Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals.
Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals.
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DOI：
10.7554/elife.08904
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发表时间：
2015-10-14
期刊：
影响因子：
7.7
通讯作者：
Ruiz-Trillo I
中科院分区：
文献类型：
--
作者：
de Mendoza A;Suga H;Permanyer J;Irimia M;Ruiz-Trillo I
通过差异基因组调控的细胞类型特化是复杂多细胞性的标志。然而，目前还不清楚这个过程是如何从单细胞生物过渡到多细胞生物的。为了解决这个问题，我们研究了转录动力学的鱼孢子虫Creolimax fragrantissima，一个相对的动物，经历多核发育。我们发现，Creolimax利用动态调节的选择性剪接，长的基因间非编码RNA和共调节基因模块与动物多细胞在细胞类型特异性的方式。此外，我们的研究表明，三种最接近的动物亲戚（鱼孢子虫，丝状虫和choanoflagellates）的不同细胞类型是谱系特异性创新的产物。此外，对分泌组的蛋白质组学调查揭示了对真菌样生活方式的适应。总之，动物原生生物亲属中细胞类型的多样性及其复杂的基因组调控表明，动物最后的单细胞祖先已经能够详细说明细胞类型。DOI：http://dx.doi.org/10.7554/eLife.08904.001所有现存的动物都是单细胞祖先的后代，了解这些祖先如何成为第一个多细胞动物仍然是进化生物学领域的一个重大挑战。实现这一目标的早期突破是认识到，尽管它们大多是单细胞生物，但动物的近亲共享动物用于支持其多细胞生活方式的大部分基本基因工具包。这个共享的工具包还包括允许动物中的每种专门细胞类型（例如皮肤细胞或肝细胞）表达其履行特定作用所需的基因子集的基因。发现动物的单细胞亲属在其生命周期中如何调节这些和其他“多细胞相关”基因是理解动物如何成为多细胞的下一个关键步骤。Creolimax fragrantissima是一种单细胞动物。这种生物体生命周期的一个阶段涉及其细胞核（包含其遗传物质）多次复制，而细胞本身不分裂。在这个发育阶段之后，新的细胞形成，每个细胞都接受一个细胞核，并释放出来在环境中自由生活。描述了C. fragrantissima调节哪些基因在这两个非常不同的发育阶段表达，可以为多细胞动物如何进化以调节特定细胞类型的基因提供新的线索。然而，对C语言中的这些过程知之甚少。真香现在，de门多萨等人已经对C. fragrantissima的基因组，并分析哪些基因在其生命周期的各个阶段表达。该分析表明，该生物体以多种方式调节其基因表达，这些方式更常见于多细胞动物中的基因调节。此外，当与其他两种在生命周期中具有短暂多细胞阶段的动物亲属进行比较时，de门多萨等人发现，这三种生物在这些相似的生命周期阶段表达了相似的基因。此外，C. fragrantissima将食物从外部排出，然后吸收营养。利用一系列技术，de门多萨等人鉴定了参与这些过程的蛋白质，并发现许多蛋白质是独立于真菌中的对应物进化而来的。此外，在某些情况下，这些蛋白质的基因实际上是通过称为横向基因转移的过程从细菌中获得的。这些发现表明，多细胞动物的最后一个单细胞祖先可能已经具有创造不同细胞类型的生物学能力。在分子水平上了解单细胞物种中发现的细胞类型是否与海绵和梳状水母等简单动物的细胞类型相似，是确定活动物祖先的下一步。DOI：http://dx.doi.org/10.7554/eLife.08904.002网站
Cell-type specification through differential genome regulation is a hallmark of complex multicellularity. However, it remains unclear how this process evolved during the transition from unicellular to multicellular organisms. To address this question, we investigated transcriptional dynamics in the ichthyosporean Creolimax fragrantissima, a relative of animals that undergoes coenocytic development. We find that Creolimax utilizes dynamic regulation of alternative splicing, long inter-genic non-coding RNAs and co-regulated gene modules associated with animal multicellularity in a cell-type specific manner. Moreover, our study suggests that the different cell types of the three closest animal relatives (ichthyosporeans, filastereans and choanoflagellates) are the product of lineage-specific innovations. Additionally, a proteomic survey of the secretome reveals adaptations to a fungal-like lifestyle. In summary, the diversity of cell types among protistan relatives of animals and their complex genome regulation demonstrates that the last unicellular ancestor of animals was already capable of elaborate specification of cell types. DOI: http://dx.doi.org/10.7554/eLife.08904.001 All living animals are descended from a single-celled ancestor, and understanding how these ancestors became the first multicellular animals remains a major challenge in the field of evolutionary biology. An early breakthrough towards this goal was the realization that, even though they’re mostly single-celled organisms, the closest living relatives of animals share most of the basic gene toolkit that animals use to support their multicellular lifestyles. This shared toolkit also includes the genes that allow each specialized cell type in an animal (for example, a skin cell or liver cell) to express the subset of genes that it needs to fulfil its specific role. Discovering how the single-celled relatives of animals regulate these and other “multicellularity-related” genes during their life cycles is the next crucial step towards understanding how animals became multicellular. Creolimax fragrantissima is a single-celled relative of animals. One stage in this organism’s life cycle involves its nucleus (which contains its genetic material) replicating multiple times without the cell itself dividing. After this stage of development, new cells are formed, each receiving with a single nucleus, and released to live freely in the environment. Characterizing how C. fragrantissima regulates which genes are expressed during these two very different stages of development could shed new light on how multicellular animals evolved to regulate their genes in specific cell types. However, little is known about these processes in C. fragrantissima. Now, de Mendoza et al. have both sequenced C. fragrantissima’s genome and analysed which genes are expressed during the stages of its life cycle. This analysis reveals that this organism regulates its gene expression in several ways that are more commonly associated with gene regulation in multicellular animals. Furthermore, when compared to two other living relatives of animals that have brief multicellular stages in their life cycles, de Mendoza et al. found that the three organisms expressed similar genes during these similar life cycle stages. Furthermore, like fungi, C. fragrantissima digests its food externally and then absorbs the nutrients. Using a range of techniques, de Mendoza et al. identified the proteins involved in these processes and discovered that many had evolved independently from their counterparts in fungi. Furthermore, in some cases, the genes for these proteins had actually been acquired from bacteria via a process called lateral gene transfer. Together these findings suggest that it was likely that the last single-celled ancestor of multicellular animals already had the biological ability to create different cell types. Understanding if the cell types found in single-celled species resemble cell types from simple animals, such as sponges and comb jellies, at a molecular level is the next step towards determining what the ancestor of living animals looked like. DOI: http://dx.doi.org/10.7554/eLife.08904.002