In the Light of Evolution Volume V: Cooperation and Conflict (2011) / Chapter Skim
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7 Social Evolution in Multispecies Biofilms--SARA MITRI, JOO B. XAVIER, and KEVIN R. FOSTER
7 Social Evolution in Multispecies Biofilms--SARA MITRI, JOO B. XAVIER, and KEVIN R. FOSTER
Pages 137-164
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From page 137... ...
We use a computer simulation of spatially structured cellular groups that captures key features of their biology and physical environment. When nutrient competition is strong, we find that the addition of new species can inhibit cooperation by eradicat ing secreting strains before they can become established.
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. This realization, along with the rapidly decreasing cost of DNA sequencing, has led to an impressive effort to identify and catalog microbial diversity across a wide range of environments.
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Modern stromatolites consist of multilayered sheets of microorganisms, and are a good example of very diverse, yet spatially structured microbial communities (copyright Merv Feick, http://www.Indiana9Fossils.com)
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A growing body of empirical work has shown that genotypic mixing has the potential to limit cooperativity in a wide range of microbial traits (Greig and Travisano, 2004; Gore et al., 2009) , including enzyme secretion (Griffin et al., 2004)
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The general question we ask is: What are the conditions that allow a cooperative secretor strain to o utcompete the nonsecretor strain, or vice versa? Whereas we focus on a secretion phenotype, the general conclusions of the model should have relevance for any cooperative traits that affect the growth rate of neighboring cells (Kreft, 2004)
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Cells may also secrete extracellular products, which become available to neighboring cells through diffusion. In the simulations presented, we assume that secretion carries an energetic cost of 30% of growth rate, in line with experimental results (Diggle et al., 2007b; Harcombe, 2010)
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Strain 1n does not secrete the product. Product secretion incurs a cost of 30% of the cells' growth rate.
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rarely benefit from the secretions. In agreement with this logic, at a low nutrient concentration, secretor cells have a significantly higher fitness than nonsecretors, regardless of whether product secretion incurred a cost (30% of their growth rate)
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In particular, species 2 is a proxy for multiple species that overlap only slightly (in space and/or time) with the focal species (see diagram)
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cooperative clumps of secretors such that secretors are more often overgrown. Consistent with the importance of ecological competition with species 2, we observe that the advantage of secretors over nonsecretors is significantly negatively correlated with the maximum growth rate of species 2 (Spearman's rank correlation test, r = −0.51, P < 0.001, Fig.
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This pattern was not observed at low nutrient concentrations (Fig.
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In particular, the fitness of nonsecretors is no longer significantly different from that of the secretors at low nutrient concentrations (Mann–Whitney test, df = 38, P = 0.22)
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. Product secretion by 1s incurs a cost of 30% of the cells' growth rate.
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The result is that in three-way competi tions, the secretors always perform poorly. Competition Among Microbial Groups The results presented above predict the evolutionary trajectory within a group of microbes and form a good first step to understand the effect of additional species on cooperation within a microbial group.
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We find that ecological competition with other species can preferentially harm secretor cells over nonsecretors. This result arises because investment in secretion can slow the growth of cell lin eages at critical stages and lead to their overgrowth by another species.
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152 / Sara Mitri et al. A 1s 1n + 2 Log invasion index 1 0 -1 -2 2-3 21 Nutrient concentration + B C + 1s1n 1s 1n + + 2 2 3 2 Log invasion index Log invasion index 2 1 1 0 0 -1 -1 -2 -2 -3 2-3 21 2-3 21 Nutrient concentration Nutrient concentration + + D E 1s 1n 1s 1n 2 + 2 + + 2 2 Log invasion index Log invasion index 1 1 0 0 -1 -1 -2 -2 2-3 21 2-3 21 Nutrient concentration Nutrient concentration
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, dark gray] n s s n cells separately in 40 replicates with high and low nutrient concentrations.
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. Social Insulation Under high-nutrient conditions, competitive effects are less severe and, accordingly, the impact of additional species upon within-species cooperation is reduced.
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With different nutrient requirements, the segregation index within species is significantly higher than between species under low nutrient concentrations (Mann–Whitney test, df = 38, P < 0.001, Fig. 7.6, Bottom Left)
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It appears that this condition allows secretors of the two species to mix, while keeping the two phenotypes of species 1 separate. This result is not observed when nutrient concentration is high.
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. The potential for such higher-level selection to shape microbial communities was seen in a large-scale simulation of microbial species growing and dispersing among a series of 10 interconnected flasks (Williams and Lenton, 2008)
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A central theme is the importance of spatial structure for microbial interactions, which can simultaneously promote within-species cooperation and limit among-species interac tions. Spatial structure in microbial groups can depend on a number of factors in addition to nutrient concentrations emphasized here.
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MGL−3 3.5 × 10−5 Half saturation constant for growth KG substrate concentration Number of cells of strain or species Dimensionless NA Nx,t x in a cell group at time t MEMX−1T−1 Rate of secretion of extracellular 1 RE 1s product by strain 1s MEMX−1T−1 Rate of secretion of extracellular 0 or 1 RE 2 product by species 2 T−1 Fitness of strain or species x NA wx MXL−3 Concentration of biomass of strain NA X1 s 1s (secretor cells) MXL−3 Concentration of biomass of strain NA X1 n 1n (nonsecretor cells)
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) is a function of local product secreted by strain or species x, f ð½Ex �Þ ¼ 1; ½Ex � > τ: All other symbols are defined in Table S1.
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is the Laplacian of the local solute concentration [S] , r is cell growth rate (computed using Table 7.2)
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The index is related to, and expected to correlate with, the relatedness coefficient from social evolution theory. However, the exact relation will depend on both the relative benefits of secretions to neighboring cells (Nadell et al., 2010)
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ACKNOWLEDGMENTS We thank Angus Buckling, Dan Cronforth, Laurent Keller, Wook Kim, Jan-Ulrich Kreft, Daniel Marbach, Carey Nadell, Nuno Oliveira, Jonas Schluter, and two anonymous reviewers for useful discussions and
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by a seed grant from the Lucille Castori Center for Microbes, Inflammation, and Cancer; and K.R.F. by European Research Council Grant 242670.
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