Burkholderia from Fungus Gardens of Fungus-Growing Ants Produces Antifungals That Inhibit the Specialized Parasite Escovopsis
Burkholderia from Fungus Gardens of Fungus-Growing Ants Produces Antifungals That Inhibit the Specialized Parasite Escovopsis
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DOI：
10.1128/aem.00178-21
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发表时间：
2021-07-01
影响因子：
4.4
通讯作者：
Currie, Cameron R.
中科院分区：
文献类型：
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作者：
Francoeur, Charlotte B.;May, Daniel S.;Currie, Cameron R.
在与动物相关的微生物组中，特定微生物分类群的功能作用通常是不明确的。在这里，我们使用真菌生长的蚂蚁系统，一个微生物共生模型，来确定存在于蚂蚁真菌花园中的关键细菌分类群的潜在防御作用。真菌花园是蚂蚁的外部消化系统，共生真菌白松菇属（Leucoagaricus）将植物基质转化为蚂蚁的能量。真菌园是寄生真菌属的宿主。在这里，我们研究了伯克氏菌的潜在作用，发生在蚂蚁真菌花园抑制Escovopsis。我们从取样的52个菌落中的50%中分离出了伯克霍尔德菌属和副伯克霍尔德菌属的细菌成员，表明伯克霍尔德菌科的成员是各种真菌生长蚂蚁属的真菌花园中的常见居民。通过抗菌抑制生物测定，我们发现32株分离株中有28株对至少一株Escovopsis菌株有抑制作用，抑制区大于1 cm。真菌花园相关burkholderaceae的基因组评估表明，具有强抑制作用的分离株均属于burkholderia属，并且含有生物合成基因簇，编码产生两种抗真菌物质：burkholdine1213和pyrrolnitrin。培养分离物的有机提取物证实，这些化合物具有抑制Escovopsis的抗真菌活性，但在相同浓度下，对Leucoagaricus不起作用。总的来说，这些新发现结合先前的证据表明，真菌花园微生物组的成员在维持真菌生长蚁群的健康和功能方面发挥着重要作用。许多生物与微生物合作以保护自己免受寄生虫和病原体的侵害。真菌生长的蚂蚁必须保护为蚂蚁提供食物的共生真菌白衣真菌免受一种特殊的真菌寄生虫的侵害。蚂蚁采取多种方法，包括清除真菌花园的杂草以去除Escovopsis孢子，以及庇护伪心菌，这种细菌可以产生抑制Escovopsis的抗真菌剂。此外，真菌花园中常见的一种细菌，伯克霍尔德氏菌，已知会产生抑制Escovopsis spp的次级代谢物。在本研究中，我们从真菌生长的蚂蚁中分离出伯克霍尔德氏菌，评估了分离物对Escovopsis spp的抑制能力，并鉴定了两种负责抑制的化合物。我们的研究结果表明，伯克霍尔德氏菌经常在真菌花园中发现，这增加了真菌生长蚂蚁系统中抑制特殊寄生虫Escovopsis生长的另一种可能机制。
Within animal-associated microbiomes, the functional roles of specific microbial taxa are often uncharacterized. Here, we use the fungus-growing ant system, a model for microbial symbiosis, to determine the potential defensive roles of key bacterial taxa present in the ants' fungus gardens. Fungus gardens serve as an external digestive system for the ants, with mutualistic fungi in the genus Leucoagaricus converting the plant substrate into energy for the ants. The fungus garden is host to specialized parasitic fungi in the genus Escovopsis. Here, we examine the potential role of Burkholderia spp. that occur within ant fungus gardens in inhibiting Escovopsis. We isolated members of the bacterial genera Burkholderia and Paraburkholderia from 50% of the 52 colonies sampled, indicating that members of the family Burkholderiaceae are common inhabitants in the fungus gardens of a diverse range of fungus-growing ant genera. Using antimicrobial inhibition bioassays, we found that 28 out of 32 isolates inhibited at least one Escovopsis strain with a zone of inhibition greater than 1 cm. Genomic assessment of fungus garden-associated Burkholderiaceae indicated that isolates with strong inhibition all belonged to the genus Burkhoideria and contained biosynthetic gene clusters that encoded the production of two antifungals: burkholdine1213 and pyrrolnitrin. Organic extracts of cultured isolates confirmed that these compounds are responsible for antifungal activities that inhibit Escovopsis but, at equivalent concentrations, not Leucoagaricus spp. Overall, these new findings, combined with previous evidence, suggest that members of the fungus garden microbiome play an important role in maintaining the health and function of fungus-growing ant colonies.IMPORTANCE Many organisms partner with microbes to defend themselves against parasites and pathogens. Fungus-growing ants must protect Leucoagaricus spp., the fungal mutualist that provides sustenance for the ants, from a specialized fungal parasite, Escovopsis. The ants take multiple approaches, including weeding their fungus gardens to remove Escovopsis spores, as well as harboring Pseudonocardia spp., bacteria that produce antifungals that inhibit Escovopsis. In addition, a genus of bacteria commonly found in fungus gardens, Burkholderia, is known to produce secondary metabolites that inhibit Escovopsis spp. In this study, we isolated Burkholderia spp. from fungus-growing ants, assessed the isolates' ability to inhibit Escovopsis spp., and identified two compounds responsible for inhibition. Our findings suggest that Burkholderia spp. are often found in fungus gardens, adding another possible mechanism within the fungus-growing ant system to suppress the growth of the specialized parasite Escovopsis.