Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development.
PpsR from the anoxygenic phototrophic bacterium Rhodobacter sphaeroides has been known as an oxygen- and light-dependent repressor of bacteriochlorophyll and carotenoid biosynthesis genes and puc operons involved in photosystem development. However, the putative PpsR-binding sites, TGTN12ACA, are also located upstream of numerous nonphotosystem genes, thus raising the possibility that the role of PpsR is broader. To characterize the PpsR regulon, transcriptome profiling was performed on the wild-type strain grown at high and low oxygen tensions, on the strain overproducing PpsR, and on the ppsR mutant. Transcriptome analysis showed that PpsR primarily regulates photosystem genes; the consensus PpsR binding sequence is TGTcN10gACA (lowercase letters indicate lesser conservation); the presence of two binding sites is required for repression in vivo. These findings explain why numerous single TGTN12ACA sequences are nonfunctional. In addition to photosystem genes, the hemC and hemE genes involved in the early steps of tetrapyrrole biosynthesis were identified as new direct targets of PpsR repression. Unexpectedly, PpsR was found to indirectly repress the puf and puhA operons encoding photosystem core proteins. The upstream regions of these operons contain no PpsR binding sites. Involvement in regulation of these operons suggests that PpsR functions as a master regulator of photosystem development. Upregulation of the puf and puhA operons that resulted from ppsR inactivation was sufficient to restore the ability to grow phototrophically to the prrA mutant. PrrA, the global redox-dependent activator, was previously considered indispensable for phototrophic growth. It is revealed that the PrrBA and AppA-PpsR systems, believed to work independently, in fact interact and coordinately regulate photosystem development.
Moskvin
Oleg V
OV
Department of Molecular Biology, University of Wyoming, Laramie, WY 82071, USA.
Gomelsky
Larissa
L
Gomelsky
Mark
M
D001426:Bacterial Proteins / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics*; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D020411:Oligonucleotide Array Sequence Analysis; D010100:Oxygen / Q000378:metabolism; D010788:Photosynthesis / Q000235:genetics*; D018085:Regulon / Q000235:genetics; D012097:Repressor Proteins / Q000235:genetics*; D012242:Rhodobacter sphaeroides / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism*; D014158:Transcription, Genetic / Q000235:genetics*
D001426:Bacterial Proteins; D004268:DNA-Binding Proteins; D012097:Repressor Proteins; D010100:Oxygen
J Bacteriol. 2001 Dec;183(24):7371-80
11717296
Mol Microbiol. 2002 Aug;45(3):827-36
12139627
J Biol Chem. 2004 Mar 5;279(10):9146-55
14662761
J Biol Chem. 1995 Sep 1;270(35):20453-8
7657621
J Biol Chem. 1998 Nov 13;273(46):30762-9
9804853
Cell Mol Life Sci. 2004 Feb;61(4):417-36
14999403
J Bacteriol. 1994 May;176(10):2869-76
8188588
Mol Gen Genet. 1989 Jul;218(1):1-12
2550757
J Biol Chem. 1998 Dec 25;273(52):35319-25
9857073
J Biol Chem. 1997 Jul 18;272(29):18391-6
9218481
J Bacteriol. 2000 Apr;182(8):2253-61
10735869
J Bacteriol. 2000 Jun;182(11):3081-7
10809685
J Bacteriol. 1994 Jan;176(1):32-43
8282708
J Biol Chem. 2002 Apr 26;277(17):14363-6
11882647
J Bacteriol. 1997 Jan;179(1):128-34
8981989
Photosynth Res. 2001;70(1):19-41
16228360
J Biol Chem. 1995 Sep 8;270(36):21167-75
7673149
Microbiol Mol Biol Rev. 2004 Jun;68(2):263-79
15187184
J Bacteriol. 2004 Jul;186(14):4748-58
15231807
J Bacteriol. 1995 Aug;177(16):4609-18
7642486
J Bacteriol. 1996 Feb;178(4):985-93
8576072
J Bacteriol. 2004 May;186(10):3133-42
15126475
Genome Res. 2004 Jun;14(6):1188-90
15173120
J Mol Biol. 2004 Sep 24;342(4):1171-86
15351643
Gene. 1988 Oct 15;70(1):191-7
2853689
Microbiology. 2004 Mar;150(Pt 3):697-706
14993319
Cell. 2002 Sep 6;110(5):613-23
12230978
Nature. 2002 May 9;417(6885):202-5
12000965
Microbiology. 2003 Feb;149(Pt 2):377-88
12624200
Proc Natl Acad Sci U S A. 2004 Aug 17;101(33):12306-11
15292515
J Cell Physiol. 1957 Feb;49(1):25-68
13416343
J Biol Chem. 1998 Nov 13;273(46):30757-61
9804852
Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):147-53; discussion 153-4
12594923
Biochemistry. 2003 Jun 10;42(22):6726-34
12779327
J Bacteriol. 2003 Oct;185(20):6171-84
14526029
Photochem Photobiol. 2003 Sep;78(3):290-7
14556317
Trends Biochem Sci. 2002 Oct;27(10):497-500
12368079
Mol Gen Genet. 1991 Sep;228(3):433-44
1896013
Nucleic Acids Res. 2000 Feb 15;28(4):862-7
10648776
J Bacteriol. 2004 Nov;186(22):7726-35
15516587
J Bacteriol. 1995 Mar;177(6):1634-7
7883723
Nucleic Acids Res. 2003 Feb 15;31(4):e15
12582260
Antonie Van Leeuwenhoek. 1994;66(1-3):151-64
7747929
Nucleic Acids Res. 2002 May 15;30(10):e48
12000853