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Physical aspects of evolutionary transitions to multicellularity

Reference	BB/F021844/1
Principal Investigator / Supervisor	Professor Raymond Goldstein
Co-Investigators / Co-Supervisors
Institution	University of Cambridge
Department	Applied Maths and Theoretical Physics
Funding type	Research
Value (£)	566,923
Status	Completed
Type	Research Grant
Start date	01/06/2008
End date	31/05/2011
Duration	36 months

Abstract

This research addresses a fundamental problem in evolutionary biology: the transition from single cell organisms to multicellular ones. A model lineage, the Volvocalean green algae, will be studied to determine the scaling laws in motility and metabolism that may help explain the driving forces which led to multicellularity. These organisms range from unicellulular, totipotent Chlamydomonas to multicellular Volvox species with thousands of cells and exhibiting germ-soma differentiation. Prior studies have established that the collective flagellar beating of the larger species generates such high fluid flows that advective molecular transport strongly dominates diffusive transport, while the unicellular members are in the regime of low Peclet number. This led to a hypothesis that flagella-driven fluid flows confer an advantage in nutrient uptake rate to larger organisms and thereby provide an evolutionary driving force toward larger species. Our detailed investigation of this hypothesis will involve experimental studies and aspects of mathematical biology. We will utilize fluid dynamical and cell biological methods to study scaling laws for swimming and metabolism across a range of species, and develop mathematical methods to understand this and the associated metabolite exchange dynamics at high Peclet number. The interrelated issues of flagellar synchronization, rotational motions, and phototaxis will be studied by high-speed digital video microscopy and particle imaging velocimetry, and analyzed theoretically, with the goal of understanding how many thousands of flagella can produce the coordinated motions necessary for life processes. Co-funded by EPSRC.

Summary

A very profound and interesting issue in the evolution of complex life forms is the manner by which the transition from unicellular organisms to multicellular ones occurred. There at least two fundamental issues in this most basic transition. What are the advantages of increasing size? and: What are the driving forces behind cell specialization? These questions must be viewed in the context of the most basic feature of life: the continuous exchange with the environment of nutrients and wastes. Given that the simplest unicellular organisms and their multicellular successors inhabit an aqueous environment, it is clear that the physics of buoyancy, diffusion, and mixing should play an important role in these considerations. In the conventional biological view appopriate to small organisms such as individual bacteria which swim slowly, diffusion is much faster than advection by fluid motions. Such is generally not the case for larger organisms, which create fluid flows around themselves by the action of multitudes of flagella. These flows increase in speed with increasing organism size, to the point that they outpace diffusion. Using modern techniques from fluid mechanics, we have recently established that the Volvocalean green algae, a lineage of photosynthetic organisms that serves as a model for research on evolutionary transitions to multicellularity, covers a very broad range of the balance between diffusion and stiring, from diffusion-dominated at the single cell level, to stirring-dominated for colonies composed of thousands of cells. This lineage affords the possibility of deconstructing laws in motility and metabolism that may help explain the evolutionary driving forces which led to multicellularity. These flows are driven by the coordinated action of thousands of flagella on the surface of these colonies, and imply metabolic dynamics fundamentally different than those limited by passive diffusion. Our recent work suggests that such flows can play a crucialrole in the colony metabolism, and would have conferred an evolutionary advantage to larger organisms. The developments outlined above have allowed us to establish a working hypothesis which links motility, mixing, and multicellularity. The next step is the full exploration of this hypothesis. Using the volvocine green algae as a model lineage, we have four main goals. (i) We will implement an experimental method by which the link between metabolic activity and fluid flow can be tested. This will be accomplished with optical methods that probe the amount of photosynthesis occurring in these algae, both in the presence and absence of fluid flow from flagellar beating. These flows will be created in microscopic channels created with methods in the field of 'microfluidics.' (ii) We will develop a method to study the manner in which multiple flagella becomes synchronized on these organsisms. This will involve the use of high-speed imaging to visualize flagellar coordination during swimming and phototaxis, as a probe of the hydrodynamic synchronization of molecular motors which underlies the collective fluid flows. A key issue is the dependence of synchronization dynamics on inter-somatic cell spacing, a range of which can be studied using diverse members of the volvocine algae at various points in their life cycles. (iii) Further develop mathematical models of flagella-driven flows and their implications for scaling laws in locomotion, metabolite exchange, and thus evolutionary transitions to multicellularity. (iv) Develop theoretical models for the dynamics by which these algae steer toward the light by modulating their flagellar beating.

Committee	Closed Committee - Engineering & Biological Systems (EBS)
Research Topics	Plant Science, Systems Biology
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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