The genome of the basal agaricomycete Xanthophyllomyces dendrorhous provides insights into the organization of its acetyl-CoA derived pathways and the evolution of Agaricomycotina

Xanthophyllomyces dendrorhous is a basal agaricomycete with uncertain taxonomic placement, known for its unique ability to produce astaxanthin, a carotenoid with antioxidant properties. It was the aim of this study to elucidate the organization of its CoA-derived pathways and to use the genomic information of X. dendrorhous for a phylogenomic investigation of the Basidiomycota. The genome assembly of a haploid strain of Xanthophyllomyces dendrorhous revealed a genome of 19.50 Megabases with 6385 protein coding genes. Phylogenetic analyses were conducted including 48 fungal genomes. These revealed Ustilaginomycotina and Agaricomycotina as sister groups. In the latter a well-supported sister-group relationship of two major orders, Polyporales and Russulales, was inferred. Wallemia occupies a basal position within the Agaricomycotina and X. dendrorhous represent the basal lineage of the Tremellomycetes, highlighting that the typical tremelloid parenthesomes have either convergently evolved in Wallemia and the Tremellomycetes, or were lost in the Cystofilobasidiales lineage. A detailed characterization of the CoA-related pathways was done and all genes for fatty acid, sterol and carotenoid synthesis have been assigned. The current study provides some basic insights into the evolution of Agaricomycotina and ascertains that Wallemia with tremelloid parenthesomes is the most basal agaricomycotinous lineage and that Cystofilobasidiales without tremelloid parenthesomes are deeply rooted within Tremellomycetes, suggesting that parenthesomes at septal pores might be the core synapomorphy for the Agaricomycotina. The genome sequence of X. dendrorhous will extremely facilitate genetic pathway engineering for optimized astaxanthin or oxidative alcohol production.

Xanthophyllomyces dendrorhous（红发夫酵母）是一类分类地位尚未明确的基底伞菌纲（Agaricomycetes）物种，因其具备合成具有抗氧化活性的类胡萝卜素（carotenoid）虾青素（astaxanthin）的独特能力而广受关注。本研究旨在阐明其辅酶A（CoA）衍生代谢通路的组成架构，并利用红发夫酵母的基因组信息开展担子菌门（Basidiomycota）的系统基因组学（phylogenomic）研究。对一株红发夫酵母单倍体菌株（haploid strain）的基因组组装（genome assembly）结果显示，其基因组大小为19.50兆碱基，共包含6385个蛋白编码基因。本研究开展了涵盖48个真菌基因组的系统发育分析，结果显示黑粉菌亚门（Ustilaginomycotina）与伞菌亚门（Agaricomycotina）为姊妹群（sister groups）。在伞菌亚门这一支中，两个主要类群——多孔菌目（Polyporales）与红菇目（Russulales）之间被推断出具有高支持率的姊妹群关系。沃勒姆菌属（Wallemia）在伞菌亚门中处于基部演化位置，而红发夫酵母则代表银耳纲（Tremellomycetes）的基部谱系，这提示典型的银耳类桶孔覆垫（parenthesomes）要么在沃勒姆菌属与银耳纲中发生了趋同演化（convergently evolved），要么在囊膜酵母目（Cystofilobasidiales）的谱系中丢失。本研究对辅酶A相关代谢通路进行了详细表征，并完成了脂肪酸、固醇及类胡萝卜素合成相关全部基因的功能注释。本研究为伞菌亚门的演化提供了基础认知，并证实携带银耳类桶孔覆垫的沃勒姆菌属是最基部的伞菌亚门谱系，而缺乏该结构的囊膜酵母目则深嵌于银耳纲内部，这提示隔膜孔（septal pores）处的桶孔覆垫可能是伞菌亚门的核心共有衍征（synapomorphy）。红发夫酵母的基因组序列将极大促进用于优化虾青素合成或氧化型醇类生产的代谢通路工程（genetic pathway engineering）研究。