Demonstration of a sensory rhodopsin in eubacteria

Jung, Kwang Hwan; Trivedi, Vishwa D.; Spudich, John L.

doi:10.1046/j.1365-2958.2003.03395.x

Cited by 235 publications

(304 citation statements)

References 57 publications

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“…Moreover, in tests for enzymatic activity all-trans-retinal was the major product and only trace amounts of 13-cis-retinal became detectable (21). Whereas animal visual pigments solely bind cis-retinoid stereoisomers, cyanobacterial opsins readily bind all-trans-retinal to form the bipartite sensory rhodopsin complex (22).…”

Section: Discussionmentioning

confidence: 99%

NinaB combines carotenoid oxygenase and retinoid isomerase activity in a single polypeptide

Oberhauser

Voolstra

Bangert

et al. 2008

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

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In animals, successful production of the visual chromophore (11-cis-retinal or derivatives thereof such as 11-cis-3-hydroxy-retinal) is essential for photoreceptor cell function and survival. These carotenoid-derived compounds must combine with a protein moiety (the opsin) to establish functional visual pigments. Evidence from cell culture systems has implicated that the retinal pigment epithelium protein of 65 kDa (RPE65) is the long-sought all-trans to 11-cis retinoid isomerase. RPE65 is structurally related to nonheme iron oxygenases that catalyze the conversion of carotenoids into retinoids. In vertebrate genomes, two carotenoid oxygenases and RPE65 are encoded, whereas in insect genomes only a single representative of this protein family, named NinaB (denoting neither inactivation nor afterpotential mutant B), is encoded. We here cloned and functionally characterized the ninaB gene from the great wax moth Galleria mellonella. We show that the recombinant purified enzyme combines isomerase and oxygenase (isomerooxygenase) activity in a single polypeptide. From kinetics and isomeric composition of cleavage products of asymmetrical carotenoid substrates, we propose a model for the spatial arrangement between substrate and enzyme. In Drosophila, we show that carotenoid-isomerooxygenase activity of NinaB is more generally found in insects, and we provide physiological evidence that carotenoids such as 11-cis-retinal can promote visual pigment biogenesis in the dark. Our study demonstrates that trans/cis isomerase activity can be intrinsic to this class of proteins and establishes these enzymes as key components for both invertebrate and vertebrate vision. RPE65 ͉ vision ͉ visual chromophoreA nimal visual pigments (rhodopsins) are bipartite G-proteincoupled receptors consisting of an opsin moiety and a carotenoid-derived retinylidene chromophore (1). Two fundamental issues in the pathway for visual chromophore production have resisted molecular analysis for a long time: first, the oxidative cleavage of C 40 carotenoids into C 20 retinoids; and second, the all-trans to 11-cis isomerization of retinoids.The molecular basis for the oxidative cleavage was resolved by cloning and characterization of NinaB (denoting neither inactivation nor afterpotential mutant B), which converts carotenoids into retinoids in Drosophila melanogaster (2, 3). Thereafter, several related carotenoid-15,15Ј-oxygenases (CMO1) have been identified and characterized in vertebrates including human beings (4-7). In addition, in vertebrates a second type of carotenoid-oxygenase, carotenoid-9Ј,10Ј-monooxygenase (CMO2) has been identified that cleaves carotenoids asymmetrically (8, 9), although its physiological function is not yet fully understood.The isomerization problem concerns the questions of how the visual chromophore is produced to establish functional visual pigments and, in vertebrates, how the all-trans visual photoproduct is isomerized back to the 11-cis chromophore, to maintain visual responsiveness. Recently, evidence in cell cultur...

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Section: Discussionmentioning

confidence: 99%

NinaB combines carotenoid oxygenase and retinoid isomerase activity in a single polypeptide

Oberhauser

Voolstra

Bangert

et al. 2008

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

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“…They are common in animals, green algae and archaebacteria. In addition, recently discovered rhodopsins (Spudich et al ., 2000;Jung et al ., 2003) suggest the occurrence of retinal in Eubacteria and fungi. However, there is no report of the formation of retinal or its derivatives in the eubacterial domain of life.…”

Section: Introductionmentioning

confidence: 99%

Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803

Ruch

Beyer

Ernst³

et al. 2005

Molecular Microbiology

113

131

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“…Thus, rapid diversification of photosynthetic machineries and antenna pigments followed the glycobacterial revolution. Photoreceptors allowing physiological chromatic adaptation and light-oriented movements probably also stem from the glycobacterial ancestor; sensory rhodopsins occur in cyanobacteria and proteobacteria ( Jung et al 2003;Ruiz-Gonzalez & Marin 2004;Venter et al 2004;Vogeley et al 2004). One green non-S bacterium photosynthesizes using geothermal radiation in deep-sea vents (Beatty et al 2005); like sulphur-oxidizers there, they are glycobacteria and so younger than chlorobacteria.…”

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confidence: 99%

Cell evolution and Earth history: stasis and revolution

Cavalier‐Smith

2006

Phil. Trans. R. Soc. B

251

278

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This synthesis has three main parts. The first discusses the overall tree of life and nature of the last common ancestor (cenancestor). I emphasize key steps in cellular evolution important for ordering and timing the major evolutionary innovations in the history of the biosphere, explaining especially the origins of the eukaryote cell and of bacterial flagella and cell envelope novelties. Second, I map the tree onto the fossil record and discuss dates of key events and their biogeochemical impact. Finally, I present a broad synthesis, discussing evidence for a three-phase history of life. The first phase began perhaps ca 3.5 Gyr ago, when the origin of cells and anoxic photosynthesis generated the arguably most primitive prokaryote phylum, Chlorobacteria (ZChloroflexi), the first negibacteria with cells bounded by two acyl ester phospholipid membranes. After this 'chlorobacterial age' of benthic anaerobic evolution protected from UV radiation by mineral grains, two momentous quantum evolutionary episodes of cellular innovation and microbial radiation dramatically transformed the Earth's surface: the glycobacterial revolution initiated an oxygenic 'age of cyanobacteria' and, as the ozone layer grew, the rise of plankton; immensely later, probably as recently as ca 0.9 Gyr ago, the neomuran revolution ushered in the 'age of eukaryotes', Archaebacteria (arguably the youngest bacterial phylum), and morphological complexity. Diversification of glycobacteria ca 2.8 Gyr ago, predominantly inhabiting stratified benthic mats, I suggest caused serial depletion of 13 C by ribulose 1,5-bis-phosphate caboxylase/oxygenase (Rubisco) to yield ultralight late Archaean organic carbon formerly attributed to methanogenesis plus methanotrophy. The late origin of archaebacterial methanogenesis ca 720 Myr ago perhaps triggered snowball Earth episodes by slight global warming increasing weathering and reducing CO 2 levels, to yield runaway cooling; the origin of anaerobic methane oxidation ca 570 Myr ago reduced methane flux at source, stabilizing Phanerozoic climates. I argue that the major cellular innovations exhibit a pattern of quantum evolution followed by very rapid radiation and then substantial stasis, as described by Simpson. They yielded organisms that are a mosaic of extremely conservative and radically novel features, as characterized by De Beer's phrase 'mosaic evolution'. Evolution is not evenly paced and there are no real molecular clocks.

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Demonstration of a sensory rhodopsin in eubacteria

Cited by 235 publications

References 57 publications

NinaB combines carotenoid oxygenase and retinoid isomerase activity in a single polypeptide

NinaB combines carotenoid oxygenase and retinoid isomerase activity in a single polypeptide

Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803

Cell evolution and Earth history: stasis and revolution

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