Temperature-Induced Transcriptional Responses of a Deep-Biosphere Bacterium Illuminate its Adaptation to Growth from 20oC to 79oC

Temperature affects cell function and survival. Most organisms are adapted to growing within a temperature range that rarely exceeds ~ 30°C, but the anaerobic thermophilic bacterium Kosmotoga olearia TBF 19.5.1 (phylum Thermotogae) is capable of growing over an extremely wide temperature range (20°C-79°C). We used transcriptomic and comparative genomic analyses to elucidate the mechanisms enabling this extraordinary trait. When growth of K. olearia at 30°C, 40°C, and 77°C was compared to its optimal growth at 65°C, 573 of 2,224 genes (25%) were significantly differentially expressed. We find that K. olearia remodels its metabolism significantly at different temperatures, with increased expression of genes involved in energy and carbohydrate metabolism at high temperatures and up-regulation of amino acid metabolism at lower temperatures. At sub-optimal temperatures, many transcriptional changes were similar to those observed in mesophilic bacteria at physiologically low temperatures, including up-regulation of genes encoding enzymes for fatty acid synthesis, typical cold stress genes, and ribosomal proteins. In comparison to other Thermotogae, K. olearia has multiple copies of some cold-associated genes, suggesting that an increase in gene copy number is a strategy for cold adaptation. Many of these cold response genes were likely acquired by lateral gene transfer, highlighting the role of gene exchange in bacterial thermoadaptation. Notably, at 77°C a large number of the up-regulated genes encode proteins with hypothetical functions, indicating that many features of adaptations to high temperature growth are still unknown. Ambient temperature change is a physiological challenge faced by all living organisms. Manipulating laboratory cultures of Kosmotoga olearia, a bacterium with an extraordinarily wide growth temperature range (20°C to 79°C), we investigated differences in gene expression across its growth range. We found that changes in temperature affect expression of about one quarter of K. olearia genes, including many regulatory genes, which in turn elicits re-modeling of the cellular membrane and changes in metabolism. A large fraction of the temperature-responsive genes, however, are functionally uncharacterized. Many of K. olearia's genes needed for low temperature growth may have been acquired from mesophilic microorganisms, suggesting that K. olearia's thermophilic ancestors expanded their ecological niche via lateral gene transfer.