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Enrichment and Broad Representation of Plant Biomass-Degrading Enzymes in the Specialized Hyphal Swellings of Leucoagaricus gongylophorus the Fungal Symbiont of Leaf-Cutter Ants

机译:切叶蚁的真菌共生亮斑龙舌菌专门菌丝肿胀中植物生物量降解酶的富集和广泛表达

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摘要

Leaf-cutter ants are prolific and conspicuous constituents of Neotropical ecosystems that derive energy from specialized fungus gardens they cultivate using prodigious amounts of foliar biomass. The basidiomycetous cultivar of the ants, Leucoagaricus gongylophorus, produces specialized hyphal swellings called gongylidia that serve as the primary food source of ant colonies. Gongylidia also contain plant biomass-degrading enzymes that become concentrated in ant digestive tracts and are deposited within fecal droplets onto fresh foliar material as ants incorporate it into the fungus garden. Although the enzymes concentrated by L. gongylophorus within gongylidia are thought to be critical to the initial degradation of plant biomass, only a few enzymes present in these hyphal swellings have been identified. Here we use proteomic methods to identify proteins present in the gongylidia of three Atta cephalotes colonies. Our results demonstrate that a diverse but consistent set of enzymes is present in gongylidia, including numerous plant biomass-degrading enzymes likely involved in the degradation of polysaccharides, plant toxins, and proteins. Overall, gongylidia contained over three quarters of all biomass-degrading enzymes identified in the L. gongylophorus genome, demonstrating that the majority of the enzymes produced by this fungus for biomass breakdown are ingested by the ants. We also identify a set of 40 of these enzymes enriched in gongylidia compared to whole fungus garden samples, suggesting that certain enzymes may be particularly important in the initial degradation of foliar material. Our work sheds light on the complex interplay between leaf-cutter ants and their fungal symbiont that allows for the host insects to occupy an herbivorous niche by indirectly deriving energy from plant biomass.
机译:切叶蚁是新热带生态系统中多产的,明显的组成部分,它们是利用大量叶面生物量从他们种植的专门真菌园中获取能量的。蚂蚁的担子菌变种Leucoagaricus gongylophorus产生称为gongylidia的专门菌丝肿胀,作为蚂蚁菌落的主要食物来源。弓形虫还含有植物生物质降解酶,这些酶会在蚂蚁的消化道中浓缩,并在蚂蚁将其掺入真菌园后,在粪便液滴中沉积到新鲜的叶面材料上。尽管人们认为,由冈蝇中的冈蝇乳杆菌浓缩的酶对于植物生物量的初始降解至关重要,但仅鉴定出存在于这些菌丝肿胀中的几种酶。在这里,我们使用蛋白质组学方法来鉴定存在于三个Atta头足类菌落的gongylidia中的蛋白质。我们的结果表明,在淋球菌中存在多种多样但一致的酶,包括可能与多糖,植物毒素和蛋白质降解有关的多种植物生物质降解酶。总体而言,gongylidia包含在L. gongylophorus基因组中鉴定的所有生物量降解酶的四分之三,这表明该真菌为生物量分解而产生的大多数酶被蚂蚁摄取。与完整的真菌园样品相比,我们还鉴定了一组富含40种这种植物中的酶,这表明某些酶可能在叶材料的初始降解中特别重要。我们的工作揭示了切叶蚁与其真菌共生体之间复杂的相互作用,使宿主昆虫可以通过间接从植物生物质中获取能量来占据草食性生态位。

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