Switch between life history strategies due to changes in glycolytic enzyme gene dosage in Saccharomyces cerevisiae

Abstract

Adaptation is the process whereby a population or species becomes better fitted to its habitat through modifications of various life history traits which can be positively or negatively correlated. The molecular factors underlying these covariations remain to be elucidated. Using Saccharomyces cerevisiae as a model system, we have investigated the effects on life history traits of varying the dosage of genes involved in the transformation of resources into energy. Changing gene dosage for each of three glycolytic enzyme genes (hexokinase 2, phosphoglucose isomerase, and fructose-1,6-bisphosphate aldolase) resulted in variation in enzyme activities, glucose consumption rate, and life history traits (growth rate, carrying capacity, and cell size). However, the range of effects depended on which enzyme was expressed differently. Most interestingly, these changes revealed a genetic trade-off between carrying capacity and cell size, supporting the discovery of two extreme life history strategies already described in yeast populations: the "ants," which have lower glycolytic gene dosage, take up glucose slowly, and have a small cell size but reach a high carrying capacity, and the "grasshoppers," which have higher glycolytic gene dosage, consume glucose more rapidly, and allocate it to a larger cell size but reach a lower carrying capacity. These results demonstrate antagonist pleiotropy for glycolytic genes and show that altered dosage of a single gene drives a switch between two life history strategies in yeast.

FIG. 1.

Mean activity of glucose-phosphorylating enzymes (white bars), phosphoglucose isomerase (gray bars), and fructose-1,6-bisphosphate aldolase (dark gray bars) in expression mutants relative to the wild-type (wt) strain (A_ij/A_wt). The symbol Δ indicates deletions of one (pgiΔ and fbaΔ) or two (hxk2Δ/hxk2Δ) genomic copies. Overexpression of a gene in the multicopy pCM190 vector is indicated by a superscript (over).

FIG. 2.

Relationships between the glucose consumption rate (J_T25) and growth rate (R_T25), carrying capacity, or cell size. Each point is obtained from a replicate of a transformed strain. Open squares, HXK2-transformed strains; gray triangles, PGI1-transformed strains; black diamonds, FBA1-transformed strains.

FIG. 3.

Relationship between the carrying capacity (K) and cell size. The symbols are the same as those described in the legend of Fig. 2.