Parallel Evolution Does Not Improve The Predictability of the Transcriptional Response to Heat Stress

Parallel evolution—the accumulation of similar changes in independently evolving populations—is seen as a sign of adaptation and can occur at different levels, from the genome to cellular phenotypes. However, it is unclear how parallel evolution cascades across levels, for example from genomes to transcriptomes. Microbes have been shown to adapt to changing environments through single mutations affecting the expression of hundreds to thousands of genes, which restored the transcriptomes to a less stressed state. Temperature being a complex stressor with a wide genomic basis of adaptation, such first-step mutations can introduce many beneficial gene expression changes at once. To investigate the effect of high-temperature-adaptation on the transcriptome of Pseudoalteromonas haloplanktis TAC125 (PhTAC125), a cold-adapted marine bacterium, we performed RNA-Seq of PhTAC125 and five evolved clones from an earlier evolution experiment at temperatures across their thermal range. Surprisingly, we did not find that high-temperature-adaptation reduced the levels of stress in the transcriptome with evolved clones showing only slightly reduced heat shock responses. This is consistent with the fact that the upper thermal limit of the evolved clones is only 1 °C above the limit of PhTAC125. At the same time and despite the high levels of parallel genome evolution observed in the previous evolution experiment, we did not find parallel transcriptome evolution. Taken together, our findings show that while genomes and the resulting growth phenotypes can evolve in parallel, the same must not be true for intermediate phenotypic levels such as the transcriptome.