Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system.

中文翻译：

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细菌有助于通才草食动物系统中的植物次生化合物降解。

草食动物必须克服各种植物防御，包括应对植物次生化合物 (PSC)。为了帮助这些防御性化学物质解毒，已知几种昆虫食草动物体内含有具有降解 PSC 的代谢能力的肠道微生物群。切叶蚁是多面性食草动物，从专门的真菌园中获取食物，这些真菌园充当外部消化系统，降解蚂蚁觅食的各种植物。有体外证据表明，某些 PSC 会伤害切叶蚁的真菌栽培种Leucoagaricus gogylophorus，这表明变形杆菌的作用-存在于真菌园内的主要细菌群落。在这项研究中，我们研究了切叶蚁真菌园中存在的共生细菌降解 PSC 的能力。我们培养了真菌花园细菌，对 42 个分离株的基因组进行了测序，并鉴定了参与 PSC 降解的基因，包括编码细胞色素 P450 酶的基因和香叶醇、枯木酸盐、肉桂酸盐和 α-蒎烯/柠檬烯降解途径中的基因。使用元转录组学分析，我们发现其中一些降解基因是原位表达的。大多数细菌分离物在 PSC 存在下生长不受阻碍，并且使用气相色谱-质谱 (GC-MS)，我们确定从芽孢杆菌属、伯克霍尔德氏菌属、肠杆菌属、克雷伯氏菌属和假单胞菌属降解 α-蒎烯、β-石竹烯或芳樟醇。使用顶空采样器，我们发现真菌园的亚菌落在 36 小时内减少了 α-蒎烯和芳樟醇，而单独的L. gongylophorus菌株仅减少了芳樟醇。总体而言，我们的研究结果表明，真菌园中的细菌群落在减轻 PSC 对切叶蚁系统的影响方面发挥着关键作用。