Transcriptional response of the photoheterotrophic marine bacterium Dinoroseobacter shibae to changing light regimes

Abstract

Bacterial aerobic anoxygenic photosynthesis (AAP) is an important mechanism of energy generation in aquatic habitats, accounting for up to 5% of the surface ocean's photosynthetic electron transport. We used Dinoroseobacter shibae, a representative of the globally abundant marine Roseobacter clade, as a model organism to study the transcriptional response of a photoheterotrophic bacterium to changing light regimes. Continuous cultivation of D. shibae in a chemostat in combination with time series microarray analysis was used in order to identify gene-regulatory patterns after switching from dark to light and vice versa. The change from heterotrophic growth in the dark to photoheterotrophic growth in the light was accompanied by a strong but transient activation of a broad stress response to the formation of singlet oxygen, an immediate downregulation of photosynthesis-related genes, fine-tuning of the expression of ETC components, as well as upregulation of the transcriptional and translational apparatus. Furthermore, our data suggest that D. shibae might use the 3-hydroxypropionate cycle for CO₂ fixation. Analysis of the transcriptome dynamics after switching from light to dark showed relatively small changes and a delayed activation of photosynthesis gene expression, indicating that, except for light other signals must be involved in their regulation. Providing the first analysis of AAP on the level of transcriptome dynamics, our data allow the formulation of testable hypotheses on the cellular processes affected by AAP and the mechanisms involved in light- and stress-related gene regulation.