Cryo-EM Structure of the Whole Photosynthetic Reaction Center Apparatus from the Green Sulfur Bacterium

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2023 Jan 24

PMID 36693097

Authors

Hao Xie

Alexandros Lyratzakis

Radhika Khera

Myrto Koutantou

Sonja Welsch

Hartmut Michel

Georgios Tsiotis

Affiliations

Soon will be listed here.

Abstract

Light energy absorption and transfer are very important processes in photosynthesis. In green sulfur bacteria light is absorbed primarily by the chlorosomes and its energy is transferred via the Fenna-Matthews-Olson (FMO) proteins to a homodimeric reaction center (RC). Here, we report the cryogenic electron microscopic structure of the intact FMO-RC apparatus from at 2.5 Å resolution. The FMO-RC apparatus presents an asymmetric architecture and contains two FMO trimers that show different interaction patterns with the RC core. Furthermore, the two permanently bound transmembrane subunits PscC, which donate electrons to the special pair, interact only with the two large PscA subunits. This structure fills an important gap in our understanding of the transfer of energy from antenna to the electron transport chain of this RC and the transfer of electrons from reduced sulfur compounds to the special pair.

Citing Articles

A Simple Expression for the Screening of Excitonic Couplings between Chlorophylls as Inferred for Photosystem I Trimers.

Eder M, Renger T Int J Mol Sci. 2024; 25(16).

PMID: 39201694 PMC: 11355009. DOI: 10.3390/ijms25169006.

Anoxygenic photosynthesis with emphasis on green sulfur bacteria and a perspective for hydrogen sulfide detoxification of anoxic environments.

Kushkevych I, Prochazka V, Vitezova M, Dordevic D, El-Salam M, Rittmann S Front Microbiol. 2024; 15:1417714.

PMID: 39056005 PMC: 11269200. DOI: 10.3389/fmicb.2024.1417714.

Investigating the Balance between Structural Conservation and Functional Flexibility in Photosystem I.

Nelson N Int J Mol Sci. 2024; 25(10).

PMID: 38791114 PMC: 11121529. DOI: 10.3390/ijms25105073.

The synergy between the PscC subunits for electron transfer to the P special pair in Chlorobaculum tepidum.

Lyratzakis A, Daskalakis V, Xie H, Tsiotis G Photosynth Res. 2024; 160(2-3):87-96.

PMID: 38625595 PMC: 11108878. DOI: 10.1007/s11120-024-01093-7.

Self-aggregation of zinc bacteriochlorophyll-d analogs with an acylhydrazone moiety as the 13-keto-carbonyl alternative.

Fujii S, Tamiaki H Photochem Photobiol. 2024; 101(1):63-69.

PMID: 38581225 PMC: 11737012. DOI: 10.1111/php.13949.

References

Williams C, Headd J, Moriarty N, Prisant M, Videau L, Deis L . MolProbity: More and better reference data for improved all-atom structure validation. Protein Sci. 2017; 27(1):293-315. PMC: 5734394. DOI: 10.1002/pro.3330. View

Stark H . GraFix: stabilization of fragile macromolecular complexes for single particle cryo-EM. Methods Enzymol. 2010; 481:109-26. DOI: 10.1016/S0076-6879(10)81005-5. View

Nielsen J, Kulminskaya N, Bjerring M, Linnanto J, Ratsep M, Pedersen M . In situ high-resolution structure of the baseplate antenna complex in Chlorobaculum tepidum. Nat Commun. 2016; 7:12454. PMC: 4992139. DOI: 10.1038/ncomms12454. View

Axelrod H, Abresch E, Okamura M, Yeh A, Rees D, Feher G . X-ray structure determination of the cytochrome c2: reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol. 2002; 319(2):501-15. DOI: 10.1016/S0022-2836(02)00168-7. View

Hippler M, Drepper F, Haehnel W, Rochaix J . The N-terminal domain of PsaF: precise recognition site for binding and fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 1998; 95(13):7339-44. PMC: 22610. DOI: 10.1073/pnas.95.13.7339. View

Hirano Y, Higuchi M, Azai C, Oh-Oka H, Miki K, Wang Z . Crystal structure of the electron carrier domain of the reaction center cytochrome c(z) subunit from green photosynthetic bacterium Chlorobium tepidum. J Mol Biol. 2010; 397(5):1175-87. DOI: 10.1016/j.jmb.2010.02.011. View

Oh-Oka H, Iwaki M, Itoh S . Viscosity dependence of the electron transfer rate from bound cytochrome c to P840 in the photosynthetic reaction center of the green sulfur bacterium Chlorobium tepidum. Biochemistry. 1997; 36(30):9267-72. DOI: 10.1021/bi9701787. View

Afonine P, Klaholz B, Moriarty N, Poon B, Sobolev O, Terwilliger T . New tools for the analysis and validation of cryo-EM maps and atomic models. Acta Crystallogr D Struct Biol. 2018; 74(Pt 9):814-840. PMC: 6130467. DOI: 10.1107/S2059798318009324. View

Orf G, Blankenship R . Chlorosome antenna complexes from green photosynthetic bacteria. Photosynth Res. 2013; 116(2-3):315-31. DOI: 10.1007/s11120-013-9869-3. View

10.

Umena Y, Kawakami K, Shen J, Kamiya N . Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature. 2011; 473(7345):55-60. DOI: 10.1038/nature09913. View

11.

Schmidt Am Busch M, Muh F, Madjet M, Renger T . The Eighth Bacteriochlorophyll Completes the Excitation Energy Funnel in the FMO Protein. J Phys Chem Lett. 2015; 2(2):93-8. DOI: 10.1021/jz101541b. View

12.

Tronrud D, Wen J, Gay L, Blankenship R . The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosynth Res. 2009; 100(2):79-87. DOI: 10.1007/s11120-009-9430-6. View

13.

Kolsch A, Hejazi M, Stieger K, Feifel S, Kern J, Muh F . Insights into the binding behavior of native and non-native cytochromes to photosystem I from . J Biol Chem. 2018; 293(23):9090-9100. PMC: 5995507. DOI: 10.1074/jbc.RA117.000953. View

14.

Cole C, Barber J, Barton G . The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 2008; 36(Web Server issue):W197-201. PMC: 2447793. DOI: 10.1093/nar/gkn238. View

15.

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View

16.

Gisriel C, Azai C, Cardona T . Recent advances in the structural diversity of reaction centers. Photosynth Res. 2021; 149(3):329-343. PMC: 8452559. DOI: 10.1007/s11120-021-00857-9. View

17.

Grant T, Rohou A, Grigorieff N . TEM, user-friendly software for single-particle image processing. Elife. 2018; 7. PMC: 5854467. DOI: 10.7554/eLife.35383. View

18.

Saga Y, Yoshida N, Yamada S, Mizoguchi T, Tamiaki H . Biosynthesis of unnatural glycolipids possessing diyne moiety in the acyl chain in the green sulfur photosynthetic bacterium grown by supplementation of 10,12-heptadecadiynic acid. Biochem Biophys Rep. 2017; 9:42-46. PMC: 5614547. DOI: 10.1016/j.bbrep.2016.11.007. View

19.

Rohou A, Grigorieff N . CTFFIND4: Fast and accurate defocus estimation from electron micrographs. J Struct Biol. 2015; 192(2):216-21. PMC: 6760662. DOI: 10.1016/j.jsb.2015.08.008. View

20.

Punjani A, Rubinstein J, Fleet D, Brubaker M . cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat Methods. 2017; 14(3):290-296. DOI: 10.1038/nmeth.4169. View