The genetic architecture underlying nematode responses to grassland soil bacteria and its effects on fitness

Background/Question/Methods

Soil nematode communities are important components of the micro fauna in grassland ecosystems and their interaction with soil microbes affects important ecological processes such as decomposition and nutrient recycling. To study genetic mechanisms underlying ecologically important traits involved in the response of nematode communities to soil microbes, we employed genomic tools available for the model nematode, Caenorhabditis elegans. We used transcriptional profiling to identify genes that were differentially expressed in response to different soil bacteria.  Some bacteria can be poor quality food and also be pathogenic to nematodes, thus represent a significant stress. We used available mutations for some of these genes to determine the functional consequences the loss of gene function on the nematode responses. We asked two questions:  1) What were the effects of the mutations in these genes on fitness, in particular when exposed to stressful bacteria?  2) Although transcriptional profiling studies can identify genes that are differentially regulated in response to environmental stimuli, how the expressed genes provide functional specificity to a particular environment remains largely unknown.  

Results/Conclusions

We compared the relative fitness of strains bearing these mutations across bacterial environments and found that the deleterious effects of many mutations were alleviated in the presence of stressful bacteria. We defined a bacteria to be stressful if the fitness of wild-type C. elegans was reduced when compared other benign strains. We compared fitness in the presence of the laboratory standard bacterium, E. coli OP50 and a strain of Bacillus megaterium and a Pseudomonas sp. most similar to P. florescens, both isolated from Tallgrass prairie soils. We found B. megaterium to be the most stressful and Pseudomonas sp. to be benign, with E. coli being intermediate. Specifically, we found that mutations in 14/35 genes tested lead to increased fitness in the presence of B. megaterium as compared to Pseudomonas sp. We then used survivorship as an indicator of the negative effects of bacteria on the nematode using the same benign and stressful bacteria. We found that genes had both bacteria-specific and bacteria-shared responses. We then analyzed double mutant strains and found bacteria-specific genetic interaction effects. Together our studies suggest that plasticity in gene interactions and their environment-specific modulation have important implications for host phenotypic differentiation and adaptation to changing environments.