Multicellularity and the functional interdependence of motility and molecular transport

Abstract

Benefits, costs, and requirements accompany the transition from motile totipotent unicellular organisms to multicellular organisms having cells specialized into reproductive (germ) and vegetative (sterile soma) functions such as motility. In flagellated colonial organisms such as the volvocalean green algae, organized beating by the somatic cells' flagella yields propulsion important in phototaxis and chemotaxis. It has not been generally appreciated that for the larger colonies flagellar stirring of boundary layers and remote transport are fundamental for maintaining a sufficient rate of metabolite turnover, one not attainable by diffusive transport alone. Here, we describe experiments that quantify the role of advective dynamics in enhancing productivity in germ somadifferentiated colonies. First, experiments with suspended deflagellated colonies of Volvox carteri show that forced advection improves productivity. Second, particle imaging velocimetry of fluid motion around colonies immobilized by micropipette aspiration reveals flow fields with very large characteristic velocities U extending to length scales exceeding the colony radius R. For a typical metabolite diffusion constant D, the associated Peclet number Pe ‫؍‬ 2UR͞D Ͼ Ͼ 1, indicative of the dominance of advection over diffusion, with striking augmentation at the cell division stage. Near the colony surface, flows generated by flagella can be chaotic, exhibiting mixing due to stretching and folding. These results imply that hydrodynamic transport external to colonies provides a crucial boundary condition, a source for supplying internal diffusional dynamics.diffusion ͉ flagella ͉ Volvox T he efficient exchange of nutrients, metabolites, and wastes is among the most basic factors affecting the fitness of organisms. Understanding the effect of resource delivery and exchange on metabolic rate, as organisms increase in size, is leading to rapid advances across disparate fields of the life sciences, from comparative biology to ecosystem ecology (1-4). Yet, these insights have not been applied to the analysis of the evolutionary transitions which underlie the hierarchy of life (5, 6). Although cooperative endeavors provide substantial benefits, certain key problems must be solved for a group to emerge into a new complex individual. As lower level units (cells) associate to form groups, the constraints of surface to volume ratio, S͞V, and of spatial organization limit the type and extent of interactions with the environment, with profound effects on metabolism, growth rate, viability, and fecundity. We refer to this as the ''transport limitation'' and view it as a general aspect of evolutionary transitions in individuality.Nutrient consumption increases proportionally with the size of the organism, creating an increased boundary layer of nutrient depletion. In the absence of active mixing of the medium, this decreases the passive diffusion of nutrients. This transport limitation constraint as size increases can be circumvented in several ways. For example, d...

Evolution of individuality during the transition from unicellular to multicellular life

“…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.…”

“…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).…”

“…In addition, during development, as reproductive cells increase in size, motility does not change for small species, but declines for the larger species (14,25). Apparently, because the length of the flagella increases as cells increase in size, this allows the smaller species to maintain their motility as they increase in size during development (15,25).…”

“…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).…”

“…Second, we ask why reproductive altruism arises only in the larger members of the volvocine group. Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size (14,15).…”