Ecological diversity in fungi is largely defined by metabolic traits, including the ability to produce secondary or “specialized” metabolites (SMs) that mediate interactions with other organisms. Fungal SM pathways are frequently encoded in biosynthetic gene clusters (BGCs), which facilitate the identification and characterization of metabolic pathways. Variation in BGC composition reflects the diversity of their SM products. Recent studies have documented surprising diversity of BGC repertoires among isolates of the same fungal species, yet little is known about how this population-level variation is inherited across macroevolutionary timescales. Here, we applied a novel linkage-based algorithm to reveal previously unexplored dimensions of diversity in BGC composition, distribution, and repertoire across 101 species of Dothideomycetes, which are considered the most phylogenetically diverse class of fungi and known to produce many SMs. We predicted both complementary and overlapping sets of clustered genes compared with existing methods and identified novel gene pairs that associate with known secondary metabolite genes. We found that variation among sets of BGCs in individual genomes is due to nonoverlapping BGC combinations and that several BGCs have biased ecological distributions, consistent with niche-specific selection. We observed that total BGC diversity scales linearly with increasing repertoire size, suggesting that secondary metabolites have little structural redundancy in individual fungi. We project that there is substantial unsampled BGC diversity across specific families of Dothideomycetes, which will provide a roadmap for future sampling efforts. Our approach and findings lend new insight into how BGC diversity is generated and maintained across an entire fungal taxonomic class.

中文翻译：

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代谢结构最大程度地提高了真菌的生物合成多样性。

真菌的生态多样性在很大程度上由代谢性状定义，包括产生介导与其他生物体相互作用的次生或“特殊”代谢物（SM）的能力。真菌SM途径经常在生物合成基因簇（BGC）中编码，这有助于代谢途径的鉴定和表征。BGC成分的变化反映了他们SM产品的多样性。最近的研究表明，在同一真菌物种的分离物中，BGC组成成分具有令人惊讶的多样性，但对于这种种群水平变异是如何在宏观进化时间尺度上遗传的却知之甚少。在这里，我们应用了一种新颖的基于链接的算法，以揭示BGC的101种物种中BGC组成，分布和库中多样性的先前未曾探索的维度。十二指肠菌，被认为是种类最丰富的真菌，已知会产生许多SM。与现有方法相比，我们预测了群集基因的互补集和重叠集，并确定了与已知次级代谢产物基因相关的新型基因对。我们发现，单个基因组中BGC的集合之间的差异是由于不重叠的BGC组合所致，并且一些BGC的生态分布有偏差，这与利基特定的选择一致。我们观察到，总BGC多样性随库大小的增加呈线性比例，这表明次生代谢物在单个真菌中几乎没有结构冗余。我们预测，在特定的丝裂菌家族中，存在大量未采样的BGC多样性，这将为将来的采样工作提供一个路线图。我们的方法和发现为在整个真菌分类学类别中如何产生和维持BGC多样性提供了新的见解。