The molecular basis of phenotypic evolution in social amoebas

社会阿米巴原虫表型进化的分子基础

• 批准号: BB/K000799/1
• 负责人: Pauline Schaap
• 金额: $ 85.8万
• 依托单位: University of Dundee
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2013
• 资助国家: 英国
• 起止时间: 2013 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=BB%2FK000799%2F1
• 关键词: molecular; basis; phenotypic; evolution; social

Biologists want to understand how complex multicellular organisms have evolved from simple single-celled ancestors. We know in theory what happened: Spontaneous mutations in the genes of earlier organisms caused small changes in the developmental program of their offspring. This sometimes resulted in an improved adult that more successfully reproduced, and therefore gradually replaced the earlier form. However, to really understand this process and prove that it actually occurred, we have to trace back which genes were mutated and how this mutation changed gene function. We also need to know which developmental mechanisms were regulated by the mutated genes and how the altered developmental mechanism eventually produced the improved adult form. Because it is not possible to obtain such detailed information for highly evolved animals like ourselves, we investigate this problem in the social amoebas. These organisms live as single cells when they are feeding, but aggregate when starved to form a multicellular fruiting body, in which a proportion of cells is preserved as spores. The other cells form a stalk and other structures to support the spore mass. This life style depends on mutual collaboration and specialization of cells. One species, D.discoideum, is used by many laboratories as a model system to understand how cells move, eat, propagate and communicate with each other. In previous research, we constructed a family tree of all 100 known social amoeba species, which showed that there are four major groups of social amoebas. For each of the 100 species, we have measured 30 properties (traits), which describe their behaviours, the size and shape of their component parts and the number of cell types in which they can differentiate. By combining this information with the family tree, we have gained information in what order these traits evolved and which traits are always seen together. The earliest social amoeba formed very small fruiting bodies directly from aggregates. All cells first differentiated into prespore cells and then some changed again to form the stalk. These early species probably used a compound called glorin to aggregate and, like their ancestors the solitary amoebas, they could still form cysts from single cells to survive starvation.The ability to form large fruiting bodies appeared together with an intermediate migratory "slug" stage that could bring the aggregates to the soil surface. Inside the slug prestalk and prespore cells differentiated in the same proportions as needed in the fruiting body. Cells also formed new structures to support the stalk and used cAMP pulses to aggregate. However, they lost the ability to form cysts. In the new project we want to understand how these traits evolved and why they evolved together. What is the connection between them and what novel mechanisms were needed to obtain more cell types and build larger structures. Secondly, we want to understand how the genes of the more advanced species were altered to make these changes possible.In collaboration with a German team, we have recently sequenced the genomes of species that represent groups 1,2 and 3 of social amoebas. The genome of D.discoideum in group 4 was already sequenced before. We can now, in theory, identify changes in all the genes that occurred during evolution. However, due to the large number of genes in each organism (~12.000) this requires at first a computational approach to identify the most likely genes to be involved in the mechanisms that we want to study. Once candidate genes have been selected, we can replace the gene of a more evolved species with that of an earlier form and see whether this results in the loss of the more advanced property. The reverse is also possible. In this manner we will be able to determine the genetic mechanisms that have been used by evolution to generate the enormous variety of multicellular organisms that we see today.

生物学家想了解复杂的多细胞生物是如何从简单的单细胞祖先进化而来的。我们在理论上知道发生了什么：早期生物体基因的自发突变导致其后代发育程序的微小变化。这有时会导致一个更成功地繁殖的改进的成年人，因此逐渐取代了早期的形式。然而，要真正理解这一过程并证明它确实发生了，我们必须追溯哪些基因发生了突变，以及这种突变如何改变基因功能。我们还需要知道哪些发育机制受到突变基因的调控，以及改变的发育机制最终如何产生改进的成体形式。由于不可能获得像我们这样高度进化的动物的详细信息，我们在社会阿米巴中研究这个问题。这些生物在进食时以单细胞形式生活，但在饥饿时聚集形成多细胞子实体，其中一部分细胞以孢子形式保存。其他细胞形成柄和其他结构来支撑孢子团。这种生活方式依赖于细胞的相互协作和专业化。其中一个物种D.discoideum被许多实验室用作模型系统，以了解细胞如何移动，进食，繁殖和相互交流。在以前的研究中，我们构建了一个所有100种已知的社会性阿米巴物种的家谱，这表明有四个主要的社会性阿米巴。对于100个物种中的每一个，我们测量了30个特性（性状），这些特性描述了它们的行为，它们组成部分的大小和形状以及它们可以分化的细胞类型的数量。通过将这些信息与家谱相结合，我们已经获得了这些特征进化的顺序以及哪些特征总是一起出现的信息。最早的社会性变形虫直接从聚集体中形成非常小的子实体。所有细胞先分化为前孢子细胞，然后部分细胞再分化形成柄。这些早期的物种可能使用一种叫做glorin的化合物来聚集，就像它们的祖先孤独的变形虫一样，它们仍然可以从单细胞中形成包囊来生存饥饿。形成大型子实体的能力出现在一个中间迁移的“鼻涕虫”阶段，可以将聚集体带到土壤表面。在蛞蝓体内，前柄细胞和前孢子细胞按子实体所需的比例分化。细胞还形成了新的结构来支持茎，并使用cAMP脉冲来聚集。然而，它们失去了形成囊肿的能力。在这个新项目中，我们想了解这些特征是如何进化的，以及为什么它们会一起进化。它们之间的联系是什么，需要什么新的机制来获得更多的细胞类型和构建更大的结构。其次，我们想了解更高级物种的基因是如何改变的，使这些变化成为可能。在与一个德国小组的合作下，我们最近对代表社会性变形虫第1、2和3组的物种的基因组进行了测序。第4组盘状杜父菌的基因组此前已被测序。从理论上讲，我们现在可以识别进化过程中发生的所有基因的变化。然而，由于每个生物体中有大量的基因（~12.000），这首先需要一种计算方法来确定最有可能参与我们想要研究的机制的基因。一旦候选基因被选定，我们就可以用一种更早的形式的基因取代进化程度更高的物种的基因，看看这是否会导致更先进的特性的丧失。反过来也是可能的。通过这种方式，我们将能够确定进化所使用的遗传机制，以产生我们今天看到的各种各样的多细胞生物。

项目成果

A cyanobacterial light activated adenylyl cyclase partially restores development of a Dictyostelium discoideum, adenylyl cyclase a null mutant.

• DOI: 10.1016/j.jbiotec.2014.08.008
• 发表时间: 2014-12-10
• 期刊: JOURNAL OF BIOTECHNOLOGY
• 影响因子: 4.1
• 作者: Chen, Zhi-hui;Raffelberg, Sarah;Losi, Aba;Schaap, Pauline;Gaertner, Wolfgang
• 通讯作者: Gaertner, Wolfgang

The Evolution of Aggregative Multicellularity and Cell-Cell Communication in the Dictyostelia.

• DOI: 10.1016/j.jmb.2015.08.008
• 发表时间: 2015-11-20
• 期刊: JOURNAL OF MOLECULAR BIOLOGY
• 影响因子: 5.6
• 作者: Du, Qingyou;Kawabe, Yoshinori;Schilde, Christina;Chen, Zhi-hui;Schaap, Pauline
• 通讯作者: Schaap, Pauline

The social amoeba Polysphondylium pallidum loses encystation and sporulation, but can still erect fruiting bodies in the absence of cellulose.

• DOI: 10.1016/j.protis.2014.07.003
• 发表时间: 2014-09
• 期刊: PROTIST
• 影响因子: 2.5
• 作者: Du, Qingyou;Schaap, Pauline
• 通讯作者: Schaap, Pauline

Dictyostelium discoideum Protocols

• DOI: 10.1007/978-1-62703-302-2
• 发表时间: 2006-07
• 作者: L. Eichinger;F. Rivero

Secreted Cyclic Di-GMP Induces Stalk Cell Differentiation in the Eukaryote Dictyostelium discoideum.

• DOI: 10.1128/jb.00321-15
• 发表时间: 2016-01-01
• 期刊: Journal of bacteriology
• 影响因子: 3.2
• 作者: Chen ZH;Schaap P
• 通讯作者: Schaap P