Omega Rhodopsins: A Versatile Class of Microbial Rhodopsins
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Microbial rhodopsins are a superfamily of photoactive membrane proteins with the covalently bound retinal cofactor. Isomerization of the retinal chromophore upon absorption of a photon triggers conformational changes of the protein to function as ion pumps or sensors. After the discovery of proteorhodopsin in an uncultivated γ-proteobacterium, light-activated proton pumps have been widely detected among marine bacteria and, together with chlorophyll-based photosynthesis, are considered as an important axis responsible for primary production in the biosphere. Rhodopsins and related proteins show a high level of phylogenetic diversity; we focus on a specific class of bacterial rhodopsins containing the ‘3 omega motif.’ This motif forms a stack of three non-consecutive aromatic amino acids that correlates with the B–C loop orientation and is shared among the phylogenetically close ion pumps such as the NDQ motif-containing sodiumpumping rhodopsin, the NTQ motif-containing chloride-pumping rhodopsin, and some protonpumping rhodopsins including xanthorhodopsin. Here, we reviewed the recent research progress on these ‘omega rhodopsins,’ and speculated on their evolutionary origin of functional diversity.
Abstract
Microbial rhodopsins are a superfamily of photoactive membrane proteins with the covalently bound retinal cofactor. Isomerization of the retinal chromophore upon absorption of a photon triggers conformational changes of the protein to function as ion pumps or sensors. After the discovery of proteorhodopsin in an uncultivated γ-proteobacterium, light-activated proton pumps have been widely detected among marine bacteria and, together with chlorophyll-based photosynthesis, are considered as an important axis responsible for primary production in the biosphere. Rhodopsins and related proteins show a high level of phylogenetic diversity; we focus on a specific class of bacterial rhodopsins containing the ‘3 omega motif.’ This motif forms a stack of three non-consecutive aromatic amino acids that correlates with the B–C loop orientation and is shared among the phylogenetically close ion pumps such as the NDQ motif-containing sodiumpumping rhodopsin, the NTQ motif-containing chloride-pumping rhodopsin, and some protonpumping rhodopsins including xanthorhodopsin. Here, we reviewed the recent research progress on these ‘omega rhodopsins,’ and speculated on their evolutionary origin of functional diversity.
참고문헌 (76)
- Spudich JL, "Retinylidene proteins : structures and functions from archaea to humans", Annu. Rev. Cell Dev. Biol, 16, pp.365~392 (2000)
- Kandori H, "Hydration switch model for the proton transfer in the Schiff base region of bacteriorhodopsin", Biochim. Biophys. Acta, 1658, pp.72~79 (2004)
- Ernst OP, "Microbial and animal rhodopsins : structures, functions, and molecular mechanisms", Chem. Rev, 114, pp.126~163 (2014)
- Fuhrman JA, "Proteorhodopsins : an array of physiological roles? Nat", Rev. Microbiol, 6, pp.488~494 (2008)
- Oesterhelt D, "Rhodopsin-like protein from the purple membrane of Halobacterium halobium", Nat. New Biol, 233, pp.149~152 (1971)
- Oesterhelt D, "Functions of a new photoreceptor membrane", Proc. Natl. Acad. Sci. USA, 70, pp.2853~2857 (1973)
- Hildebrand E, "Two photosystems controlling behavioural responses of Halobacterium halobium", Nature, 257, pp.46~48 (1975)
- Schobert B, "Halorhodopsin is a light-driven chloride pump", J. Biol. Chem, 257, pp.10306~10313 (1982)
- Nagel G, "Channelrhodopsin-1 : a light-gated proton channel in green algae", Science, 296, pp.2395~2398 (2002)
- Sineshchekov OA, "Two rhodopsins mediate phototaxis to low-and high-intensity light in Chlamydomonas reinhardtii", Proc. Natl. Acad. Sci. USA, 99, pp.8689~8694 (2002)
- Beja O, "Bacterial rhodopsin : evidence for a new type of phototrophy in the sea", Science, 289, pp.1902~1906 (2000)
- Mongodin EF, "The genome of Salinibacter ruber : convergence and gene exchange among hyperhalophilic bacteria and archaea", Proc. Natl. Acad. Sci. USA, 102, pp.18147~18152 (2005)
- Balashov SP, "Xanthorhodopsin : a proton pump with a lightharvesting carotenoid antenna", Science, 309, pp.2061~2064 (2005)
- Sharma AK, "Actinorhodopsins : proteorhodopsin-like gene sequences found predominantly in non-marine environments", Environ. Microbiol, 10, pp.1039~1056 (2008)
- Kwon SK, "Genomic makeup of the marine flavobacterium Nonlabens(Donghaeana)dokdonensis and identification of a novel class of rhodopsins", Genome Biol. Evol, 5, pp.187~199 (2013)
- Yoshizawa S, "Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria", Proc. Natl. Acad. Sci. USA, 111, pp.6732~6737 (2014)
- Inoue K, "A light-driven sodium ion pump in marine bacteria", Nat. Commun, 4, pp.1678~ (2013)
- Inoue K, "A natural light-driven inward proton pump", Nat. Commun, 7, pp.13415~ (2016)
- Needham DM, "A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators", Proc. Natl. Acad. Sci. USA, 116, pp.20574~20583 (2019)
- Pushkarev A, "A distinct abundant group of microbial rhodopsins discovered using functional metagenomics", Nature, 558, pp.595~599 (2018)
- Kim K, "Crystal structure and functional characterization of a light-driven chloride pump having an NTQ motif", Nat. Commun, 7, pp.12677~ (2016)
- Morizumi T, "X-ray crystallographic structure and oligomerization of Gloeobacter rhodopsin", Sci. Rep, 9, pp.11283~ (2019)
- Shibata M, "Oligomeric states of microbial rhodopsins determined by high-speed atomic force microscopy and circular dichroic spectroscopy", Sci. Rep, 8, pp.8262~ (2018)
- Luecke H, "Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore", Proc. Natl. Acad. Sci. USA, 105, pp.16561~16565 (2008)
- Balashov SP, "Reconstitution of gloeobacter rhodopsin with echinenone : role of the 4-keto group", Biochemistry, 49, pp.9792~9799 (2010)
- Tsukamoto T, "Thermal and spectroscopic characterization of a proton pumping rhodopsin from an extreme thermophile", J. Biol. Chem, 288, pp.21581~21592 (2013)
- Tsukamoto T, "X-ray crystallographic structure of thermophilic rhodopsin : implications for high thermal stability and optogenetic function", J. Biol. Chem, 291, pp.12223~12232 (2016)
- Tian B, "Carotenoid biosynthesis in extremophilic Deinococcus-Thermus bacteria", Trends Microbiol, 18, pp.512~520 (2010)
- Misra R, "Retinal-salinixanthin interactions in a thermophilic rhodopsin", J. Phys. Chem. B, 123, pp.10~20 (2019)
- Nakamura Y, "Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids", DNA Res, 10, pp.137~145 (2003)
- Choi AR, "Cyanobacterial light-driven proton pump, gloeobacter rhodopsin : complementarity between rhodopsin-based energy production and photosynthesis", PLoS One, 9, pp.e110643~ (2014)
- Imasheva ES, "Reconstitution of Gloeobacter violaceus rhodopsin with a lightharvesting carotenoid antenna", Biochemistry, 48, pp.10948~10955 (2009)
- Iyer ES, "Efficient femtosecond energy transfer from carotenoid to retinal in gloeobacter rhodopsin-salinixanthin complex", J. Phys. Chem. B, 119, pp.2345~2349 (2015)
- Jana S, "Retinal binding to Apo-Gloeobacter rhodopsin : the role of pH and retinal-carotenoid interaction", J. Phys. Chem. B, 121, pp.10759~10769 (2017)
- Rusch DB, "The Sorcerer II Global Ocean Sampling expedition : northwest Atlantic through eastern tropical Pacific", PLoS Biol, 5, pp.e77~ (2007)
- Jezberova J, "Insights into variability of actinorhodopsin genes of the LG1 cluster in two different freshwater habitats", PLoS One, 8, pp.e68542~ (2013)
- Sharma AK, "Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria", ISME J, 3, pp.726~737 (2009)
- Keffer JL, "Characterization of an unconventional rhodopsin from the freshwater actinobacterium Rhodoluna lacicola", J. Bacteriol., 197, pp.2704~2712 (2015)
- Nakamura S, "Photochemical characterization of actinorhodopsin and its functional existence in the natural host", Biochim. Biophys. Acta, 1857, pp.1900~1908 (2016)
- Dwulit-Smith JR, "acI actinobacteria assemble a functional actinorhodopsin with natively synthesized retinal", Appl. Environ. Microbiol, 84, pp.e01678~ (2018)
- Mizuno CM, "Genomes of planktonic Acidimicrobiales : widening horizons for marine Actinobacteria by metagenomics", mBio, 6, pp.e02083~ (2015)
- Pushkarev A, "Functional metagenomic screen reveals new and diverse microbial rhodopsins", ISME J, 10, pp.2331~2335 (2016)
- Kato Y, "Kinetic analysis of H+-Na+ selectivity in a light-driven Na+-pumping rhodopsin", J. Phys. Chem. Lett, 6, pp.5111~5115 (2015)
- Zhao H, "Coexistence of light-driven Na+ and H+ transport in a microbial rhodopsin from Nonlabens dokdonensis", J. Photochem. Photobiol. B, 172, pp.70~76 (2017)
- Li H, "In vitro demonstration of dual light-driven Na(+)", H(+)pumping by a microbial rhodopsin, 2015, pp.109, 1446~1453
- da Silva GF, "Cation-specific conformations in a dual-function ion-pumping microbial rhodopsin", Biochemistry, 54, pp.3950~3959 (2015)
- Kovalev K, "Structure and mechanisms of sodiumpumping KR2 rhodopsin", Sci. Adv., 5, pp.eaav2671~ (2019)
- Tsunoda SP, "Functional characterization of sodium-pumping rhodopsins with different pumping properties", PLoS One, 12, pp.e0179232~ (2017)
- Gushchin I, "Crystal structure of a light-driven sodium pump", Nat. Struct. Mol. Biol, 22, pp.390~395 (2015)
- Kato HE, "Structural basis for Na+ transport mechanism by a lightdriven Na+ pump", Nature, 521, pp.48~53 (2015)
- Inoue K, "The role of the NDQ motif in sodium-pumping rhodopsins", Angew. Chem. Int. Ed. Engl, 54, pp.11536~11539 (2015)
- Abe-Yoshizumi R, "Role of Asn112 in a light-driven sodium ion-pumping rhodopsin", Biochemistry, 55, pp.5790~5797 (2016)
- Tahara S, "Ultrafast photoreaction dynamics of a lightdriven sodium-ion-pumping retinal protein from Krokinobacter eikastus revealed by femtosecond time-resolved absorption spectroscopy", J. Phys. Chem. Lett, 6, pp.4481~4486 (2015)
- Hontani Y, "The photochemistry of sodium ion pump rhodopsin observed by watermarked femto-to submillisecond stimulated Raman spectroscopy", Phys. Chem. Chem. Phys, 18, pp.24729~24736 (2016)
- Suomivuori CM, "Energetics and dynamics of a light-driven sodium-pumping rhodopsin", Proc. Natl. Acad. Sci. USA, 114, pp.7043~7048 (2017)
- Nakajima Y, "Presence of a haloarchaeal halorhodopsin-like Clpump in marine bacteria", Microbes Environ, 33, pp.89~97 (2018)
- Kandori H, "Ion-pumping microbial rhodopsins", Front. Mol. Biosci, 2, pp.52~ (2015)
- Sasaki J, "Conversion of bacteriorhodopsin into a chloride ion pump", Science, 269, pp.73~75 (1995)
- Hasemi T, "Characterization of a Cyanobacterial chloride-pumping rhodopsin and its conversion into a proton pump", J. Biol. Chem, 291, pp.355~362 (2016)
- Inoue K, "Spectroscopic study of a light-driven chloride ion pump from marine bacteria", J. Phys. Chem. B, 118, pp.11190~11199 (2014)
- Tsukamoto T, "Implications for the light-driven chloride ion transport mechanism of Nonlabens marinus rhodopsin 3 by its photochemical characteristics", J. Phys. Chem. B, 121, pp.2027~2038 (2017)
- Hosaka T, "Structural mechanism for light-driven transport by a new type of chloride ion pump, Nonlabens marinus rhodopsin-3", J. Biol. Chem, 291, pp.17488~17495 (2016)
- Inoue K, "Asymmetric functional conversion of eubacterial light-driven ion pumps", J. Biol. Chem, 291, pp.9883~9893 (2016)
- Anashkin VA, "Engineering a carotenoidbinding site in Dokdonia sp. PRO95 Na+-translocating rhodopsin by a single amino acid substitution", Photosynth. Res., 136, pp.161~169 (2018)
- Konno M, "Mutant of a light-driven sodium ion pump can transport cesium ions", J. Phys. Chem. Lett, 7, pp.51~55 (2016)
- Inoue K, "Red-shifting mutation of light-driven sodium-pump rhodopsin", Nat. Commun, 10, pp.1993~ (2019)
- Mackin KA, "An empirical test of convergent evolution in rhodopsins", Mol. Biol. Evol, 31, pp.85~95 (2014)
- Shalaeva DN, "Eukaryotic G protein-coupled receptors as descendants of prokaryotic sodiumtranslocating rhodopsins", Biol. Direct, 10, pp.63~ (2015)
- Pinhassi J, "Marine bacterial and archaeal ion-pumping rhodopsins : genetic diversity, physiology, and ecology", Microbiol. Mol. Biol. Rev, 80, pp.929~954 (2016)
- Albers SV, "Bioenergetics and solute uptake under extreme conditions", Extremophiles, 5, pp.285~294 (2001)
- Hase CC, "Sodium ion cycle in bacterial pathogens : evidence from cross-genome comparisons", Microbiol. Mol. Biol. Rev, 65, pp.353~370 (2001)
- Riedel T, "Genomics and physiology of a marine flavobacterium encoding a proteorhodopsin and a xanthorhodopsin-like protein", PLoS One, 8, pp.e57487~ (2013)
- Kwon YM, "Diversity and functional analysis of light-driven pumping rhodopsins in marine Flavobacteria", Microbiologyopen, 5, pp.212~223 (2016)
- Guerrero LD, "Evidence of microbial rhodopsins in Antarctic Dry Valley edaphic systems", Environ. Microbiol, 19, pp.3755~3767 (2017)
- Hamilton JJ, "Metabolic network analysis and metatranscriptomics reveal auxotrophies and nutrient sources of the cosmopolitan freshwater microbial lineage acI", mSystems, 2, pp.e00091~ (2017)
- Wurzbacher C, "Environmental actinorhodopsin expression revealed by a new in situ filtration and fixation sampler", Environ. Microbiol. Rep, 4, pp.491~497 (2012)
