The Photoheterotroph Dokdonia sp. MED134 Modulates the Expression of Resource Acquisition and Anaplerotic Carbon Fixation Pathways in Response to Temperature

Abstract

Temperature has an overriding impact on microbial physiology, but the molecular basis of thermal acclimation in many ecologically relevant marine bacterial taxa remains unexplored. We used quantitative transcriptomics to analyse the transcriptional reprogramming of a proteorhodopsin-based photoheterotroph, Dokdonia sp. MED134, during thermal acclimation from 10°C to 34°C. Temperature significantly impacted the expression of most MED134 genes (84%). Marker genes of the general stress response were induced towards cold temperature (10°C). Conversely, highly expressed genes associated with DNA replication and resource acquisition, like TonB-dependent transporters and gliding motility genes, were upregulated towards warm temperatures along this thermal range, when growth rates were fast. The mRNA transcript abundance of most genes related to the TCA cycle was not differentially expressed by temperature. By contrast, the expression of genes associated with anaplerotic carbon fixation was significantly enhanced at the optimum growth temperature (25°C). The expression of the proteorhodopsin was minimum at 10°C, and its regulation by light was impaired at 34°C, suggesting regulatory imbalances in this key phototrophic gene under supra-optimal warm conditions. Our findings highlight potential implications of growth temperature for regulating mechanisms of nutrient and energy acquisition, as well as the intracellular carbon flux in globally abundant marine photoheterotrophs.