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The MSDIN family in amanitin-producing mushrooms and evolution of the prolyl oligopeptidase genes.
IMA Fungus ( IF 5.2 ) Pub Date : 2019-01-10 , DOI: 10.5598/imafungus.2018.09.02.01
Hong Luo 1 , Qing Cai 1 , Yunjiao Lüli 1, 2 , Xuan Li 3 , Rohita Sinha 4 , Heather E Hallen-Adams 5 , Zhu L Yang 1
Affiliation  

The biosynthetic pathway for amanitins and related cyclic peptides in deadly Amanita (Amanitaceae) mushrooms represents the first known ribosomal cyclic peptide pathway in the Fungi. Amanitins are found outside of the genus in distantly related agarics Galerina (Strophariaceae) and Lepiota (Agaricaceae). A long-standing question in the field persists: why is this pathway present in these phylogenetically disjunct agarics? Two deadly mushrooms, A. pallidorosea and A. subjunquillea, were deep sequenced, and sequences of biosynthetic genes encoding MSDINs (cyclic peptide precursor) and prolyl oligopeptidases (POPA and POPB) were obtained. The two Amanita species yielded 29 and 18 MSDINs, respectively. In addition, two MSDIN sequences were cloned from L. brunneoincarnata basidiomes. The toxin MSDIN genes encoding amatoxins or phallotoxins from the three genera were compared, and a phylogenetic tree constructed. Prolyl oligopeptidase B (POPB), a key enzyme in the biosynthetic pathway, was used in phylogenetic reconstruction to infer the evolutionary history of the genes. Phylogenies of POPB and POPA based on both coding and amino acid sequences showed very different results: while POPA genes clearly reflected the phylogeny of the host species, POPB did not; strikingly, it formed a well-supported monophyletic clade, despite that the species belong to different genera in disjunct families. POPA, a known house-keeping gene, was shown to be restricted in a branch containing only Amanita species and the phylogeny resembled that of those Amanita species. Phylogenetic analyses of MSDIN and POPB genes showed tight coordination and disjunct distribution. A POPB gene tree was compared with a corresponding species tree, and distances and substitution rates were compared. The result suggested POPB genes have significant smaller distances and rates than the house-keeping rpb2, discounting massive gene loss. Under this assumption, the incongruency between the gene tree and species tree was shown with strong support. Additionally, k-mer analyses consistently cluster Galerina and Amanita POPB genes, while Lepiota POPB is distinct. Our result suggests that horizontal gene transfer (HGT), at least between Amanita and Galerina, was involved in the acquisition of POPB genes, which may shed light on the evolution of the α-amanitin biosynthetic pathway.

中文翻译:

产生金黄色素的蘑菇中的MSDIN家族和脯氨酰寡肽酶基因的进化。

致命的鹅膏菌(Amanitaceae)蘑菇中的鹅膏菌素和相关环肽的生物合成途径代表了真菌中第一个已知的核糖体环肽途径。在距离较近的木耳Galerina(Strophariaceae)和Lepiota(Agaricaceae)的属外,发现了天青素。该领域中一个长期存在的问题仍然存在:为什么这些系统发育分离的琼脂菌中存在这种途径?对两个致命的蘑菇,A。pallidorosea和A. subjunquillea,进行了深度测序,并获得了编码MSDINs(环肽前体)和脯氨酰寡肽酶(POPA和POPB)的生物合成基因序列。两种鹅膏菌物种分别产生29和18个MSDIN。另外,从布氏乳杆菌(L. brunneoincarnata)basidiomes克隆了两个MSDIN序列。比较了来自这三个属的编码毒素的MSDIN基因或鬼笔毒素,并构建了系统进化树。脯氨酰寡肽酶B(POPB)是生物合成途径中的关键酶,被用于系统发育重建中以推断基因的进化历史。基于编码和氨基酸序列的POPB和POPA的系统发育显示出截然不同的结果:虽然POPA基因清楚地反映了宿主物种的系统发育,但POPB没有。令人惊讶的是,尽管该物种属于分离家族的不同属,却形成了一个支撑良好的单系进化枝。POPA是一种已知的持家基因,显示仅在一个鹅膏菌属物种的分支中受到限制,其系统发育类似于那些鹅膏菌属物种。MSDIN和POPB基因的系统发育分析显示紧密的协调和分散的分布。将POPB基因树与相应的树进行比较,并比较距离和替代率。结果表明,POPB基因的距离和发生率比管家rpb2小得多,大大降低了基因丢失的可能性。在此假设下,基因树与物种树之间的不一致表现出了强有力的支持。此外,k-mer分析一致地聚类了Galerina和Amanita POPB基因,而Lepiota POPB是截然不同的。我们的结果表明,至少在鹅膏菌和Galerina之间进行水平基因转移(HGT)参与了POPB基因的获取,这可能为α-amanitin生物合成途径的进化提供了启示。将POPB基因树与相应的树进行比较,并比较距离和替代率。结果表明,POPB基因的距离和发生率比管家rpb2小得多,大大降低了基因丢失的可能性。在此假设下,基因树与物种树之间的不一致表现出了强有力的支持。此外,k-mer分析一致地聚类了Galerina和Amanita POPB基因,而Lepiota POPB是截然不同的。我们的结果表明,至少在鹅膏菌和Galerina之间进行水平基因转移(HGT)参与了POPB基因的获取,这可能为α-amanitin生物合成途径的进化提供了启示。将POPB基因树与相应的物种树进行比较,并比较距离和替代率。结果表明,POPB基因的距离和发生率比管家rpb2小得多,大大降低了基因丢失的可能性。在此假设下,基因树与物种树之间的不一致表现出了强有力的支持。此外,k-mer分析一致地聚类了Galerina和Amanita POPB基因,而Lepiota POPB是截然不同的。我们的结果表明,至少在鹅膏菌和Galerina之间进行水平基因转移(HGT)参与了POPB基因的获取,这可能为α-amanitin生物合成途径的进化提供了启示。结果表明,POPB基因的距离和发生率比管家rpb2小得多,大大降低了基因丢失的可能性。在此假设下,基因树与物种树之间的不一致表现出了强有力的支持。此外,k-mer分析一致地聚类了Galerina和Amanita POPB基因,而Lepiota POPB是截然不同的。我们的结果表明,至少在鹅膏菌和Galerina之间进行水平基因转移(HGT)参与了POPB基因的获取,这可能为α-amanitin生物合成途径的进化提供了启示。结果表明,POPB基因的距离和发生率比管家rpb2小得多,大大降低了基因丢失的可能性。在此假设下,基因树与物种树之间的不一致表现出了强有力的支持。此外,k-mer分析一致地聚类了Galerina和Amanita POPB基因,而Lepiota POPB是截然不同的。我们的结果表明,至少在鹅膏菌和Galerina之间进行水平基因转移(HGT)参与了POPB基因的获取,这可能为α-amanitin生物合成途径的进化提供了启示。
更新日期:2019-11-01
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