The Vitamin B12-Dependent Photoreceptor AerR Relieves Photosystem Gene Repression by Extending the Interaction of CrtJ with Photosystem Promoters.
Purple nonsulfur bacteria adapt their physiology to a wide variety of environmental conditions often through the control of transcription. One of the main transcription factors involved in controlling expression of theRhodobacter capsulatusphotosystem is CrtJ, which functions as an aerobic repressor of photosystem genes. Recently, we reported that a vitamin B12binding antirepressor of CrtJ called AerR is required for anaerobic expression of the photosystem. However, the mechanism whereby AerR regulates CrtJ activity is unclear. In this study, we used a combination of next-generation sequencing and biochemical methods to globally identify genes under control of CrtJ and the role of AerR in controlling this regulation. Our results indicate that CrtJ has a much larger regulon than previously known, with a surprising regulatory function under both aerobic and anaerobic photosynthetic growth conditions. A combination ofin vivochromatin immunoprecipitation-DNA sequencing (ChIP-seq) and ChIP-seq and exonuclease digestion (ChIP-exo) studies andin vitrobiochemical studies demonstrate that AerR forms a 1:2 complex with CrtJ (AerR-CrtJ2) and that this complex binds to many promoters under photosynthetic conditions. The results ofin vitroandin vivoDNA binding studies indicate that AerR-CrtJ2anaerobically forms an extended interaction with the bacteriochlorophyllbchCpromoter to relieve repression by CrtJ. This is contrasted by aerobic growth conditions where CrtJ alone functions as an aerobic repressor ofbchCexpression. These results indicate that the DNA binding activity of CrtJ is modified by interacting with AerR in a redox-regulated manner and that this interaction alters CrtJ's function.IMPORTANCEPhotoreceptors control a wide range of physiology often by regulating downstream gene expression in response to light absorption via a bound chromophore. Different photoreceptors are known to utilize a number of different compounds for light absorption, including the use of such compounds as flavins, linearized tetrapyrroles (bilins), and carotenoids. Recently, a novel class of photoreceptors that use vitamin B12(cobalamin) as a blue-light-absorbing chromophore have been described. In this study, we analyzed the mechanism by which the vitamin B12binding photoreceptor AerR controls the DNA binding activity of the photosystem regulator CrtJ. This study shows that a direct interaction between the vitamin B12binding photoreceptor AerR with CrtJ modulates CrtJ binding to DNA and importantly, the regulatory outcome of gene expression, as shown here with photosystem promoters.
Molecular and Cellular Biochemistry Department, Indiana University, Bloomington, Indiana, USA.
Mingxu
M
Fang
Molecular and Cellular Biochemistry Department, Indiana University, Bloomington, Indiana, USA bauer@indiana.edu.
Carl E
CE
Bauer
D000332:Aerobiosis; D000693:Anaerobiosis; D001426:Bacterial Proteins / Q000378:metabolism*; D047369:Chromatin Immunoprecipitation; D004269:DNA, Bacterial / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000378:metabolism*; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D059014:High-Throughput Nucleotide Sequencing; D020283:Photoreceptors, Microbial / Q000378:metabolism*; D011401:Promoter Regions, Genetic; D011485:Protein Binding; D016354:Rhodobacter capsulatus / Q000235:genetics*; D014157:Transcription Factors / Q000378:metabolism*; D014805:Vitamin B 12 / Q000378:metabolism*
D001426:Bacterial Proteins; C107183:CrtJ protein, Rhodobacter; D004269:DNA, Bacterial; D004268:DNA-Binding Proteins; D020283:Photoreceptors, Microbial; D014157:Transcription Factors; D014805:Vitamin B 12
PpsR ortholog; global transcription factor; photoreceptor; redox regulation; transcriptional regulation; transcriptomics