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 α-proteobacterium, a transcriptional response to the reactive oxygen species singlet oxygen (1O2) is controlled by the group IV σ factor σE and the anti-σ factor ChrR. In this study, we integrated various large datasets to identify genes within the 1O2 stress response that contain σE-dependent promoters both within R. sphaeroides and across the bacterial phylogeny. Transcript pattern clustering and a σE-binding sequence model were used to predict candidate promoters that respond to 1O2 stress in R. sphaeroides. These candidate promoters were experimentally validated to nine R. sphaeroides σE-dependent promoters that control the transcription of 15 1O2-activated genes. Knowledge of the R. sphaeroides response to 1O2 and its regulator σE–ChrR was combined with large-scale phylogenetic and sequence analyses to predict the existence of a core set of approximately eight conserved σE-dependent genes in α-proteobacteria and γ-proteobacteria. The bacteria predicted to contain this conserved response to 1O2 include photosynthetic species, as well as free-living and symbiotic/pathogenic nonphotosynthetic species. Our analysis also predicts that the response to 1O2 evolved within the time frame of the accumulation of atmospheric molecular oxygen on this planet.