Gonçalves Carla, Harrison Marie-Claire, Steenwyk Jacob L, Opulente Dana A, LaBella Abigail L, Wolters John F, Zhou Xiaofan, Shen Xing-Xing, Groenewald Marizeth, Hittinger Chris Todd, Rokas Antonis
Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.
bioRxiv. 2023 Sep 17:2023.09.14.557833. doi: 10.1101/2023.09.14.557833.
Many distantly related organisms have convergently evolved traits and lifestyles that enable them to live in similar ecological environments. However, the extent of phenotypic convergence evolving through the same or distinct genetic trajectories remains an open question. Here, we leverage a comprehensive dataset of genomic and phenotypic data from 1,049 yeast species in the subphylum Saccharomycotina (Kingdom Fungi, Phylum Ascomycota) to explore signatures of convergent evolution in cactophilic yeasts, ecological specialists associated with cacti. We inferred that the ecological association of yeasts with cacti arose independently ~17 times. Using machine-learning, we further found that cactophily can be predicted with 76% accuracy from functional genomic and phenotypic data. The most informative feature for predicting cactophily was thermotolerance, which is likely associated with duplication and altered evolutionary rates of genes impacting the cell envelope in several cactophilic lineages. We also identified horizontal gene transfer and duplication events of plant cell wall-degrading enzymes in distantly related cactophilic clades, suggesting that putatively adaptive traits evolved through disparate molecular mechanisms. Remarkably, multiple cactophilic lineages and their close relatives are emerging human opportunistic pathogens, suggesting that the cactophilic lifestyle-and perhaps more generally lifestyles favoring thermotolerance-may preadapt yeasts to cause human disease. This work underscores the potential of a multifaceted approach involving high throughput genomic and phenotypic data to shed light onto ecological adaptation and highlights how convergent evolution to wild environments could facilitate the transition to human pathogenicity.
许多亲缘关系较远的生物已经趋同进化出了使它们能够生活在相似生态环境中的特征和生活方式。然而，通过相同或不同遗传轨迹进化的表型趋同程度仍然是一个悬而未决的问题。在这里，我们利用来自子囊菌门酵母亚门1049种酵母的基因组和表型数据的综合数据集，来探索与仙人掌相关的生态专家——嗜仙人掌酵母中的趋同进化特征。我们推断酵母与仙人掌的生态关联独立出现了约17次。通过机器学习，我们进一步发现，根据功能基因组和表型数据可以以76%的准确率预测嗜仙人掌性。预测嗜仙人掌性最具信息性的特征是耐热性，这可能与几个嗜仙人掌谱系中影响细胞膜的基因的复制和进化速率改变有关。我们还在远缘的嗜仙人掌类群中鉴定出了植物细胞壁降解酶的水平基因转移和复制事件，这表明假定的适应性特征是通过不同的分子机制进化而来的。值得注意的是，多个嗜仙人掌谱系及其近亲正在成为人类机会性病原体，这表明嗜仙人掌生活方式——也许更普遍地说，有利于耐热性的生活方式——可能使酵母预先适应引起人类疾病。这项工作强调了一种涉及高通量基因组和表型数据的多方面方法在揭示生态适应方面的潜力，并突出了向野生环境的趋同进化如何促进向人类致病性的转变。
