Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, School of Life Science, South China Normal University, Guangzhou, 510631, China.
School of Marine and Fisheries, Guangdong Eco-engineering Polytechnic, Guangzhou, 510320, China.
BMC Biol. 2024 Aug 13;22(1):170. doi: 10.1186/s12915-024-01969-z.
Tubulins are major components of the eukaryotic cytoskeletons that are crucial in many cellular processes. Ciliated protists comprise one of the oldest eukaryotic lineages possessing cilia over their cell surface and assembling many diverse microtubular structures. As such, ciliates are excellent model organisms to clarify the origin and evolution of tubulins in the early stages of eukaryote evolution. Nonetheless, the evolutionary history of the tubulin subfamilies within and among ciliate classes is unclear.
We analyzed the evolutionary pattern of ciliate tubulin gene family based on genomes/transcriptomes of 60 species covering 10 ciliate classes. Results showed: (1) Six tubulin subfamilies (α_Tub, β_Tub, γ_Tub, δ_Tub, ε_Tub, and ζ_Tub) originated from the last eukaryotic common ancestor (LECA) were observed within ciliates. Among them, α_Tub, β_Tub, and γ_Tub were present in all ciliate species, while δ_Tub, ε_Tub, and ζ_Tub might be independently lost in some species. (2) The evolutionary history of the tubulin subfamilies varied. Evolutionary history of ciliate γ_Tub, δ_Tub, ε_Tub, and ζ_Tub showed a certain degree of consistency with the phylogeny of species after the divergence of ciliate classes, while the evolutionary history of ciliate α_Tub and β_Tub varied among different classes. (3) Ciliate α- and β-tubulin isoforms could be classified into an "ancestral group" present in LECA and a "divergent group" containing only ciliate sequences. Alveolata-specific expansion events probably occurred within the "ancestral group" of α_Tub and β_Tub. The "divergent group" might be important for ciliate morphological differentiation and wide environmental adaptability. (4) Expansion events of the tubulin gene family appeared to be consistent with whole genome duplication (WGD) events in some degree. More Paramecium-specific tubulin expansions were detected than Tetrahymena-specific ones. Compared to other Paramecium species, the Paramecium aurelia complex underwent a more recent WGD which might have experienced more tubulin expansion events.
Evolutionary history among different tubulin gene subfamilies seemed to vary within ciliated protists. And the complex evolutionary patterns of tubulins among different ciliate classes might drive functional diversification. Our investigation provided meaningful information for understanding the evolution of tubulin gene family in the early stages of eukaryote evolution.
微管蛋白是真核细胞骨架的主要成分，在许多细胞过程中至关重要。纤毛原生动物是拥有细胞表面纤毛并组装许多不同微管结构的最古老的真核生物谱系之一。因此，纤毛原生动物是阐明真核生物进化早期微管蛋白起源和进化的极好模型生物。尽管如此，纤毛原生动物类内和类间的微管蛋白亚家族的进化历史尚不清楚。
我们基于涵盖 10 个纤毛类的 60 个物种的基因组/转录组，分析了纤毛原生动物微管蛋白基因家族的进化模式。结果表明：（1）在纤毛原生动物中观察到 6 个微管蛋白亚家族（α_Tub、β_Tub、γ_Tub、δ_Tub、ε_Tub 和 ζ_Tub）起源于最后的真核生物共同祖先（LECA）。其中，α_Tub、β_Tub 和 γ_Tub 存在于所有纤毛原生动物物种中，而 δ_Tub、ε_Tub 和 ζ_Tub 可能在某些物种中独立丢失。（2）微管蛋白亚家族的进化历史各不相同。纤毛原生动物γ_Tub、δ_Tub、ε_Tub 和 ζ_Tub 的进化历史与纤毛类分化后的物种系统发育有一定程度的一致性，而纤毛原生动物α_Tub 和 β_Tub 的进化历史在不同类群中有所不同。（3）纤毛原生动物的α-和β-微管蛋白同工型可分为存在于 LECA 的“祖先进化群”和仅包含纤毛序列的“分化进化群”。α_Tub 和 β_Tub 的“祖先进化群”中可能发生了顶复门特有的扩张事件。“分化进化群”可能对纤毛原生动物的形态分化和广泛的环境适应性很重要。（4）在某种程度上，微管蛋白基因家族的扩张事件似乎与全基因组复制（WGD）事件一致。在 Paramecium 中检测到的特定 tubulin 扩张事件比 Tetrahymena 中检测到的更多。与其他 Paramecium 物种相比，Paramecium aurelia 复合体经历了更近的 WGD，可能经历了更多的 tubulin 扩张事件。
不同微管蛋白基因亚家族之间的进化历史在纤毛原生动物中似乎有所不同。不同纤毛类之间复杂的微管蛋白进化模式可能推动了功能多样化。我们的研究为理解真核生物进化早期微管蛋白基因家族的进化提供了有意义的信息。
