Probing the cellular pathways governing aerobic anoxygenic phototrophy

Heterotrophic bacteria have evolved multiple strategies for using light energy to supplement their respiratory metabolism. One strategy, aerobic anoxygenic phototrophy (AAnP), is widespread in aquatic proteobacteria. It has been hypothesized that this pathway provides a growth advantage under conditions of organic carbon limitation, but the molecular network connecting AAnP to cell physiology and metabolism has not been characterized. Here we present our findings from three complementary approaches in the model organism Erythrobacter longus: 1) growth physiology of strains deficient in light harvesting and carbon assimilation pathways, 2) global fitness profiling of transposon mutant libraries to discover new genetic connections between carbon metabolism and photophysiology, and 3) quantitative proteomics and transcriptomics over a day-night cycle. Our findings show that the availability of carbon substrates and light interact to control the production of bacteriochlorophyll a, the major photosynthetic pigment in E. longus. Light enhanced the growth of wild-type E. longus cells grown on pyruvate, butyrate, and glucose, but not on a complex rich medium, and this growth advantage was bacteriochlorophyll a-dependent. Over the diel cycle, bacteriochlorophyll a production, along with expression of photosynthesis-related pathways, was strongly periodic in complex rich medium, but much less so on glucose and butyrate. Finally, our transposon mutagenesis approach identified candidate regulatory genes that may play key roles in governing AAnP expression. Together, our genetics, physiology, and global gene expression profiling results shed new light on a widespread and ecologically important metabolic strategy in aquatic systems.