Lichen-forming fungi are known to produce a large number of secondary metabolites. Some metabolites are deposited in the cortical layer of the lichen thallus where they exert important ecological functions, such as UV filtering. The fact that closely related lineages of lichen-forming fungi can differ in cortical chemistry suggests that natural product biosynthesis in lichens can evolve independent from phylogenetic constraints. Usnic acid is one of the major cortical pigments in lichens. Here we used a comparative genomic approach on 46 lichen-forming fungal species of the Lecanoromycetes to elucidate the biosynthetic gene content and evolution of the gene cluster putatively responsible for the biosynthesis of usnic acid. Whole genome sequences were gathered from taxa belonging to different orders and families of Lecanoromycetes, where Parmeliaceae is the most well-represented taxon, and analyzed with a variety of genomic tools. The highest number of biosynthetic gene clusters was found in Evernia prunastri, Pannoparmelia angustata and Parmotrema austrosinense, respectively and lowest in Canoparmelia nairobiensis, Bulbothrix sensibilis and Hypotrachyna scytodes. We found that all studied species producing usnic acid contain the putative usnic acid biosynthetic gene cluster, whereas the cluster was absent in all genomes of species lacking usnic acid. The absence of the gene cluster was supported by an additional unsuccessful search for ß-ketoacylsynthase, the most conserved domain of the gene cluster, in the genomes of species lacking usnic acid. The domain architecture of this PKS cluster - homologous to the already known usnic acid PKS cluster (MPAS) and CYT450 (MPAO) - varies within the studied species, whereas the gene arrangement is highly similar in closely related taxa. We hypothesize that the ancestor of these lichen-forming fungi contained the putative usnic acid producing PKS cluster and that the gene cluster was lost repeatedly during the evolution of these groups. Our study provides insight into the genomic adaptations to the evolutionary success of these lichen forming fungal species and sets a baseline for further exploration of biosynthetic gene content and its evolutionary significance.

中文翻译：

---

生物合成基因簇的全基因组分析揭示了与地衣形成真菌中松萝酸缺失相关的基因丢失

已知形成地衣的真菌会产生大量次生代谢物。一些代谢物沉积在地衣叶体的皮质层中，在那里它们发挥重要的生态功能，例如过滤紫外线。形成地衣的真菌的密切相关谱系在皮质化学上可能不同这一事实表明，地衣中的天然产物生物合成可以独立于系统发育限制而进化。松萝酸是地衣中主要的皮质色素之一。在这里，我们对 Lecanoromycetes 的 46 种形成地衣的真菌物种使用了比较基因组方法，以阐明假定负责松萝酸生物合成的基因簇的生物合成基因含量和进化。从属于不同目和家族的 Lecanoromycetes 的分类群中收集全基因组序列，其中 Parmeliaceae 是代表性最强的分类群，并使用各种基因组工具进行分析。生物合成基因簇数量最多的是Evernia prunastri、Pannoparmelia angustata和Parmotrema austrosinense分别在Canoparmelia nairobiensis、Bulbothrix sensibilis和Hypotrachyna scytodes 中最低。我们发现所有研究的产生松萝酸的物种都包含假定的松萝酸生物合成基因簇，而在所有缺乏松萝酸的物种的基因组中都不存在该簇。在缺乏松萝酸的物种的基因组中，对 ß-酮酰基合成酶（基因簇中最保守的结构域）的额外搜索失败支持了基因簇的缺失。此 PKS 集群的域架构 - 与已知的松香酸 PKS 集群（MPAS）同源) 和 CYT450 ( MPAO ) - 在研究的物种内变化，而基因排列在密切相关的分类群中高度相似。我们假设这些形成地衣的真菌的祖先包含推定的产生松萝酸的 PKS 簇，并且在这些群体的进化过程中基因簇反复丢失。我们的研究提供了对这些地衣形成真菌物种进化成功的基因组适应性的洞察，并为进一步探索生物合成基因含量及其进化意义奠定了基线。