Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: photoconversion and signal transduction.
Phytochromes are red-light photoreceptors that regulate light responses in plants, fungi, and bacteria via reversible photoconversion between red (Pr) and far-red (Pfr) light-absorbing states. Here we report the crystal structure at 2.9 A resolution of a bacteriophytochrome from Pseudomonas aeruginosa with an intact, fully photoactive photosensory core domain in its dark-adapted Pfr state. This structure reveals how unusual interdomain interactions, including a knot and an "arm" structure near the chromophore site, bring together the PAS (Per-ARNT-Sim), GAF (cGMP phosphodiesterase/adenyl cyclase/FhlA), and PHY (phytochrome) domains to achieve Pr/Pfr photoconversion. The PAS, GAF, and PHY domains have topologic elements in common and may have a single evolutionary origin. We identify key interactions that stabilize the chromophore in the Pfr state and provide structural and mutational evidence to support the essential role of the PHY domain in efficient Pr/Pfr photoconversion. We also identify a pair of conserved residues that may undergo concerted conformational changes during photoconversion. Modeling of the full-length bacteriophytochrome structure, including its output histidine kinase domain, suggests how local structural changes originating in the photosensory domain modulate interactions between long, cross-domain signaling helices at the dimer interface and are transmitted to the spatially distant effector domain, thereby regulating its histidine kinase activity.
Yang
Xiaojing
X
Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL 60637, USA. xiaojingyang@uchicago.edu
Kuk
Jane
J
Moffat
Keith
K
D001426:Bacterial Proteins / Q000737:chemistry / Q000378:metabolism; D008958:Models, Molecular; D010777:Photochemistry; D010834:Phytochrome / Q000737:chemistry* / Q000378:metabolism*; D017434:Protein Structure, Tertiary; D011550:Pseudomonas aeruginosa / Q000737:chemistry*; D015398:Signal Transduction
D001426:Bacterial Proteins; D010834:Phytochrome
J Biol Chem. 2005 Sep 16;280(37):32389-97
16009707
Proc Natl Acad Sci U S A. 2007 Jul 24;104(30):12571-6
17640891
Methods Enzymol. 1997;276:523-30
9048379
Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21
9757107
Annu Rev Plant Biol. 2006;57:837-58
16669784
Biochemistry. 2007 Jan 16;46(2):416-23
17209552
Nature. 2002 May 9;417(6885):202-5
12000965
Acc Chem Res. 2007 Apr;40(4):258-66
17279729
FEBS J. 2005 Apr;272(8):1927-36
15819886
J Biol Chem. 2008 May 2;283(18):12212-26
18192276
Biol Direct. 2006 Sep 05;1:25
16953892
Nature. 2005 Nov 17;438(7066):325-31
16292304
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2807-12
12604773
Biochemistry. 2005 Nov 22;44(46):15203-15
16285723
Eur J Hum Genet. 2000 Jun;8(6):399-406
10878659
Trends Plant Sci. 2002 Aug;7(8):357-66
12167331
Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11628-33
12186972
Biochemistry. 2000 Nov 7;39(44):13487-95
11063585
Biophys J. 2006 Sep 1;91(5):1811-22
16751241
Plant Cell. 2006 Jan;18(1):4-14
16387836
J Biol Chem. 2001 Nov 2;276(44):41182-90
11493605
J Am Chem Soc. 2007 Jan 10;129(1):126-32
17199291
Mol Microbiol. 1993 May;8(3):435-41
8326858
EMBO J. 2005 Dec 21;24(24):4247-59
16319927
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2184-95
15572771
Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11057-61
1662380
Methods Enzymol. 1997;276:307-26
27754618
J Biol Chem. 2005 Jul 1;280(26):24491-7
15878872
Plant Cell. 2004 Aug;16(8):2104-16
15273294
Chemphyschem. 2007 Aug 6;8(11):1657-63
17614346
Acta Crystallogr D Biol Crystallogr. 2001 Oct;57(Pt 10):1373-82
11567148
J Biol Chem. 2005 Oct 7;280(40):34358-64
16061486
Curr Biol. 1997 Nov 1;7(11):R674-7
9382818
Trends Biochem Sci. 1997 Dec;22(12):458-9
9433123
J Biol Chem. 2007 Apr 20;282(16):12298-309
17322301
Semin Cell Dev Biol. 2000 Dec;11(6):449-56
11145874
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
15572765
J Mol Biol. 2006 Dec 8;364(4):655-66
17027028
Proc Natl Acad Sci U S A. 2004 Dec 14;101(50):17334-9
15548612
Methods Enzymol. 1997;276:472-494
27799110
Acta Crystallogr D Biol Crystallogr. 2002 Nov;58(Pt 11):1948-54
12393927
Proc Natl Acad Sci U S A. 2008 Aug 5;105(31):10709-14
18667691
J Biol Chem. 2006 Sep 22;281(38):28162-73
16803878