Molecular Mechanisms and Evolutionary Robustness of a Color Switch in Proteorhodopsins

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2024 Jan 24

PMID 38266078

Authors

Jiafei Mao

Xinsheng Jin

Man Shi

David Heidenreich

Lynda J Brown

Richard C D Brown

Moreno Lelli

Xiao He

Clemens Glaubitz

Affiliations

Soon will be listed here.

Abstract

Proteorhodopsins are widely distributed photoreceptors from marine bacteria. Their discovery revealed a high degree of evolutionary adaptation to ambient light, resulting in blue- and green-absorbing variants that correlate with a conserved glutamine/leucine at position 105. On the basis of an integrated approach combining sensitivity-enhanced solid-state nuclear magnetic resonance (ssNMR) spectroscopy and linear-scaling quantum mechanics/molecular mechanics (QM/MM) methods, this single residue is shown to be responsible for a variety of synergistically coupled structural and electrostatic changes along the retinal polyene chain, ionone ring, and within the binding pocket. They collectively explain the observed color shift. Furthermore, analysis of the differences in chemical shift between nuclei within the same residues in green and blue proteorhodopsins also reveals a correlation with the respective degree of conservation. Our data show that the highly conserved color change mainly affects other highly conserved residues, illustrating a high degree of robustness of the color phenotype to sequence variation.

Citing Articles

Structural insights into the mechanism and dynamics of proteorhodopsin biogenesis and retinal scavenging.

Hirschi S, Lemmin T, Ayoub N, Kalbermatter D, Pellegata D, Ucurum Z Nat Commun. 2024; 15(1):6950.

PMID: 39138159 PMC: 11322631. DOI: 10.1038/s41467-024-50960-3.

References

Hou G, Byeon I, Ahn J, Gronenborn A, Polenova T . Recoupling of chemical shift anisotropy by R-symmetry sequences in magic angle spinning NMR spectroscopy. J Chem Phys. 2012; 137(13):134201. PMC: 3477183. DOI: 10.1063/1.4754149. View

Man D, Wang W, Sabehi G, Aravind L, Post A, Massana R . Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 2003; 22(8):1725-31. PMC: 154475. DOI: 10.1093/emboj/cdg183. View

Shen C, Jin X, Glover W, He X . Accurate Prediction of Absorption Spectral Shifts of Proteorhodopsin Using a Fragment-Based Quantum Mechanical Method. Molecules. 2021; 26(15). PMC: 8347797. DOI: 10.3390/molecules26154486. View

Salomon-Ferrer R, Gotz A, Poole D, Le Grand S, Walker R . Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald. J Chem Theory Comput. 2015; 9(9):3878-88. DOI: 10.1021/ct400314y. View

Klein A, Rovo P, Sakhrani V, Wang Y, Holmes J, Liu V . Atomic-resolution chemical characterization of (2x)72-kDa tryptophan synthase via four- and five-dimensional H-detected solid-state NMR. Proc Natl Acad Sci U S A. 2022; 119(4). PMC: 8795498. DOI: 10.1073/pnas.2114690119. View

Melaccio F, Del Carmen Marin M, Valentini A, Montisci F, Rinaldi S, Cherubini M . Toward Automatic Rhodopsin Modeling as a Tool for High-Throughput Computational Photobiology. J Chem Theory Comput. 2016; 12(12):6020-6034. DOI: 10.1021/acs.jctc.6b00367. View

Zhu T, Zhang J, He X . Correction of erroneously packed protein's side chains in the NMR structure based on ab initio chemical shift calculations. Phys Chem Chem Phys. 2014; 16(34):18163-9. DOI: 10.1039/c4cp02553a. View

Romei M, Lin C, Mathews I, Boxer S . Electrostatic control of photoisomerization pathways in proteins. Science. 2020; 367(6473):76-79. PMC: 7035911. DOI: 10.1126/science.aax1898. View

Cavalli A, Salvatella X, Dobson C, Vendruscolo M . Protein structure determination from NMR chemical shifts. Proc Natl Acad Sci U S A. 2007; 104(23):9615-20. PMC: 1887584. DOI: 10.1073/pnas.0610313104. View

10.

Otten R, Padua R, Bunzel H, Nguyen V, Pitsawong W, Patterson M . How directed evolution reshapes the energy landscape in an enzyme to boost catalysis. Science. 2020; 370(6523):1442-1446. PMC: 9616100. DOI: 10.1126/science.abd3623. View

11.

Inoue K, Ono H, Abe-Yoshizumi R, Yoshizawa S, Ito H, Kogure K . A light-driven sodium ion pump in marine bacteria. Nat Commun. 2013; 4:1678. DOI: 10.1038/ncomms2689. View

12.

Ashkenazy H, Abadi S, Martz E, Chay O, Mayrose I, Pupko T . ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res. 2016; 44(W1):W344-50. PMC: 4987940. DOI: 10.1093/nar/gkw408. View

13.

Altun A, Yokoyama S, Morokuma K . Spectral tuning in visual pigments: an ONIOM(QM:MM) study on bovine rhodopsin and its mutants. J Phys Chem B. 2008; 112(22):6814-27. PMC: 2491561. DOI: 10.1021/jp709730b. View

14.

Shi L, Ahmed M, Zhang W, Whited G, Brown L, Ladizhansky V . Three-dimensional solid-state NMR study of a seven-helical integral membrane proton pump--structural insights. J Mol Biol. 2009; 386(4):1078-93. DOI: 10.1016/j.jmb.2009.01.011. View

15.

Hoffmann M, Wanko M, Strodel P, Konig P, Frauenheim T, Schulten K . Color tuning in rhodopsins: the mechanism for the spectral shift between bacteriorhodopsin and sensory rhodopsin II. J Am Chem Soc. 2006; 128(33):10808-18. DOI: 10.1021/ja062082i. View

16.

Sunagawa S, Acinas S, Bork P, Bowler C, Eveillard D, Gorsky G . Tara Oceans: towards global ocean ecosystems biology. Nat Rev Microbiol. 2020; 18(8):428-445. DOI: 10.1038/s41579-020-0364-5. View

17.

Leeder A, Brown L, Becker-Baldus J, Mehler M, Glaubitz C, Brown R . Synthesis of isotopically labeled all-trans retinals for DNP-enhanced solid-state NMR studies of retinylidene proteins. J Labelled Comp Radiopharm. 2017; 61(13):922-933. DOI: 10.1002/jlcr.3576. View

18.

He X, Wang B, Merz Jr K . Protein NMR chemical shift calculations based on the automated fragmentation QM/MM approach. J Phys Chem B. 2009; 113(30):10380-8. DOI: 10.1021/jp901992p. View

19.

Pushkarev A, Hevroni G, Roitman S, Shim J, Choi A, Jung K . The Use of a Chimeric Rhodopsin Vector for the Detection of New Proteorhodopsins Based on Color. Front Microbiol. 2018; 9:439. PMC: 5859045. DOI: 10.3389/fmicb.2018.00439. View

20.

Aladin V, Vogel M, Binder R, Burghardt I, Suess B, Corzilius B . Complex Formation of the Tetracycline-Binding Aptamer Investigated by Specific Cross-Relaxation under DNP. Angew Chem Int Ed Engl. 2019; 58(15):4863-4868. DOI: 10.1002/anie.201811941. View