The advantages of clumpiness

August 18, 2011 § Leave a comment

A nice paper that emerged from a collaboration between the Murray lab and Kevin Foster (ex-Bauer Fellow, now at the Zoology Department at Oxford University and the Oxford Center for Integrative Systems Biology) just came out in PLoS Biology (Koschwanez et al. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biology 9(8): e1001122).  The paper makes two interesting points that are potentially relevant to the evolution of multicellular organisms.   The first is that yeast strains that grow in clumps of cells should, and do, have an advantage over strains that grow as single cells when both strains are grown in low levels of sucrose.  The theoretical argument the authors make goes like this: to metabolize sucrose, cells need to secrete invertase, which chops up sucrose to give fructose and glucose; each cell then needs to absorb as much as possible of the monosaccharides produced before they diffuse away.  A cell can only capture the fructose and glucose that happens to bump into the transporters on its cell wall.  So, even though sucrose has the same food value as glucose + fructose, single cells should grow less effectively on sucrose than on glucose + fructose; and there should be a threshold sucrose concentration below which a single cell cannot grow at all.  In contrast, cells living in a clump should benefit from the fact that all of their neighbors are producing monosaccharides too; even though an individual cell might not be able to take up all the glucose and fructose it produces using its invertase enzymes, it will capture some of the monosaccharides that escape from its neighbors.  Thus, clumping cells should grow better than single cells in low concentrations of sucrose.  When Koschwanez et al. did the experiments all of these predictions were confirmed.

The second point is even more interesting.  The invertase system is a classic set-up for cheating; the cells secreting invertase are effectively producing a “public good” — the monosaccharides produced by the action of the invertase on sucrose are available to anyone nearby.  At the same time, producing invertase has a cost, which the authors measure as a fitness disadvantage of 0.35% in exponentially growing cells.  Under some conditions, therefore, cells that don’t secrete invertase grow better than those that do, because they are able to take up the monosaccharides produced by the cells around them without producing the costly invertase enzyme.  Whether this works depends on factors like cell density (high is good for cheating) and how much the culture is agitated (shaking helps spread sugars around, which is also good for cheating).  But Koschwanez et al. show that the clumping strain does better than single-cell strains when competed with matched clumping or non-clumping cheaters, under a variety of conditions.  Clumping allows the cells that are playing fair to stick together and share resources; conversely, if you’re a cheater growing in a clump it’s harder to escape your (similarly cheating) sisters and daughters.

When an interesting paper like this comes out from not one, but two, of our friends, I would normally make every effort to write a properly detailed post about it.  But this one has been written up all over, at New Scientist, the Harvard Gazette, MSNBC and a PLoS Biology minireview, among others; and most intimidatingly of all by Ed Yong. It’s good to see so much interest, and since I can’t think of a single point that hasn’t already been made I’ll content myself with pointing you to the rest of the coverage.  Enjoy!

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