Contribution of individual random mutations to genotype-by-environment interactions in Escherichia coli

Numerous studies have shown genotype-by-environment (G×E) interactions for traits related to organismal fitness. However, the genetic architecture of the interaction is usually unknown because these studies used genotypes that differ from one another by many unknown mutations. These mutations were also present as standing variation in populations and hence had been subject to prior selection. Based on such studies, it is therefore impossible to say what fraction of new, random mutations contributes to G×E interactions. In this study, we measured the fitness in four environments of 26 genotypes of Escherichia coli, each containing a single random insertion mutation. Fitness was measured relative to their common progenitor, which had evolved on glucose at 37°C for the preceding 10,000 generations. The four assay environments differed in limiting resource and temperature (glucose, 28°C; maltose, 28°C; glucose, 37°C; and maltose, 37°C). A highly significant interaction between mutation and resource was found. In contrast, there was no interaction involving temperature. The resource interaction reflected much higher among mutation variation for fitness in maltose than in glucose. At least 11 mutations (42%) contributed to this G×E interaction through their differential fitness effects across resources. Beneficial mutations are generally thought to be rare but, surprisingly, at least three mutations (12%) significantly improved fitness in maltose, a resource novel to the progenitor. More generally, our findings demonstrate that G×E interactions can be quite common, even for genotypes that differ by only one mutation and in environments differing by only a single factor.