Structural characterization of proton-pumping rhodopsin lacking a cytoplasmic proton donor residue by X-ray crystallography

Suzuki, Kenzi; Marín, María del Carmen; Konno, Masae; Bagherzadeh, Reza; Murata, Takeshi; Inoue, Kazuhide

doi:10.1016/j.jbc.2022.101722

Cited by 7 publications

(16 citation statements)

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“…Many more DTG opsin sequences belonging to this cluster were found in numerous stratfreshDB MAGs classified to Mycobacteriales and Solirubrobacterales within Actinobacteria, and notably most of these MAGs were recovered from clearwater environments (Figures 2a and 2b). DTG rhodopsins were initially discovered in soil-and plant-associated Proteobacteria (Harris et al 2015;Sudo & Yoshizawa 2016;Suzuki et al 2022) and our findings expand the taxonomic diversity of DTG rhodopsins.…”

Section: Opsin Gene Prevalence and Diversity In Freshwater Actinobact...supporting

confidence: 71%

“…The DTG rhodopsin was previously recovered in soil-and plant-associated Proteobacteria as an light-driven outward H + -pump; and its photochemical behavior is pH dependent and H + -pumping slows down at high extracellular pH, which might prevent intracellular alkalization in alkalized environments (Harris et al 2015;Sudo & Yoshizawa 2016;Suzuki et al 2022). DTG rhodopsins are phylogenetically close to DTS rhodopsins, forming a DTG/DTS cluster (Suzuki et al 2022).…”

Section: Diversity Of Opsin Genes In Clear and Humic Watersmentioning

confidence: 99%

“…The DTS rhodopsin from Sphingomonas paucimobilis functions as an outward H + -pump at pH lower than 7.0 and its photocycle speed is also pH dependent and slows down with increasing extracellular pH (Maliar et al 2020). The pH dependance of DTG/DTS rhodopsins might be due to the lack of a carboxylic H + -donating residue as in the DTE/DTD variants (Suzuki et al 2022), and therefore it is plausible that rhodopsins in the DTG/DTS cluster are all pH-dependent. In our study, we found DTG opsin genes in Mycobacteriales and Solirubrobacterales within Actinobacteria, and 121 out of the 130 DTG sequences were from four clearwater lakes with an average pH of 7.6 (averaged from these lakes at depths where these sequences were recovered) (Figure 2b).…”

Section: Diversity Of Opsin Genes In Clear and Humic Watersmentioning

confidence: 99%

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Diversity, distribution, and expression of opsin genes in freshwater lakes

Linz

Stevens³

et al. 2022

Preprint

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Microbial opsin genes are widely distributed in aquatic environments and may significantly contribute to phototrophy and energy budgets in global oceans. However, the study of freshwater opsin genes has been largely limited. Here, we explored Type I opsin gene diversity, ecological distribution, and expression in lakes with contrasting physicochemical and optical characteristics. Using metagenomes and derived draft genomes from a clearwater lake and a humic bog, we recovered opsin genes from Actinobacteria, Proteobacteria, Bacteroidetes, Verrucomicrobia, Planctomycetes, Chloroflexi, and Candidatus Saccharibacteria. Most were predicted to encode green light-absorbing proton pumps within the proteorhodopsin and xanthorhodopsin groups, with the humic bog harboring much less diversity. Notably, viral opsin and novel actinobacterial opsin genes phylogenetically significantly different from the typical actinorhodopsin were recovered. Analyses of the surface layer of 33 freshwater systems revealed an inverse correlation between opsin gene abundance and lake dissolved organic carbon (DOC). In humic water with high terrestrial DOC and light-absorbing humic substances, opsin gene abundance was low and dramatically declined within the first few meters, whereas the abundance remained relatively high along the bulk water column in clearwater lakes with low DOC. These results suggest opsin gene distribution is influenced by lake optical properties and DOC. Gene expression analysis confirmed the significance of opsin-based phototrophy in clearwater lakes and revealed different diel expressional patterns among major phyla. Overall, our analyses recovered novel diversity, revealed distribution patterns, confirmed opsin gene expression, and suggested the significance of rhodopsin-based phototrophy in freshwater energy budgets, especially in clearwater lakes.

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Section: Opsin Gene Prevalence and Diversity In Freshwater Actinobact...supporting

confidence: 71%

Section: Diversity Of Opsin Genes In Clear and Humic Watersmentioning

confidence: 99%

Section: Diversity Of Opsin Genes In Clear and Humic Watersmentioning

confidence: 99%

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Diversity, distribution, and expression of opsin genes in freshwater lakes

Linz

Stevens³

et al. 2022

Preprint

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“…A partial photosynthesis gene cluster (PGC) ( bchI , bchD , bchO , bchF , bchG , ppaA , ppsR, and tspO ) typical of aerobic anoxygenic phototrophs ( 14 ) was also found. In addition, two putative homologs of the functional proton-pumping DTG/DTS rhodopsin of Pseudomonas putida ( 15 ) were identified, each adjacent to a gene encoding beta-carotene 15,15′-dioxygenases associated with biosynthesis of the retinal cofactor of light-driven rhodopsin proton pumps.…”

Section: Announcementmentioning

confidence: 99%

Complete Genome of Sphingomonas aerolata PDD-32b-11, Isolated from Cloud Water at the Summit of Puy de Dôme, France

Jarrige

Nadalig

Joly

et al. 2022

Microbiol Resour Announc

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“…By learning a detailed energy conversion mechanism from natural molecular engines, we will obtain guidelines for the design of “Molecular Engine”. Dr. Maria del Carmen Marin at the University of Tokyo focuses on the ion transport mechanism of an outward-directed light-driven H + pumping microbial rhodopsin, Psp R. From the structural insight [ 1 ], she has succeeded in creating Psp R mutants which pump H + inwardly. Dr. Ryohei Kobayashi and Dr. Akihiro Otomo present on rotary ATPases, the most abundant biological molecular engine.…”

mentioning

confidence: 99%

Tackle “Molecular Engine” by early-career researchers

Otomo

Kosugi

2022

BIOPHYSICS

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Edited by Haruki NakamuraThe Novel Prize in Chemistry 2016 was awarded for "Design and production of molecular machines". Many molecular machines, molecules that move like machines on the nanoscale, have been successfully synthesized and methods to produce mechanical motions have been developed. On the other hand, it has been suggested that various functions are produced by introducing the function "converting energy" to "molecular mechanical motions". Five years ago, pioneer researchers defined such molecular machines, which have the function of energy conversion, as "Molecular Engine". They have researched energy conversion mechanisms of biomolecular machines in detail, understood the essence and general law by physics, and synthesized artificially "Molecular Engines" by chemistry. "Molecular Engine", design of autonomous functions through energy conversion, has buded by the orchestration of chemists, biologists, and physicists in the last five years supported by Grant-in-Aid for Scientific Research on Innovative Areas (18H05418).This scientific concept should be passed down to the next generations for further development. To this end, early-career researchers in various research fields are trying to elucidate the energy conversion mechanism of molecular machines and to design novel ones. Here, we invite eight early-career researchers who will lead the field in the future and have a symposium at the 60 th Annual Meeting of the Biophysical Society of Japan held in September 2022.Four researchers talk about researches of biological "Molecular Engine". By learning a detailed energy conversion mechanism from natural molecular engines, we will obtain guidelines for the design of "Molecular Engine". Dr. Maria del Carmen Marin at the University of Tokyo focuses on the ion transport mechanism of an outward-directed light-driven H + pumping microbial rhodopsin, PspR. From the structural insight [1], she has succeeded in creating PspR mutants which pump H + inwardly. Dr. Ryohei Kobayashi and Dr. Akihiro Otomo present on rotary ATPases, the most abundant biological molecular engine. Dr. Kobayashi at Institute for Molecular Science reports a detailed mechanism of a regulatory protein for mitochondrial ATP synthase, IF1. One of the unique features of IF1 is the unidirectional regulation, that is, it inhibits ATP hydrolysis but does not inhibit ATP synthesis. He elucidated the unidirectional regulation system

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Structural characterization of proton-pumping rhodopsin lacking a cytoplasmic proton donor residue by X-ray crystallography

Cited by 7 publications

References 68 publications

Diversity, distribution, and expression of opsin genes in freshwater lakes

Diversity, distribution, and expression of opsin genes in freshwater lakes

Complete Genome of Sphingomonas aerolata PDD-32b-11, Isolated from Cloud Water at the Summit of Puy de Dôme, France

Tackle “Molecular Engine” by early-career researchers

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