With the post-genomic era came a dramatic increase in high-throughput technologies, of which transcriptional profiling by microarrays was one of the most popular. One application of this technology is to identify genes that are differentially expressed in response to different environmental conditions. These experiments are constructed under the assumption that the differentially expressed genes are functionally important in the environment where they are induced. However, whether differential expression is predictive of functional importance has yet to be tested. Here we have addressed this expectation by employing Caenorhabditis elegans as a model for the interaction of native soil nematode taxa and soil bacteria. Using transcriptional profiling, we identified candidate genes regulated in response to different bacteria isolated in association with grassland nematodes or from grassland soils. Many of the regulated candidate genes are predicted to affect metabolism and innate immunity suggesting similar genes could influence nematode community dynamics in natural systems. Using mutations that inactivate 21 of the identified genes, we showed that most contribute to lifespan and/or fitness in a given bacterial environment. Although these bacteria may not be natural food sources for C. elegans, we show that changes in food source, as can occur in environmental disturbance, can have a large effect on gene expression, with important consequences for fitness. Moreover, we used regression analysis to demonstrate that for many genes the degree of differential gene expression between two bacterial environments predicted the magnitude of the effect of the loss of gene function on life history traits in those environments.
Transcriptional profiling is often used to identify genes that are differentially regulated in response to different environments. These experiments assume that genes differentially expressed in response to different environments are functionally important and, furthermore, that the degree of differential gene expression is predictive of the magnitude of functional importance. In genetic experiments, function is inferred from analyzing the phenotypes of removing, reducing or altering gene function. However, to date, there has not been a specific test of how well the degree of differential gene expression between two (or more) environments is predictive of gene function. Here we identified C. elegans genes that were differentially expressed in response to different bacterial environments and determined the phenotypic differences of life history traits between these environments using mutant strains that compromised gene function. We found that differential gene expression is indeed predictive of functional importance of the identified genes in different environments. This observation has important implications for interpreting the results of transcriptional profiling experiments of populations of organisms in their native environments, where in many cases the genetic tools to disrupt gene function have not yet been fully developed or interfering with gene functions in nature may not be feasible.