A Singular Bacteriophytochrome Acquired by Lateral Gene Transfer

Jaubert, Marianne; Lavergne, Jérôme; Fardoux, Joël; Hannibal, Laure; Vuillet, Laurie; Adriano, Jean-Marc; Bouyer, Pierre; Pignol, David; Giraud, Éric; Vermeglio, André

doi:10.1074/jbc.m611173200

Cited by 31 publications

(46 citation statements)

References 32 publications

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“…The two exceptions are the above-mentioned BphP3 from Bradyrhizobium ORS 278, which binds PCB as a natural chromophore (15), and RpBphP4 from R. palustris CGA009, which does not incorporate a chromophore (42).…”

Section: Resultsmentioning

confidence: 99%

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Bathy Phytochromes in Rhizobial Soil Bacteria

2010

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Phytochromes are biliprotein photoreceptors that are found in plants, bacteria, and fungi. Prototypical phytochromes have a Pr ground state that absorbs in the red spectral range and is converted by light into the Pfr form, which absorbs longer-wavelength, far-red light. Recently, some bacterial phytochromes have been described that undergo dark conversion of Pr to Pfr and thus have a Pfr ground state. We show here that such so-called bathy phytochromes are widely distributed among bacteria that belong to the order Rhizobiales. We measured in vivo spectral properties and the direction of dark conversion for species which have either one or two phytochrome genes. Agrobacterium tumefaciens C58 contains one bathy phytochrome and a second phytochrome which undergoes dark conversion of Pfr to Pr in vivo. The related species Agrobacterium vitis S4 contains also one bathy phytochrome and another phytochrome with novel spectral properties. Rhizobium leguminosarum 3841, Rhizobium etli CIAT652, and Azorhizobium caulinodans ORS571 contain a single phytochrome of the bathy type, whereas Xanthobacter autotrophicus Py2 contains a single phytochrome with dark conversion of Pfr to Pr. We propose that bathy phytochromes are adaptations to the light regime in the soil. Most bacterial phytochromes are light-regulated histidine kinases, some of which have a C-terminal response regulator subunit on the same protein. According to our phylogenetic studies, the group of phytochromes with this domain arrangement has evolved from a bathy phytochrome progenitor.

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Section: Resultsmentioning

confidence: 99%

“…BphP3 from the Bradyrhizobium strain ORS 278 is an exception among bacteriophytochromes as it binds PCB as a natural chromophore. This phytochrome adopts a so-called Po (P-orange) ground state with an absorbance maximum in the orange range (11,15). Upon irradiation, this phytochrome converts into the Pr form.…”

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confidence: 99%

Bathy Phytochromes in Rhizobial Soil Bacteria

2010

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“…However, the light induction factor of LAPD is virtually the same as for cGMP activation of the parent receptor HsPDE2A, implying that meaningful physiological effects could still be elicited. Furthermore, with the basic design rule for red-light-regulated PDEs now established, other variants with different, possibly improved properties can readily be engineered [e.g., by introducing mutations that modulate Pr↔Pfr photochemistry (42), by resorting to BPhys with favorable characteristics (43), by replacing the effector with other PDE domains]. More generally, LAPD exemplifies that not only plant phytochromes (44) but also bacterial phytochromes constitute powerful building blocks in the engineering of novel optogenetic actuators (45).…”

Section: Discussionmentioning

confidence: 99%

Engineering of a red-light–activated human cAMP/cGMP-specific phosphodiesterase

Gasser¹,

Taiber

Yeh

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

158

161

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Significance Sensory photoreceptors not only enable organisms to derive spatial and temporal cues from incident light but also provide the basis for optogenetics, which denotes the manipulation by light of living systems with supreme spatial and temporal resolution. To expand the scope of optogenetics, we have engineered the light-activated phosphodiesterase LAPD, which degrades the ubiquitous second messengers cAMP and cGMP in a red-light–stimulated manner. Both cAMP and cGMP are key to the regulation of manifold physiological responses, and LAPD now augurs red-light control over these processes. As we demonstrate for two eukaryotic systems, LAPD does not require any additional exogenous factors, and thus permits the light perturbation of living cells in hitherto unrealized ways.

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“…P r is commonly the thermally stable dark state for both classes of phytochromes, with P fr exhibiting slow thermal reversion to P r (dark reversion). However, a small subset of biliverdin phytochromes, known as bathyphytochromes, have large amounts of P fr at thermal equilibrium (9-11), and rare cases of atypical wavelength sensitivity have also been reported (12,13). Such photosensory diversity suggests that rare divergent photochemical mechanisms have evolved, but most phytochromes retain spectrally characteristic P r and P fr states and hence are thought to share common P r and P fr structural features.…”

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confidence: 99%

Distinct classes of red/far-red photochemistry within the phytochrome superfamily

Rockwell

Shang

Martin

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

133

209

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Phytochromes are a widespread family of photosensory proteins first discovered in plants, which measure the ratio of red to far-red light to control many aspects of growth and development. Phytochromes interconvert between red-absorbing Pr and far-redabsorbing Pfr states via photoisomerization of a covalently-bound linear tetrapyrrole (bilin) chromophore located in a conserved photosensory core. From recent crystal structures of this core region, it has been inferred that the chromophore structures of Pr and Pfr are conserved in most phytochromes. Using circular dichroism spectroscopy and ab initio calculations, we establish that the Pfr states of the biliverdin-containing bacteriophytochromes DrBphP and PaBphP are structurally dissimilar from those of the phytobilincontaining cyanobacterial phytochrome Cph1. This conclusion is further supported by chromophore substitution experiments using semisynthetic bilin monoamides, which indicate that the propionate side chains perform different functional roles in the 2 classes of phytochromes. We propose that different directions of bilin D-ring rotation account for these distinct classes of red/far-red photochemistry.bilin amides ͉ biliprotein ͉ circular dichroism ͉ photoisomerization P hytochromes comprise a class of red/far-red biliprotein photoreceptors that regulate photomorphogenesis, shade avoidance, and development in higher plants (1, 2). Also found in bacteria and fungi, phytochromes characteristically photoconvert between red-absorbing P r and far-red-absorbing P fr states (3,4). Conversion between these 2 states involves Z/E photoisomerization of the 15/16 double bond of their linear tetrapyrrole (bilin) chromophores. Photosensory signaling by phytochromes relies on a conserved core comprising PAS (PER, ARNT, SIM), GAF (cGMP phosphodiesterase, adenylate cyclase, FhlA), and PHY (phytochrome-specific GAF-related) domains (5), with the bilin bound within a conserved pocket of the GAF domain (1, 6). The precise structure of the bilin chromophore, the nature of its covalent linkage to cysteine (Cys) side chains in the protein, and the location of those Cys residues vary among phytochromes (7), and 2 distinct subclasses can be distinguished on these grounds.Phytobilin-containing phytochromes, which include the plant (Phys) and cyanobacterial (Cph1) phytochromes, are found exclusively in oxygenic photosynthetic organisms. The chromophore precursor for these phytochromes is either phytochromobilin or phycocyanobilin (PCB), both of which possess reduced ethylidene-containing A-rings. For these phytochromes, covalent linkage forms between a GAF-domain Cys and the ␣-carbon of the A-ring ethylidene (Fig. S1 A). The much more widespread biliverdin-containing phytochromes (4), which include the bacteriophytochromes (BphPs) and fungal phytochromes, possess covalent linkages between a Cys residue upstream of the PAS domain and the ␤-carbon of the A-ring endo-vinyl group of biliverdin IX␣ (BV; Fig. S1B) (8). P r is commonly the thermally stable dark state for both classes of...

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A Singular Bacteriophytochrome Acquired by Lateral Gene Transfer

Cited by 31 publications

References 32 publications

Bathy Phytochromes in Rhizobial Soil Bacteria

Bathy Phytochromes in Rhizobial Soil Bacteria

Engineering of a red-light–activated human cAMP/cGMP-specific phosphodiesterase

Distinct classes of red/far-red photochemistry within the phytochrome superfamily

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