Redox Regulation of a Light-Harvesting Antenna Complex in an Anoxygenic Phototroph

ABSTRACT The purple nonsulfur bacterium Rhodopseudomonas palustris is a model for understanding how a phototrophic organism adapts to changes in light intensity because it produces different light-harvesting (LH) complexes under high light (LH2) and low light intensities (LH3 and LH4). Outside of this change in the composition of the photosystem, little is understood about how R. palustris senses and responds to low light intensity. On the basis of the results of transcription analysis of 17 R. palustris strains grown in low light, we found that R. palustris strains downregulate many genes involved in iron transport and homeostasis. The only operon upregulated in the majority of R. palustris exposed to low light intensity was pucBAd, which encodes LH4. In previous work, pucBAd expression was shown to be modulated in response to light quality by bacteriophytochromes that are part of a low-light signal transduction system. Here we found that this signal transduction system also includes a redox-sensitive protein, LhfE, and that its redox sensitivity is required for LH4 synthesis in response to low light. Our results suggest that R. palustris upregulates its LH4 system when the cellular redox state is relatively oxidized. Consistent with this, we found that LH4 synthesis was upregulated under high light intensity when R. palustris was grown semiaerobically or under nitrogen-fixing conditions. Thus, changes in the LH4 system in R. palustris are not dependent on light intensity per se but rather on cellular redox changes that occur as a consequence of changes in light intensity. IMPORTANCE An essential aspect of the physiology of phototrophic bacteria is their ability to adjust the amount and composition of their light-harvesting apparatus in response to changing environmental conditions. The phototrophic purple bacterium R. palustris adapts its photosystem to a range of light intensities by altering the amount and composition of its peripheral LH complexes. Here we found that R. palustris regulates its LH4 complex in response to the cellular redox state rather than in response to light intensity per se. Relatively oxidizing conditions, including low light, semiaerobic growth, and growth under nitrogen-fixing conditions, all stimulated a signal transduction system to activate LH4 expression. By understanding how LH composition is regulated in R. palustris, we will gain insight into how and why a photosynthetic organism senses and adapts its photosystem to multiple environmental cues.