Torruella Guifré, Galindo Luis Javier, Moreira David, López-García Purificación
Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, AgroParisTech, 91190 Gif-sur-Yvette, France; Institut de Biologia Evolutiva, UPF-CSIC, Barcelona, Catalonia 08003, Spain.
Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, AgroParisTech, 91190 Gif-sur-Yvette, France; Institute of Water Research, University of Granada, 18071 Granada, Spain; Department of Ecology, University of Granada, Campus Fuentenueva, 18071 Granada, Spain.
Curr Biol. 2025 Jan 6;35(1):198-207.e4. doi: 10.1016/j.cub.2024.10.075. Epub 2024 Dec 5.
Eukaryotes evolved from prokaryotic predecessors in the early Proterozoic and radiated from their already complex last common ancestor, diversifying into several supergroups with unresolved deep evolutionary connections. They evolved extremely diverse lifestyles, playing crucial roles in the carbon cycle. Heterotrophic flagellates are arguably the most diverse eukaryotes and often occupy basal positions in phylogenetic trees. However, many of them remain undersampled and/or incertae sedis. Progressive improvement of phylogenomic methods and a wider protist sampling have reshaped and consolidated major clades in the eukaryotic tree. This is illustrated by the Opimoda, one of the largest eukaryotic supergroups (Amoebozoa, Ancyromonadida, Apusomonadida, Breviatea, CRuMs [Collodictyon-Rigifila-Mantamonas], Malawimonadida, and Opisthokonta-including animals and fungi). However, their deepest evolutionary relationships still remain uncertain. Here, we sequenced transcriptomes of poorly studied flagellates (14 apusomonads, 7 ancyromonads, and 1 cultured Mediterranean strain of Meteora sporadica) and conducted comprehensive phylogenomics analyses with an expanded taxon sampling of early-branching protists. Our findings support the monophyly of Opimoda, with CRuMs being sister to the Amorphea (amoebozoans, breviates, apusomonads, and opisthokonts) and ancyromonads and malawimonads forming a moderately supported clade. By mapping key complex phenotypic traits onto this phylogenetic framework, we infer an opimodan biflagellate ancestor with an excavate-like feeding groove, which ancyromonads subsequently lost. Although breviates and apusomonads retained the ancestral biflagellate state, some early-diverging Amorphea lost one or both flagella, facilitating the evolution of amoeboid morphologies, novel feeding modes, and palintomic cell division resulting in multinucleated cells. These innovations likely facilitated the subsequent evolution of fungal and metazoan multicellularity.
真核生物在元古宙早期从原核生物前身进化而来，并从其已经复杂的最后共同祖先辐射演化，分化成几个具有未解决的深层进化联系的超群。它们进化出极其多样的生活方式，在碳循环中发挥着关键作用。异养鞭毛虫可以说是最多样化的真核生物，并且在系统发育树中常常占据基部位置。然而，它们中的许多仍然采样不足和/或分类地位不确定。系统发育基因组学方法的不断改进和更广泛的原生生物采样重塑并巩固了真核生物树中的主要分支。以Opimoda为例，它是最大的真核生物超群之一（变形虫门、锚定单胞虫纲、无尾鞭毛虫纲、短膜虫纲、CRuMs [盘状变形虫-刚硬变形虫-曼氏变形虫]、马拉维单胞虫纲和后鞭毛生物超群 - 包括动物和真菌）。然而，它们最深层的进化关系仍然不确定。在这里，我们对研究较少的鞭毛虫（14种无尾鞭毛虫、7种锚定单胞虫和1种培养的地中海散斑流星虫菌株）的转录组进行了测序，并对早期分支原生生物进行了扩大分类群采样的全面系统发育基因组学分析。我们的研究结果支持Opimoda的单系性，CRuMs是变形虫总门（变形虫门、短膜虫纲、无尾鞭毛虫纲和后鞭毛生物超群）的姐妹群，而锚定单胞虫和马拉维单胞虫形成一个有一定支持度的分支。通过将关键的复杂表型特征映射到这个系统发育框架上，我们推断出一个具有类似盘状变形虫进食沟的Opimoda双鞭毛祖先，锚定单胞虫随后失去了这种进食沟。虽然短膜虫纲和无尾鞭毛虫纲保留了祖先的双鞭毛状态，但一些早期分化的变形虫总门失去了一根或两根鞭毛，促进了变形虫形态、新的进食模式和导致多核细胞的反复分裂的进化。这些创新可能促进了随后真菌和后生动物多细胞性的进化。
