Currie CR,Scott JA,Summerbell RC,Malloch D(1999)Fungus-growing ants use aprotic-producing bacteria to control garden parasites. Nature 398:701-704.]然而,迄今为止,这些化合物的化学性质仍然难以捉摸。本研究对采自3种切叶蚁的19种切叶蚁相关微生物进行了鉴定,其中假诺卡氏菌属5种,革球菌属1种,链霉菌属13种。spinosus、棘突拟步行虫A. echinatior和A. volcanus的16 S-rDNA序列分析。由于链霉菌Ao 10菌株对病原菌Escovopsis具有很高的抗真菌活性,我们确定了其抗真菌活性的分子基础。使用生物测定引导的分级分离、高分辨率电喷雾质谱(HR-ESI-MS)和紫外光谱,并将结果与真实标准进行比较,我们能够识别杀念菌素大环内酯。杀念珠菌素大环内酯对Escovopsis具有高度活性,但不会显著影响共生真菌的生长。分析的3种切叶蚁中的每一种的微生物分离株中至少有一种产生杀念珠菌素大环内酯。这表明杀念菌素在保护切叶蚁的真菌花园免受病原真菌侵害方面起着重要作用。
Leaf-cutting ants such as Acromyrmex octospinosus live in obligate symbiosis with fungi of the genus Leucoagaricus, which they grow with harvested leaf material. The symbiotic fungi, in turn, serve as a major food source for the ants. This mutualistic relation is disturbed by the specialized pathogenic fungus Escovopsis sp., which can overcome Leucoagaricus sp. and thus destroy the ant colony. Microbial symbionts of leaf-cutting ants have been suggested to protect the fungus garden against Escovopsis by producing antifungal compounds [Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-704.]. To date, however, the chemical nature of these compounds has remained elusive. We characterized 19 leaf-cutting ant-associated microorganisms (5 Pseudonocardia, 1 Dermacoccus, and 13 Streptomyces) from 3 Acromyrmex species, A. octospinosus, A. echinatior, and A. volcanus, using 16S-rDNA analysis. Because the strain Streptomyces sp. Ao10 proved highly active against the pathogen Escovopsis, we identified the molecular basis of its antifungal activity. Using bioassay-guided fractionation, high-resolution electrospray mass spectrometry (HR-ESI-MS), and UV spectroscopy, and comparing the results with an authentic standard, we were able identify candicidin macrolides. Candicidin macrolides are highly active against Escovopsis but do not significantly affect the growth of the symbiotic fungus. At least one of the microbial isolates from each of the 3 leaf-cutting ant species analyzed produced candicidin macrolides. This suggests that candicidins play an important role in protecting the fungus gardens of leaf-cutting ants against pathogenic fungi.