Flows driven by flagella of multicellular organisms enhance long-range molecular transport

Short, Martin B.; Solari, Cristian A.; Ganguly, Subha; Powers, Thomas; Kessler, Judd B.; Goldstein, Raymond E.

doi:10.1073/pnas.0600566103

Cited by 156 publications

(190 citation statements)

References 24 publications

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“…The hypothesis we have tested is that tradeoffs between reproduction and survival become increasingly convex with increasing size selecting for reproductive altruism, that is, soma. In the case of the volvocine algae, soma benefits the group both by enhancing motility and by mixing the surrounding medium allowing for more effective transport of nutrients and waste than would be possible by diffusion alone (15,18).…”

Section: How Does a Group Become An Individual?mentioning

confidence: 99%

“…For example, Volvox colonies migrate vertically several meters at night, presumably in search of higher phosphorous concentrations (23). In addition to motility, flagellar action provides for mixing the surrounding medium to aid in uptake of metabolites and elimination of waste (15,18).…”

Section: Cost Of Reproductionmentioning

confidence: 99%

“…Consequently, the cell growth (dependent on photosynthesis) and division (dependent on cell growth) of somatic cells are suppressed. Because they cannot divide, they do not participate directly in the offspring but contribute to the survival and reproduction of the colony through flagellar action (14,15,18). In other words, the somatic cells express an altruistic behavior, and regA [whose expression is necessary and sufficient for this behavior (16)] is an altruistic gene.…”

Section: Origin Of Reproductive Altruismmentioning

confidence: 99%

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Evolution of individuality during the transition from unicellular to multicellular life

Michod

2007

Proc. Natl. Acad. Sci. U.S.A.

273

251

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Individuality is a complex trait, yet a series of stages each advantageous in itself can be shown to exist allowing evolution to get from unicellular individuals to multicellular individuals. We consider several of the key stages involved in this transition: the initial advantage of group formation, the origin of reproductive altruism within the group, and the further specialization of cell types as groups increase in size. How do groups become individuals? This is the central question we address. Our hypothesis is that fitness tradeoffs drive the transition of a cell group into a multicellular individual through the evolution of cells specialized at reproductive and vegetative functions of the group. We have modeled this hypothesis and have tested our models in two ways. We have studied the origin of the genetic basis for reproductive altruism (somatic cells specialized at vegetative functions) in the multicellular Volvox carteri by showing how an altruistic gene may have originated through cooption of a life-history tradeoff gene present in a unicellular ancestor. Second, we ask why reproductive altruism and individuality arise only in the larger members of the volvocine group (recognizing that high levels of kinship are present in all volvocine algae groups). Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size. Concepts from population genetics and evolutionary biology appear to be sufficient to explain complexity, at least as it relates to the problem of the major transitions between the different kinds of evolutionary individuals.evolutionary transitions ͉ multicellularity ͉ Volvox

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Section: How Does a Group Become An Individual?mentioning

confidence: 99%

Section: Cost Of Reproductionmentioning

confidence: 99%

Section: Origin Of Reproductive Altruismmentioning

confidence: 99%

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Evolution of individuality during the transition from unicellular to multicellular life

Michod

2007

Proc. Natl. Acad. Sci. U.S.A.

273

251

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“…For a free swimming particle the increase in the mass flux at the particle surface scales to Pe 1/2 in comparison with Pe 1/3 for an inert translating sphere. Similarly, Short et al (2006) study molecular transport in suspensions of Volvocine green algae and demonstrate that the increase R. A. Lambert, F. Picano, W.-P. Breugem and L. Brandt of uptake due to swimming permits cells of radius r > 10 µm to overcome diffusion limitations and satisfy metabolic requirements.…”

Section: Introductionmentioning

confidence: 99%

Active suspensions in thin films: nutrient uptake and swimmer motion

et al. 2013

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A numerical study of swimming particle motion and nutrient transport is conducted for a semidilute to dense suspension in a thin film. The steady squirmer model is used to represent the motion of living cells in suspension with the nutrient uptake by swimming particles modelled using a first-order kinetic equation representing the absorption process that occurs locally at the particle surface. An analysis of the dynamics of the neutral squirmers inside the film shows that the vertical motion is reduced significantly. The mean nutrient uptake for both isolated and populations of swimmers decreases for increasing swimming speeds when nutrient advection becomes relevant as less time is left for the nutrient to diffuse to the surface. This finding is in contrast to the case where the uptake is modelled by imposing a constant nutrient concentration at the cell surface and the mass flux results to be an increasing monotonic function of the swimming speed. In comparison to non-motile particles, the cell motion has a negligible influence on nutrient uptake at lower particle absorption rates since the process is rate limited. At higher absorption rates, the swimming motion results in a large increase in the nutrient uptake that is attributed to the movement of particles and increased mixing in the fluid. As the volume fraction of swimming particles increases, the squirmers consume slightly less nutrients and require more power for the same swimming motion. Despite this increase in energy consumption, the results clearly demonstrate that the gain in nutrient uptake make swimming a winning strategy for micro-organism survival also in relatively dense suspensions.

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“…This issue of why and how the simplest unicellular organisms evolved to become multicellular and to exhibit cellular differentiation is one of the most fundamental issues in biology (Maynard-Smith & Szathmáry 1995), and has been of particular interest since the work of the great biologist August Weismann (1892). When one asks about the driving forces behind increased size it is important to recognize (Short et al 2006;) that one of the most important Fluid dynamics at the scale of the cell…”

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confidence: 99%

Batchelor Prize Lecture Fluid dynamics at the scale of the cell

Goldstein

2016

J. Fluid Mech.

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The world of cellular biology provides us with many fascinating fluid dynamical phenomena that lie at the heart of physiology, development, evolution and ecology. Advances in imaging, micromanipulation and microfluidics over the past decade have made possible high-precision measurements of such flows, providing tests of microhydrodynamic theories and revealing a wealth of new phenomena calling out for explanation. Here I summarize progress in four areas within the field of 'active matter': cytoplasmic streaming in plant cells, synchronization of eukaryotic flagella, interactions between swimming cells and surfaces and collective behaviour in suspensions of microswimmers. Throughout, I emphasize open problems in which fluid dynamical methods are key ingredients in an interdisciplinary approach to the mysteries of life.

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Flows driven by flagella of multicellular organisms enhance long-range molecular transport

Cited by 156 publications

References 24 publications

Evolution of individuality during the transition from unicellular to multicellular life

Evolution of individuality during the transition from unicellular to multicellular life

Active suspensions in thin films: nutrient uptake and swimmer motion

Batchelor Prize Lecture Fluid dynamics at the scale of the cell

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