The Role of the Environment in Horizontal Gene Transfer

Abstract

Gene-by-environment interactions play a crucial role in horizontal gene transfer by affecting how the transferred genes alter host fitness. However, how the environment modulates the fitness effect of transferred genes has not been tested systematically in an experimental study. We adapted a high-throughput technique for obtaining very precise estimates of bacterial fitness, in order to measure the fitness effects of 44 orthologs transferred from Salmonella Typhimurium to Escherichia coli in six physiologically relevant environments. We found that the fitness effects of individual genes were highly dependent on the environment, while the distributions of fitness effects across genes were not, with all tested environments resulting in distributions of same shape and spread. Furthermore, the extent to which the fitness effects of a gene varied between environments depended on the average fitness effect of that gene across all environments, with nearly neutral and nearly lethal genes having more consistent fitness effects across all environments compared to deleterious genes. Put together, our results reveal the unpredictable nature of how environmental conditions impact the fitness effects of each individual gene. At the same time, distributions of fitness effects across environments exhibit consistent features, pointing to the generalizability of factors that shape horizontal gene transfer of orthologous genes.

Keywords: distribution of fitness effects; evolutionary barriers; gene-by-environment interactions; horizontal gene transfer.

Fig. 1.

Comparison of the selection coefficients of transferred Salmonella orthologs measured in Escherichia coli with two different techniques: (y-axis) using individual competition experiments between each of the mutants and the wild type, measured using flow cytometry, and (x-axis) competing all mutants against each other at the same time and measuring the changes in their frequencies using HTS. Solid line is linear regression, F_{1, 42} = 461, r² = 0.92, P < 0.001, with a slope of 1.017. Dotted gray line is x = y. The imbedded plot shows the correlation when only neutral and nearly neutral genes are considered (s > − 0.1) (F_{1, 28} = 45.68, r² = 0.33, P < 0.001, slope 0.701).

Fig. 2.

Selection coefficients of the transferred genes in six different environments, with named examples of genes whose effect changes conditionally. Transferred genes are ranked by their selection coefficient in M9 environment. Colors indicate the six environments used in this study.

Fig. 3.

Gene-by-environment interaction is strongest for highly deleterious genes. Relationship between mean and standard deviation of selection coefficients of newly transferred genes over all environments. Solid line is the quadratic correlation (F_{2, 41} = 32.160, r² = 0.611, P < 0.001).

Fig. 4.

The shape and spread of DFEs is not affected by the environment. Selection coefficients of the transferred genes in six environments. (A) Lines connect genes measured in the same environment, and show the overall shape of the DFEs. Genes are ranked according to their selection coefficients in the environment that they were measured in. (B) Boxplot representation of DFEs, demonstrating that the average fitness effect of transferred genes changed between environments, even if the shape and spread of the DFEs did not. Letters a, b, and c indicate the three classes of DFEs, identified by the Wilcoxon signed ranks pairwise test.