Novel Photosensory Two-Component System (PixA–NixB–NixC) Involved in the Regulation of Positive and Negative Phototaxis of Cyanobacterium Synechocystis sp. PCC 6803

Narikawa, Rei; Suzuki, Fumiko; Yoshihara, Shizue; Higashi, Satoru; Watanabe, Masakatsu; Ikeuchi, Masahiko

doi:10.1093/pcp/pcr155

Cited by 84 publications

(170 citation statements)

References 37 publications

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“…Additionally, SynEtr1-deficient Synechocystis cells transformed with a mutant SynEtr1 that cannot bind ethylene do not respond to ethylene. Our research demonstrates that SynEtr1 is an ethylene receptor and, in the context of prior research (Ulijasz et al, 2009;Narikawa et al, 2011;Song et al, 2011), likely functions as a dual input receptor for both light and ethylene. To our knowledge, this is the first report of a functional ethylene receptor in a cyanobacterium, making it the first ethylene receptor characterized in a nonplant species.…”

supporting

confidence: 61%

“…This is an integral membrane protein that is predicted to contain an ethylene-binding domain at its N terminus, followed by a phytochrome-like domain known as a cyanochrome, and a C-terminal His kinase domain that is likely to be the output domain of the protein ( Fig. 1A; Rodríguez et al, 1999;Ulijasz et al, 2009;Kwon et al, 2010;Narikawa et al, 2011;Song et al, 2011). The putative ethylene-binding domain of SynEtr1 has the seven amino acids shown to be required for ethylene binding in the ETR1 ethylene receptor from Arabidopsis ( Fig.…”

Section: Synetr1 Directly Binds Ethylenementioning

confidence: 99%

“…We previously showed that disruption of this gene eliminates ethylene-binding activity in Synechocystis, leading to the speculation that it encodes an ethylene-binding protein (Rodríguez et al, 1999). This gene, called Synechocystis Ethylene Response1 (SynEtr1), as originally designated by Ulijasz et al (2009) because of its putative role as an ethylene receptor, also has been called Positive Phototaxis A (Narikawa et al, 2011) and UV Intensity Response Sensor (Song et al, 2011), because of its role in light signaling. Despite these observations, there has been no research published that demonstrates that SynEtr1 directly binds ethylene or functions as an ethylene receptor.…”

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confidence: 99%

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Ethylene Regulates the Physiology of the Cyanobacterium Synechocystis sp. PCC 6803 via an Ethylene Receptor

2016

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Ethylene is a plant hormone that plays a crucial role in the growth and development of plants. The ethylene receptors in plants are well studied, and it is generally assumed that they are found only in plants. In a search of sequenced genomes, we found that many bacterial species contain putative ethylene receptors. Plants acquired many proteins from cyanobacteria as a result of the endosymbiotic event that led to chloroplasts. We provide data that the cyanobacterium Synechocystis (Synechocystis sp. PCC 6803) has a functional receptor for ethylene, Synechocystis Ethylene Response1 (SynEtr1). We first show that SynEtr1 directly binds ethylene. Second, we demonstrate that application of ethylene to Synechocystis cells or disruption of the SynEtr1 gene affects several processes, including phototaxis, type IV pilus biosynthesis, photosystem II levels, biofilm formation, and spontaneous cell sedimentation. Our data suggest a model where SynEtr1 inhibits downstream signaling and ethylene inhibits SynEtr1. This is similar to the inverse-agonist model of ethylene receptor signaling proposed for plants and suggests a conservation of structure and function that possibly originated over 1 billion years ago. Prior research showed that SynEtr1 also contains a light-responsive phytochrome-like domain. Thus, SynEtr1 is a bifunctional receptor that mediates responses to both light and ethylene. To our knowledge, this is the first demonstration of a functional ethylene receptor in a nonplant species and suggests that that the perception of ethylene is more widespread than previously thought.

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confidence: 61%

Section: Synetr1 Directly Binds Ethylenementioning

confidence: 99%

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Ethylene Regulates the Physiology of the Cyanobacterium Synechocystis sp. PCC 6803 via an Ethylene Receptor

2016

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“…Physiologically, CBCRs are implicated in regulation of phototaxis (30)(31)(32)(33)(34), but the best-understood CBCR function is the regulation of complementary chromatic acclimation (CCA). In CCA, cyanobacteria optimize the composition of their photosynthetic pigments in response to the availability of green and red light (35).…”

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confidence: 99%

Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle

Hirose

Rockwell

Nishiyama

et al. 2013

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

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142

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Cyanobacteriochromes (CBCRs) are cyanobacterial members of the phytochrome superfamily of photosensors. Like phytochromes, CBCRs convert between two photostates by photoisomerization of a covalently bound linear tetrapyrrole (bilin) chromophore. Although phytochromes are red/far-red sensors, CBCRs exhibit diverse photocycles spanning the visible spectrum and the near-UV (330-680 nm). Two CBCR subfamilies detect near-UV to blue light (330-450 nm) via a "two-Cys photocycle" that couples bilin 15Z/15E photoisomerization with formation or elimination of a second bilincysteine adduct. On the other hand, mechanisms for tuning the absorption between the green and red regions of the spectrum have not been elucidated as of yet. CcaS and RcaE are members of a CBCR subfamily that regulates complementary chromatic acclimation, in which cyanobacteria optimize light-harvesting antennae in response to green or red ambient light. CcaS has been shown to undergo a green/red photocycle: reversible photoconversion between a green-absorbing 15Z state ( 15Z P g ) and a red-absorbing 15E state ( 15E P r ). We demonstrate that RcaE from Fremyella diplosiphon undergoes the same photocycle and exhibits light-regulated kinase activity. In both RcaE and CcaS, the bilin chromophore is deprotonated as 15Z P g but protonated as 15E P r . This change of bilin protonation state is modulated by three key residues that are conserved in green/red CBCRs. We therefore designate the photocycle of green/red CBCRs a "protochromic photocycle," in which the dramatic change from green to red absorption is not induced by initial bilin photoisomerization but by a subsequent change in bilin protonation state.light sensing | phycobiliprotein | signal transduction | spectral tuning | two-component signaling P hytochrome photosensors initially were discovered in plants and later found in cyanobacteria, nonoxygenic photosynthetic bacteria, nonphotosynthetic bacteria, fungi, and algae (1, 2). These photoreceptors bind linear tetrapyrrole (bilin) chromophores within a conserved GAF (cGMP phosphodiesterase/adenylyl cyclase/FhlA) domain via a covalent thioether linkage to a conserved Cys residue (Fig. S1A)(3-6). Upon illumination, phytochromes reversibly convert between a red-absorbing dark state and a far-red-absorbing photoproduct. This red/far-red photocycle is triggered by photoisomerization of the bilin 15,16-double bond between the 15Z and 15E configurations (7,8), with 15Z giving red absorption and 15E far-red absorption (4, 6, 9). In phytochromes, the conjugated π system of the bilin is protonated in both photostates, and this protonation is necessary to maintain the red and far-red absorption (10-12). Conserved GAF residues supply a hydrogen bond network to tune the chemical and spectral properties of the bilin (Fig. S1B).* Cyanobacteriochromes (CBCRs) are widespread cyanobacterial photosensors with phytochrome-related GAF domains (1,2,13,14). Although CBCRs also convert between two photostates via bilin photoisomerization at C15, they exhibit much more spe...

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“…During complementary chromatic acclimation, certain cyanobacteria alter their antenna pigment and protein compositions in response to the ambient red/green-light ratio (2,3). The ability of cyanobacteria to move toward or away from light (phototaxis) is also a light color-dependent process and is usually controlled by UV/blue-or green/red-light exposure (4)(5)(6)(7). Conversely, to date, cell aggregation has been shown to be dependent on only blue-light exposure (8).…”

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confidence: 99%

Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation

Enomoto

Ni-Ni-Win

Narikawa

et al. 2015

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

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Cyanobacteriochromes (CBCRs) are cyanobacterial photoreceptors that have diverse spectral properties and domain compositions. Although large numbers of CBCR genes exist in cyanobacterial genomes, no studies have assessed whether multiple CBCRs work together. We recently showed that the diguanylate cyclase (DGC) activity of the CBCR SesA from Thermosynechococcus elongatus is activated by blue-light irradiation and that, when irradiated, SesA, via its product cyclic dimeric GMP (c-di-GMP), induces aggregation of Thermosynechococcus vulcanus cells at a temperature that is suboptimum for single-cell viability. For this report, we first characterize the photobiochemical properties of two additional CBCRs, SesB and SesC. Blue/teal light-responsive SesB has only c-di-GMP phosphodiesterase (PDE) activity, which is up-regulated by teal light and GTP. Blue/green light-responsive SesC has DGC and PDE activities. Its DGC activity is enhanced by blue light, whereas its PDE activity is enhanced by green light. A ΔsesB mutant cannot suppress cell aggregation under teal-green light. A ΔsesC mutant shows a less sensitive cell-aggregation response to ambient light. ΔsesA/ΔsesB/ΔsesC shows partial cell aggregation, which is accompanied by the loss of color dependency, implying that a nonphotoresponsive DGC(s) producing c-di-GMP can also induce the aggregation. The results suggest that SesB enhances the light color dependency of cell aggregation by degrading c-di-GMP, is particularly effective under teal light, and, therefore, seems to counteract the induction of cell aggregation by SesA. In addition, SesC seems to improve signaling specificity as an auxiliary backup to SesA/SesB activities. The coordinated action of these three CBCRs highlights why so many different CBCRs exist.

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Novel Photosensory Two-Component System (PixA–NixB–NixC) Involved in the Regulation of Positive and Negative Phototaxis of Cyanobacterium Synechocystis sp. PCC 6803

Cited by 84 publications

References 37 publications

Ethylene Regulates the Physiology of the Cyanobacterium Synechocystis sp. PCC 6803 via an Ethylene Receptor

Ethylene Regulates the Physiology of the Cyanobacterium Synechocystis sp. PCC 6803 via an Ethylene Receptor

Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle

Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation

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