Cyanobacterial Phytochrome-like PixJ1 Holoprotein Shows Novel Reversible Photoconversion Between Blue- and Green-absorbing Forms

Yoshihara, Shizue; Katayama, Mikio; Geng, Xiaoxing; Ikeuchi, Masahiko

doi:10.1093/pcp/pch214

Cited by 142 publications

(178 citation statements)

References 51 publications

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“…The cyanobacteriochrome domains contain 1 to 11 GAF domains. Except for those in Synechocystis PCC 6803 (37), Thermosynechococcus elongatus (38), Nostoc PCC 7120 (16), and N. punctiforme (39), cyanobacteriochrome domains in cyanobacterial strains have yet to be verified to bind a bilin chromophore and undergo reversible photoconversion. Only one other cyanobacterium, identified as "cyanobacterium PCC 7702," contains a ptx locus encoding homologous proteins, with identical genome context (36; see also the IMG database).…”

Section: Discussionmentioning

confidence: 99%

Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme

et al. 2015

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In cyanobacterial Nostoc species, substratum-dependent gliding motility is confined to specialized nongrowing filaments called hormogonia, which differentiate from vegetative filaments as part of a conditional life cycle and function as dispersal units. Here we confirm that Nostoc punctiforme hormogonia are positively phototactic to white light over a wide range of intensities. N. punctiforme contains two gene clusters (clusters 2 and 2i), each of which encodes modular cyanobacteriochrome-methyl-accepting chemotaxis proteins (MCPs) and other proteins that putatively constitute a basic chemotaxis-like signal transduction complex. Transcriptional analysis established that all genes in clusters 2 and 2i, plus two additional clusters (clusters 1 and 3) with genes encoding MCPs lacking cyanobacteriochrome sensory domains, are upregulated during the differentiation of hormogonia. Mutational analysis determined that only genes in cluster 2i are essential for positive phototaxis in N. punctiforme hormogonia; here these genes are designated ptx (for phototaxis) genes. The cluster is unusual in containing complete or partial duplicates of genes encoding proteins homologous to the well-described chemotaxis elements CheY, CheW, MCP, and CheA. The cyanobacteriochrome-MCP gene (ptxD) lacks transmembrane domains and has 7 potential binding sites for bilins. The transcriptional start site of the ptx genes does not resemble a sigma 70 consensus recognition sequence; moreover, it is upstream of two genes encoding gas vesicle proteins (gvpA and gvpC), which also are expressed only in the hormogonium filaments of N. punctiforme. Nearly half of unicellular and more than three-quarters of filamentous cyanobacteria in culture are motile by a gliding mechanism on a solid substratum (1). Gliding motility is a property that is rapidly lost during prolonged serial transfer in culture (2, 3, 4). In members of the nitrogen-fixing, heterocyst-forming cyanobacterial taxonomic subsection IV (Nostocales), gliding motility, if present, occurs either by vegetative filaments (in the genera Anabaena, Aphanizomenon, Cylindrospermum, and others) or exclusively by specifically differentiated filaments called hormogonia (in the genera Calothrix, Nostoc, Tolypothrix, and others) (5). Substratum-dependent gliding is much slower than flagellar swimming in suspension, ranging from 5 m/min in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 (6) to 18 m/min by vegetative filaments of the heterocyst-forming cyanobacterium Anabaena cylindrica (7), 60 m/min by hormogonium filaments of Nostoc cycadae (8), and 600 m/min by the filamentous non-heterocyst-forming cyanobacterium Oscillatoria princeps (9).Phototaxis is a behavioral characteristic of Bacteria, Archaea, and single-cell eukaryotes, as well as some animal larvae (10) that contain photoreceptors. It is a positive selective property for a phototrophic organism, allowing movement both toward higher light intensities for maximal photosynthetic activity and away from inhibitory high intensitie...

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Section: Discussionmentioning

confidence: 99%

Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme

et al. 2015

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“…Among other PatA-related proteins encoded by the Synechocystis genome are TaxP1 (PixG/ Sll0038) and PixE (Slr1693), both of which are located within phototaxis operons (5,6), and thus may share the same regulatory target(s) as LsiR. Similar to the CBCRs SyPixJ1, TePixJ, and Tlr0924 (15)(16)(17)(18), UirS possesses a dual-Cys-linked PVB chromophore whose photoactivation triggers conversion between UV (Puv) and green (Pg) light-absorbing states. Physiological analyses indicate that LsiR functions as a signal output regulator of avoidance movement of Synechocystis cells under unidirectional UV illumination.…”

Section: Discussionmentioning

confidence: 99%

“…A member of the CBCR photoreceptor family (11), UirS possesses three N-terminal transmembrane (TM) helices similar to those of the ethylene-binding domain of the Arabidopsis ethylene receptor ETR1 (12), along with two PAS domains, a CBCR GAF domain, and an H-box containing histidine kinase (HiK) domain at the C-terminal end (13). UirS belongs to a CBCR subfamily with two conserved Cys residues within its phycocyanobilin (PCB)-binding GAF domain (14), with other notable examples being Synechocystis SyPixJ/TaxD1/Sll0041 (5,15) and TePixJ/Tll0569 and Tlr0924 from Thermosynechococcus elongatus (14,16,17). Previous studies have shown that the region containing TM helices is responsible for ethylene binding in UirS (12), whereas its GAF domain can bind to the linear tetrapyrrole PCB to yield a violet/green light-switchable CBCR (18).…”

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confidence: 99%

Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803

Song

Cho

et al. 2011

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

149

238

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Positive phototaxis systems have been well studied in bacteria; however, the photoreceptor(s) and their downstream signaling components that are responsible for negative phototaxis are poorly understood. Negative phototaxis sensory systems are important for cyanobacteria, oxygenic photosynthetic organisms that must contend with reactive oxygen species generated by an abundance of pigment photosensitizers. The unicellular cyanobacterium Synechocystis sp. PCC6803 exhibits type IV pilus-dependent negative phototaxis in response to unidirectional UV-A illumination. Using a reverse genetic approach, together with biochemical, molecular genetic, and RNA expression profiling analyses, we show that the cyanobacteriochrome locus ( slr1212/uirS ) of Synechocystis and two adjacent response regulator loci ( slr1213/uirR and the PatA-type regulator slr1214/lsiR ) encode a UV-A–activated signaling system that is required for negative phototaxis. We propose that UirS, which is membrane-associated via its ETR1 domain, functions as a UV-A photosensor directing expression of lsiR via release of bound UirR, which targets the lsiR promoter. Constitutive expression of LsiR induces negative phototaxis under conditions that normally promote positive phototaxis. Also induced by other stresses, LsiR thus integrates light inputs from multiple photosensors to determine the direction of movement.

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“…In this work, we therefore define phytochromes as bilinbased photosensors with PAS-GAF-PHY tridomain modules and CBCRs as those with evolutionarily related, bilin-binding GAF domains (13). The blue/green sensor SyPixJ1 (Sll0041) was the first CBCR to be photochemically characterized (24), and CBCRs with green/red and red/green cycles have been subsequently described (11,12,25,26). CBCRs thus tune the redabsorbing PCB chromophore to detect the entire visible light spectrum, and CBCRs exhibiting similar photocycles appear to group together into subfamilies (Fig.…”

mentioning

confidence: 99%

Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes

Rockwell

Martin

Feoktistova

et al. 2011

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

178

417

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Phytochromes are well-known as photoactive red-and near IRabsorbing chromoproteins with cysteine-linked linear tetrapyrrole (bilin) prosthetic groups. Phytochrome photoswitching regulates adaptive responses to light in both photosynthetic and nonphotosynthetic organisms. Exclusively found in cyanobacteria, the related cyanobacteriochrome (CBCR) sensors extend the photosensory range of the phytochrome superfamily to shorter wavelengths of visible light. Blue/green light sensing by a wellstudied subfamily of CBCRs proceeds via a photolabile thioether linkage to a second cysteine fully conserved in this subfamily. In the present study, we show that dual-cysteine photosensors have repeatedly evolved in cyanobacteria via insertion of a second cysteine at different positions within the bilin-binding GAF domain (cGMP-specific phosphodiesterases, cyanobacterial adenylate cyclases, and formate hydrogen lyase transcription activator FhlA) shared by CBCRs and phytochromes. Such sensors exhibit a diverse range of photocycles, yet all share ground-state absorbance of near-UV to blue light and a common mechanism of light perception: reversible photoisomerization of the bilin 15,16 double bond. Using site-directed mutagenesis, chemical modification and spectroscopy to characterize novel dual-cysteine photosensors from the cyanobacterium Nostoc punctiforme ATCC 29133, we establish that this spectral diversity can be tuned by varying the lightdependent stability of the second thioether linkage. We also show that such behavior can be engineered into the conventional phytochrome Cph1 from Synechocystis sp. PCC6803. Dual-cysteine photosensors thus allow the phytochrome superfamily in cyanobacteria to sense the full solar spectrum at the earth surface from near infrared to near ultraviolet.biliprotein | optogenetics | photoreceptor | UV-A sensor

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Cyanobacterial Phytochrome-like PixJ1 Holoprotein Shows Novel Reversible Photoconversion Between Blue- and Green-absorbing Forms

Abstract: ;The gene, pixJ1 (formerly pisJ1), is predicted to encode a phytochrome-like photoreceptor that is essential for positive phototaxis in the unicellular cyanobacterium

Cited by 142 publications

References 51 publications

Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme

Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme

Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803

Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes

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