Abstract

The ability of phototrophs to convert light into biological energy is critical for life on Earth. However, there can be deleterious consequences associated with this bioenergetic conversion, including the production of toxic byproducts. For example, singlet oxygen (1O2) can be formed during photosynthesis by energy transfer from excited triplet-state chlorophyll pigments to O2. By monitoring gene expression and growth in the presence of 1O2, we show that the phototrophic bacterium Rhodobacter sphaeroides mounts a transcriptional response to this reactive oxygen species (ROS) that requires the alternative sigma factor, sigma(E). An increase in sigma(E) activity is seen when cells are exposed to 1O2 generated either by photochemistry within the photosynthetic apparatus or the photosensitizer, methylene blue. Wavelengths of light responsible for the generating triplet-state chlorophyll pigments in the photosynthetic apparatus are sufficient for a sustained increase in sigma(E) activity. Continued exposure to 1O2 is required to maintain this transcriptional response, and other ROS do not cause a similar increase in sigma(E)-dependent gene expression. When a sigma(E) mutant produces low levels of carotenoids, 1O2 is bacteriocidal, suggesting that this response is essential for protecting cells from this ROS. In addition, global gene expression analysis identified approximately 180 genes (approximately 60 operons) whose RNA levels increase > or = 3-fold in cells with increased sigma(E) activity. Gene products encoded by four newly identified sigma(E)-dependent operons are predicted to be involved in stress response, protecting cells from 1O2 damage, or the conservation of energy.