Collaborative Research: DMS/NIGMS2: Computational and Experimental Analysis of Choanoflagellate Hydrodynamic Performance - Selective Factors in the Evolution of Multicellularity

多细胞动物从单细胞原生动物祖先进化而来是地球生命史上的一个关键转折。鞭虫是与动物有着共同祖先的原生动物。它们可以是单细胞的，也可以通过细胞分裂形成多细胞集落，因此我们正在研究它们以获得对多细胞进化的见解。由于多细胞生物是通过动物祖先的自然选择进化而来的，因此影响生长、繁殖和生存的活动表现在群体中比在单细胞中更好。该项目将重点研究单细胞和多细胞领鞭毛虫在影响其适应性的活动方面的表现差异：游泳、进食和避免被捕食——所有这些都取决于生物体周围的流体流动。该项目还将解决一个重要的生态问题。鞭毛虫和其他以细菌为食并被小动物吃掉的微小原生动物是水生食物网的关键一环。许多原生动物是单细胞的，而另一些则形成多细胞群体，但单细胞与多细胞在游泳、摄食和逃跑性能上的差异尚不清楚。产生单细胞和多细胞形式的领鞭毛虫使我们能够研究群体形成对单一物种内这些功能表现的影响。单细胞领鞭毛虫具有卵形细胞体和单个鞭毛，鞭毛被微绒毛环绕。细胞通过摆动其鞭毛来游泳，这也产生了一股水流，将细菌带到捕获猎物的微绒毛的领子上。我们将协调实验室实验与数学模型和计算机模拟，研究流体动力学机制，决定鞭藻的性能。因此，从鞭藻中了解到的单细胞与多细胞群体的表现原理可能会揭示影响水生原生动物生态相互作用的机制，以及动物的进化起源。该项目还将为本科生和研究生以及博士后学者提供参与研究的机会。捕食成功和躲避捕食者可能是单细胞向多细胞进化过程中重要的选择因素。我们的跨学科团队将协调实验室实验、数学建模和计算模拟，以研究不同形态的单细胞和群体鞭毛藻的游泳、摄食和与捕食者的相互作用的流体动力学，以及海绵鞭毛细胞的泵送和摄食。模型将被开发来探测细胞形态、数量和排列的影响，这些影响可以以系统的方式变化，这在真正的鞭藻中是不可能的。这些微型系统需要新颖的方法来捕捉细胞形态、限制结构的几何形状、动态附着、细菌从鞭毛项圈上脱离，以及呈现给捕食者的化学和流体动力学信号。本文将采用正则化stokeslet方法对这些复杂系统进行建模。实验室实验将使用单细胞的鞭虫物种，它们可以形成莲座群落，鞭毛指向外面，或者形成杯状群落，可以由内而外翻转，鞭毛排列在杯子上，以及捕食鞭虫的原生动物。微型摄像技术将用于对鞭藻产生的流场进行粒子跟踪测速，并测量游泳速度、摄食率以及与捕食者的相互作用。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

The evolution of multicellular animals from a unicellular protozoan ancestor was a pivotal transition in the history of life on earth. Choanoflagellates are protozoans that share a common ancestor with animals. They can be unicellular or form multicellular colonies by cell division, so we are studying them to gain insights about the evolution of multicellularity. For multicellularity to have evolved via natural selection in the ancestors of animals, the performance of activities that affected growth, reproduction, and survival would have been better for colonies than for single cells. This project will focus on performance differences between unicellular and multicellular choanoflagellates of activities that affect their fitness: swimming, feeding, and avoiding predation – all of which depend upon the fluid flow around the organisms. This project also will address an important ecological issue. Choanoflagellates and other microscopic protozoans that eat bacteria and are in turn consumed by small animals are a critical link in aquatic food webs. Many protozoans are unicellular, while others form multicellular colonies, but the consequences to swimming, feeding, and escape performance of being single-celled versus multicellular are not yet understood. Choanoflagellates that produce both unicellular and multicellular forms permit us to study the effects of colony formation on the performance of these functions within a single species. A unicellular choanoflagellate has an ovoid cell body and a single flagellum surrounded by a collar of microvilli. The cell swims by waving its flagellum, which also creates a water current that brings bacteria to the collar of prey-capturing microvilli. We will coordinate laboratory experiments with mathematical models and computer simulations that study the hydrodynamic mechanisms that determine the performance of choanoflagellates. Thus, the principles learned from choanoflagellates about the performance of single cells versus multicellular colonies may shed light on mechanisms affecting ecological interactions of aquatic protozoans, as well as on the evolutionary origins of animals. The project will also provide opportunities for undergraduate and graduate students, and postdoctoral scholars to participate in the research.Feeding success and predator avoidance are examples of performance that might have been important selective factors in the evolution from single cells to multicellularity. Our interdisciplinary team will coordinate laboratory experiments, mathematical modeling, and computational simulations to study the hydrodynamics of swimming, feeding, and interacting with predators by unicellular versus colonial choanoflagellates of various configurations, and of pumping and feeding by sponge choanocytes. Models will be developed that probe the effects of cell morphology, number, and arrangement that can be varied in systematic ways not possible with real choanoflagellates. These microscale systems require novel methods that capture cell morphology, geometry of confining structures, dynamic attachment, and detachment of bacteria from choanoflagellate collars, and the chemical and hydrodynamic signals presented to predators. The method of regularized Stokeslets will be advanced to model these complex systems. Lab experiments will use species of choanoflagellates that can be unicellular and form rosette colonies with flagella pointing outwards, or that form cup-shaped colonies that can turn inside-out so the flagella line the cup, as well as protozoan predators on choanoflagellates. Micro videography will be used for particle-tracking velocimetry of flow fields produced by the choanoflagellates, and to measure swimming speeds, feeding rates, and interactions with predators.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.