Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
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DOI：
10.1128/mbio.02146-20
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发表时间：
2020-09-01
期刊：
影响因子：
6.4
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.;Khadempour, Lily;Currie, Cameron R.
食草动物必须克服各种植物防御，包括应对植物次生化合物（PSC）。为了帮助解毒这些防御性化学物质，已知几种食草昆虫体内含有具有降解PSC代谢能力的肠道微生物群。切叶蚁是多面手食草动物，从专门的真菌花园中获取食物，这些真菌花园充当外部消化系统，并降解蚂蚁觅食的各种植物。有体外证据表明，某些PSC伤害Leucoagaricus gongylophorus，切叶蚁的真菌品种，这表明真菌花园内存在的变形杆菌属占主导地位的细菌群落的作用。在这项研究中，我们调查了共生细菌存在于切叶蚁真菌花园内降解PSC的能力。我们培养真菌花园细菌，测序的42个菌株的基因组，并确定参与PSC降解的基因，包括编码细胞色素P450酶的基因和香叶醇，cumate，肉桂酸，和α-蒎烯/柠檬烯降解途径的基因。使用元转录组学分析，我们发现这些降解基因中的一些在原位表达。大多数细菌分离株在PSC的存在下不受阻碍地生长，并且使用气相色谱-质谱法（GC-MS），我们确定来自芽孢杆菌属、伯克霍尔德氏菌属、肠杆菌属、克雷伯氏菌属和假单胞菌属的分离株降解α-蒎烯、β-香芹烯或芳樟醇。使用顶空取样器，我们表明，亚菌落的真菌花园减少α-蒎烯和芳樟醇超过36小时的时间，而L。单独的gongylophorus菌株仅还原芳樟醇。总的来说，我们的研究结果表明，真菌花园中的细菌群落在减轻PSC对切叶蚁system.IMPORTANCE切叶蚁的影响中发挥着关键作用，切叶蚁是占主导地位的新热带区食草动物，能够从广泛的植物基质中获得能量。切叶蚁的成功很大程度上归功于它们的外部肠道，由关键的微生物共生体组成，特别是真菌互利共生菌L。gongylophorus和一致的细菌群落。已知这两种共生体在从植物材料中提取能量方面具有关键作用，但对它们在植物次生化合物解毒中的作用知之甚少。在这项研究中，我们评估了与切叶蚁真菌花园相关的细菌群落是否可以降解有害的植物化学物质。我们将切叶蚁花园中的植物次生化合物解毒确定为一个依赖于细菌群落和L.具孔的我们的研究结果表明，真菌花园及其相关的微生物群落影响蚂蚁的通才觅食能力，强调了微生物共生体在植物基质适合食草动物的重要性。
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 alpha-pinene/limonene degradation pathways. Using meta-transcriptomic 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 alpha-pinene, beta-caryophyllene, or linalool. Using a headspace sampler, we show that sub-colonies of fungus gardens reduced alpha-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.IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.