Effect of dispersal and nutrient availability on the competitive ability of toxin-producing yeast

Abstract

The ecological role of interference competition through toxin production is not well understood. In particular, it is unclear under what conditions the benefits of toxic killing outweigh the metabolic costs involved. A killer advantage has been suggested to rely on local competitive interactions where the benefits of killing accrue to the toxin producer preferentially, but this notion has little empirical support. In addition, contrasting predictions exist about the effect of resource abundance on the benefits of toxin production; this benefit should either be highest when resources are abundant and metabolic costs are relatively low or when resources are scarce and toxic killing is a 'last resort strategy' to obtain nutrients. Here, we test these predictions for one aspect of competitive ability, that is, the ability of toxin producers to invade a population of sensitive non-producers from a low initial frequency. We use competition experiments between isogenic K1 toxin-producing and non-producing strains of Saccharomyces cerevisiae, where we manipulate dispersal under two extreme nutrient conditions: one environment with and the other without replenishment of nutrients. We find that toxin production is beneficial when dispersal is limited under both nutrient conditions, but only when resources are abundant these outweigh its cost and allow invasion of the producer.

Figure 1

Fitness of the killer (K), sensitive (S) and control (C) strains relative to a resistant reference strain measured in direct competition in the Nut⁺ Dis⁺ environment with at least 20-fold replication. C and K carry the same genetic marker (grey bars), which is different from that of S (white bar). Error bars represent 95% CIs.

Figure 2

Trajectories of the log ratio of K versus S and C versus S densities during the 80 days of competition in three replicate populations in four environments: (a) Nut⁺ Dis⁻, (b) Nut⁺ Dis⁺, (c) Nut⁻ Dis⁻ and (d) Nut⁻ Dis⁺ environment. Closed symbols are for K/S and open symbols for C/S. The dashed line in (b) shows the expected trajectory based on the resource competitive difference between K and S only (i.e. without the effect of toxic killing). To estimate the frequency of K and S in the Nut⁻ environment, populations had to be destroyed, and hence the trajectories reflect the average and s.e. of three different replicate populations for each time point.

Figure 3

Assay of toxic killing in the Nut⁻ environment. The change in frequency of both the strains (S, white bars and K, grey bars) in competition relative to monoculture in four constitutive intervals during the 21 days of the experiment is shown. (a) Dis⁺ environment and (b) Dis⁻ environment. Error bars reflect the s.e. based on pseudovalues from the jackknife procedure (see §2).