Collaborative Research: Evolution of Multicellularity: Fluid Mechanics of Feeding by Unicellular vs. Multicellular Choanoflagellates

多细胞动物从单细胞原生动物的进化起源代表了生命史上的一个关键转变，也是最大的未解之谜之一。最近的遗传学研究表明，最原始的动物（海绵）与一组被称为鞭虫的原生动物非常密切相关。领鞭毛细胞通过摆动单个鞭毛来游动，并通过环绕鞭毛的微绒毛（细胞表面的毛发状突起）从周围的水中捕获食物（细菌）。一些单细胞的鞭藻可以通过细胞分裂诱导形成多细胞集落。其中一个生活在河口的物种，Salpingoeca rosetta，被用来研究多细胞生物的进化。对于多细胞生物的进化，多细胞生物一定有选择优势，但由于单细胞和群鞭虫今天仍然存在，可能存在不同的环境条件，单细胞或多细胞形式表现更好。影响鞭藻生存和繁殖的一个重要方面是捕食细菌。海洋栖息地在细菌斑块的大小、间距和丰富程度上可能有所不同。本研究利用罗塞塔花研究了多细胞和单细胞对觅食成功的影响，并发现了表现差异的机制。目的是：1)量化细菌分布不均匀的环境中单细胞与群体罗塞塔的游泳行为，确定是否以及如何在高猎物集中的斑块中聚集choanoflagellate；2)确定单细胞与群体罗塞塔在不同细菌猎物浓度下的取食率；3)研究罗塞塔水母产生水流和捕获猎物的流体力学，以阐明作为群体的一部分如何改变摄食电流，以及捕获猎物的机制和有效性。多学科团队的不同专业知识将集中在以下目标上：Koehl（生物流体动力学），King（鞭藻分子进化），Stocker（微观水生生物的生物物理学和生态学）和Fletcher（微观生物成像的先进光学技术）。本研究不仅探讨了觅食作为一种选择因子在多细胞生物的进化过程中所起的作用，而多细胞生物的进化过程是其后所有动物进化的起点，而且具有重要的生态学意义。原生动物，无论是单细胞的还是群体的，在水生食物网中都扮演着重要的角色。这个项目是第一个在单一原生动物物种中研究单细胞和多细胞对这些生态重要生物觅食的影响的项目。该项目将为研究生提供涉及物理学和生物学的研究培训，帮助他们培养跨学科合作的技能。为本项目开发的微流体系统将有助于研究斑块环境中的其他微生物，而我们的机器人鞭毛是未来研究波动游泳的原型。

The evolutionary origin of multicellular animals from a single-celled protozoan ancestor represents a pivotal transition in life's history and one of its greatest unsolved mysteries. Recent genetic studies have shown that the most primitive animals (sponges) are very closely related to a group of protozoans called choanoflagellates. A choanoflagellate cell swims by undulating a single flagellum and captures food (bacteria) from the surrounding water on a collar of microvilli (hair-like protrusions of the cell surface) that rings the flagellum. Some single-celled choanoflagellates can be induced to form multicellular colonies via cell division. One such species that lives in estuaries, Salpingoeca rosetta, is used to study the evolution of multicellularity. For multicellularity to evolve, there must have been a selective advantage to being multicellular, but since both unicellular and colonial choanoflagellates still exist today, there may be different environmental conditions under which single-celled or multicellular forms perform better. One important aspect of performance that affects choanoflagellate survival and reproduction is feeding on bacterial prey. Marine habitats can differ in the size, spacing, and richness of patches of bacteria. This study uses S. rosetta to study the consequences of being multicellular vs. unicellular to foraging success, and to discover the mechanisms responsible for differences in performance. The objectives are: 1) to quantify the swimming behavior of unicellular vs. colonial S. rosetta in environments in which bacteria are unevenly distributed, to determine if and how choanoflagellates aggregate in patches of high prey concentration; 2) to determine the feeding rates of unicellular vs. colonial S. rosetta for a range of bacterial prey concentrations; and 3) to study the fluid mechanics of water current production and prey capture by S. rosetta, to elucidate how being part of a colony alters the feeding current, and the mechanisms and effectiveness of prey capture. The diverse expertise of a multidisciplinary team will be focused on these objectives: Koehl (fluid dynamics of organisms), King (molecular evolution of choanoflagellates), Stocker (biophysics and ecology of microscopic aquatic organisms), and Fletcher (advanced optical techniques for imaging microscopic organisms). This study not only explores the role of foraging as a selective factor in the evolution of multicellularity, which set in motion all subsequent animal evolution, but also has ecological significance. Protozoans, both unicellular and colonial, play an important role in aquatic food webs. This project is the first to study, within a single protozoan species, the effects of being uni- vs. multicellular to foraging by these ecologically-important organisms.This project will provide research training for graduate students in a project involving both physics and biology, helping them develop skills for collaboration across disciplines. The microfluidics system developed for this project will be useful for studying other microscopic organisms in patchy environments, and our robotic flagellum is a prototype for future studies of undulatory swimming.