The spatial and metabolic basis of colony size variation

Abstract

Spatial structure impacts microbial growth and interactions, with ecological and evolutionary consequences. It is therefore important to quantitatively understand how spatial proximity affects interactions in different environments. We tested how proximity influences colony size when either Escherichia coli or Salmonella enterica are grown on various carbon sources. The importance of colony location changed with species and carbon source. Spatially explicit, genome-scale metabolic modeling recapitulated observed colony size variation. Competitors that determine territory size, according to Voronoi diagrams, were the most important drivers of variation in colony size. However, the relative importance of different competitors changed through time. Further, the effect of location increased when colonies took up resources quickly relative to the diffusion of limiting resources. These analyses made it apparent that the importance of location was smaller than expected for experiments with S. enterica growing on glucose. The accumulation of toxic byproducts appeared to limit the growth of large colonies and reduced variation in colony size. Our work provides an experimentally and theoretically grounded understanding of how location interacts with metabolism and diffusion to influence microbial interactions.

Increasing growth rate slows adaptation when genotypes compete for diffusing resources

“…0.05cm / box). DR = 5e-6 cm 2 / s, which is typical for a small sugar in water or a 1% agar Petri dish (Chacón et al, 2018). DB1 = DB2 = 5e-9 cm 2 / s, i.e.…”

“…Spatial structure, or more specifically the degree of localization of competitive interactions, is not a binary variable. It changes depending on resource diffusivity (Allison, 2005;Menon & Korolev, 2015;Stump, Johnson, & Klausmeier, 2018) and the proximity and growth rate of individuals (Chacón et al, 2018). Therefore, we sought to quantify spatial structure, specifically by quantifying the degree to which interactions were localized.…”

“…This is because in spatially-structured environments, competitive interactions are more likely to be localized, and so individuals with a beneficial mutation more often compete with themselves than with ancestors (Habets et al, 2007). However, localized interactions are not a requirement of spatial structure (Chacón, Möbius, & Harcombe, 2018): slow resource acquisition rates can result in population dynamics which resemble a well-mixed system. Therefore, it is uncertain…”

Increasing growth rate slows adaptation when genotypes compete for diffusing resources

“…This is because in spatially-structured environments, competitive interactions are more likely to be localized, and so individuals with a beneficial mutation compete more often with their own genotype than with ancestors [4]. However, even in the presence of spatial structure, slow resource acquisition rates can result in population dynamics which resemble a well-mixed system [7]. Therefore, it is uncertain whether the effect of spatial structure on the rate of adaptation is constant or dependent on the biological and environmental details of the species examined.…”

“…For example, epistatic interactions between mutations can result in reduced rates of adaptation that diminish the effect of additional mutations [11][12][13][14], and these diminishing returns can be compounded by spatial structure [2]. Similarly, spatial structure can increase genetic drift and founder effects, thereby reducing the rate of adaptation [7,15]. However, neither of these negative effects of spatial structure on the rate of adaptation are universal: they can be ameliorated by increased dispersal rates or resource diffusion, which serve to make a system more well-mixed [4,16,17].…”