Organization and evolution of the biological response to singlet oxygen stress

The appearance of atmospheric oxygen from photosynthetic activity led to the evolution of aerobic respiration and responses to the resulting reactive oxygen species. In Rhodobacter sphaeroides, a photosynthetic alpha-proteobacterium, a transcriptional response to the reactive oxygen species singlet oxygen ((1)O(2)) is controlled by the group IV sigma factor sigma(E) and the anti-sigma factor ChrR. In this study, we integrated various large datasets to identify genes within the (1)O(2) stress response that contain sigma(E)-dependent promoters both within R. sphaeroides and across the bacterial phylogeny. Transcript pattern clustering and a sigma(E)-binding sequence model were used to predict candidate promoters that respond to (1)O(2) stress in R. sphaeroides. These candidate promoters were experimentally validated to nine R. sphaeroides sigma(E)-dependent promoters that control the transcription of 15 (1)O(2)-activated genes. Knowledge of the R. sphaeroides response to (1)O(2) and its regulator sigma(E)-ChrR was combined with large-scale phylogenetic and sequence analyses to predict the existence of a core set of approximately eight conserved sigma(E)-dependent genes in alpha-proteobacteria and gamma-proteobacteria. The bacteria predicted to contain this conserved response to (1)O(2) include photosynthetic species, as well as free-living and symbiotic/pathogenic nonphotosynthetic species. Our analysis also predicts that the response to (1)O(2) evolved within the time frame of the accumulation of atmospheric molecular oxygen on this planet.