Abstract
Photochemically induced dynamic nuclear polarization (photo-CIDNP) has been observed in the homodimeric, type-1 photochemical reaction centers (RCs) of the acidobacterium, Chloracidobacterium (Cab.) thermophilum, by 15N magic-angle spinning (MAS) solid-state NMR under continuous white-light illumination. Three light-induced emissive (negative) signals are detected. In the RCs of Cab. thermophilum, three types of (bacterio)chlorophylls have previously been identified: bacteriochlorophyll a (BChl a), chlorophyll a (Chl a), and Zn-bacteriochlorophyll a′ (Zn-BChl a′) (Tsukatani et al. in J Biol Chem 287:5720–5732, 2012). Based upon experimental and quantum chemical 15N NMR data, we assign the observed signals to a Chl a cofactor. We exclude Zn-BChl because of its measured spectroscopic properties. We conclude that Chl a is the primary electron acceptor, which implies that the primary donor is most likely Zn-BChl a′. Chl a and 81-OH Chl a have been shown to be the primary electron acceptors in green sulfur bacteria and heliobacteria, respectively, and thus a Chl a molecule serves this role in all known homodimeric type-1 RCs.
This is a preview of subscription content, access via your institution.
References
Alia A, Roy E, Gast P et al (2004) Photochemically induced dynamic nuclear polarization in photosystem I of plants observed by 13C magic-angle spinning NMR. J Am Chem Soc 126:12819–12826. https://doi.org/10.1021/ja048051+
Becke AD (1993) Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98:5648–5652. https://doi.org/10.1063/1.464913
Bennett AE, Rienstra CM, Auger M et al (1995) Heteronuclear decoupling in rotating solids. J Chem Phys 103:6951–6958. https://doi.org/10.1063/1.470372
Bode B, Thamarath SS, Sai Sankar Gupta KB, Alia A, Jeschke G, Matysik J (2013) The solid-state photo-CIDNP effect and its analytical application. In: Kuhn L (ed) Hyperpolarization methods in NMR spectroscopy. Springer, Berlin, pp 105–121
Boxer SG, Closs GL, Katz JJ (1974) The effect of magnesium coordination on the 13C and 15N magnetic resonance spectra of chlorophyll a. Energies of nitrogen nπ* states as deduced from a the relative complete assignment of chemical shifts. J Am Chem Soc 96:7058–7066. https://doi.org/10.1021/ja00829a038
Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496. https://doi.org/10.1016/j.tim.2006.09.001
Bryant DA, Garcia Costas AM, Maresca JA et al (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–526. https://doi.org/10.1126/science.1143236
Cardona T (2015) A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth Res 126:111–134. https://doi.org/10.1007/s11120-014-0065-x
Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266
Céspedes-Camacho IF, Matysik J (2014) Spin in photosynthetic electron transport. In: Golbeck J, van der Est A (eds) The biophysics of photosynthesis. Springer, New York, pp 141–170
Chen GE, Canniffe DP, Martin EC, Hunter CN (2016) Absence of the cbb 3 terminal oxidase reveals an active oxygen-dependent cyclase involved in bacteriochlorophyll biosynthesis in Rhodobacter sphaeroides. J Bacteriol 198:2056–2063. https://doi.org/10.1128/JB.00121-16
Daviso E, Jeschke G, Matysik J (2008a) Photochemically induced dynamic nuclear polarization (photo-CIDNP) magic-angle spinning NMR. In: Aartsma TJ, Matysik J (eds) Biophysical techniques in photosynthesis. Springer, Dordrecht, pp 385–399
Daviso E, Gupta KBSS, Prakash S et al (2008b) 15N photo-CIDNP MAS NMR on RCs of Rhodobacter sphaeroides WT and R26. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Energy from the sun. Springer, Dordrecht, pp 25–28
Diller A, Alia A, Roy E et al (2005) Photo-CIDNP solid-state NMR on photosystems I and II: what makes P680 special? Photosynth Res 84:303–308. https://doi.org/10.1007/s11120-005-0411-0
Diller A, Roy E, Gast P et al (2007a) 15N photochemically induced dynamic nuclear polarization magic-angle spinning NMR analysis of the electron donor of photosystem II. Proc Natl Acad Sci USA 104:12767–12771. https://doi.org/10.1073/pnas.0701763104
Diller A, Prakash S, Alia A, Gast P, Matysik J, Jeschke G (2007b) Signals in solid-state photochemically induced dynamic nuclear polarization recover faster than with the longitudinal relaxation time. J Phys Chem B 111:10606–10614. https://doi.org/10.1021/jp072428r
Diller A, Alia A, Gast P et al (2008) 13C photo-CIDNP MAS NMR on the LH1-RC complex of Rhodopseudomonas acidophilia. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Energy from the sun. Springer, Dordrecht, pp 55–58
Egorova-Zachernyuk T, van Rossum B, Erkelens C, de Groot H (2008) Characterisation of uniformly 13C, 15N labelled bacteriochlorophyll a and bacteriopheophytin a in solution and in solid state: complete assignment of the 13C, 1H and 15N chemical shifts. Magn Res Chem 46:1074–1083. https://doi.org/10.1002/mr3c.2295
Fischer MR, de Groot HJM, Raap J et al (1992) 13C Magic angle spinning NMR study of the light-induced and temperature-dependent changes in Rhodobacter sphaeroides R26 reaction centers enriched in [4′-13C]tyrosine. Biochemistry 31:11038–11049
Fischer WW, Hemp J, Johnson JE (2016) Evolution of oxygenic photosynthesis. Annu Rev Earth Planet Sci 44:647–683. https://doi.org/10.1146/annurev-earth-060313-054810
Frisch MJ, Trucks GW, Schlegel HB et al (2009) Gaussian 09, revision D. 01. Gaussian Inc., Wallingford
Gisriel C, Sarrou I, Ferlez B et al (2017) Structure of a symmetric photosynthetic reaction center-photosystem. Science 357:1021–1025. https://doi.org/10.1126/science.aan5611
Golbeck JH (2003) Shared thematic elements in photochemical reaction centers. Proc Natl Acad Sci USA 90:1642–1646. https://doi.org/10.1073/pnas.90.5.1642
Grimme S, Ehrlich S, Goerigk L (2011) Effect of the damping function in dispersion corrected density functional theory. J Comput Chem 32:1456–1465. https://doi.org/10.1002/jcc.21759
Janssen GJ, Daviso E, van Son M et al (2010) Observation of the solid-state photo-CIDNP effect in entire cells of cyanobacteria Synechocystis. Photosynth Res 104:275–282. https://doi.org/10.1007/s11120-009-9508-1
Janssen GJ, Roy E, Matysik J, Alia A (2012) 15N photo-CIDNP MAS NMR to reveal functional heterogeneity in electron donor of different plant organisms. Appl Magn Reson 42:57–67. https://doi.org/10.1007/s00723-011-0283-8
Jeschke G (1998) A new mechanism for chemically induced dynamic nuclear polarization in the solid state. J Am Chem Soc 120:4425–4429. https://doi.org/10.1021/ja973744u
Jeschke G, Matysik J (2003) A reassessment of the origin of photochemically induced dynamic nuclear polarization effects in solids. Chem Phys 294:239–255. https://doi.org/10.1016/S0301-0104(03)00278-7
Kobayashi M, Akiyama M, Yamamura M et al (1998) Structural determination of the novel Zn-containing bacteriochlorophyll in Acidiphilium rubrum. Photomed Photobiol 20:75–80
Kobayashi M, Akiyama M, Kano H, Kise H (2006) Spectroscopy and structure determination. In: Govindjee, Sharkey TD (eds) Advances in photosynthesis and respiration, vol 25. Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, function and applications. Springer, Dordrecht, pp 79–94
Kobayashi M, Sorimachi Y, Fukayama D et al (2016) Physicochemical properties of chlorophylls and bacteriochlorophylls. In: Pessaraki M (ed) Handbook of photosynthesis. CRC Press, Boca Raton, pp 95–148
Li H, Jubelirer S, Garcia Costas AM et al (2009) Multiple antioxidant proteins protect Chlorobaculum tepidum against oxygen and reactive oxygen species. Arch Microbiol 191:853–867. https://doi.org/10.1007/s00203-009-0514-7
Liu Z, Klatt CG, Ludwig M, Rusch DB, Jensen SI, Kühl M, Ward DM, Bryant DA (2012) ‘Candidatus Thermochlorobacter aerophilum’: an aerobic chlorophotoheterotrophic member of the phylum Chlorobi. ISME J 6:1869–1882
Madigan MT (2001) Firmicutes. In: Whitman W (ed) Bergey’s manual of systematic bacteriology. Springer, New York, pp 625–630
Marenich AV, Cramer CJ, Truhlar DG (2009) Performance of SM6, SM8, and SMD on the SAMPL1 test set for the prediction of small-molecule solvation free energies. J Phys Chem B 113:6378–6396. https://doi.org/10.1021/jp809094y
Martin WF, Beatty JT, Bryant DA (2018) A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiol Rev 42:205–231. https://doi.org/10.1093/femsre/fux056
Matysik J, Alia A, Hollander JG et al (2000) A set-up to study photochemically induced dynamic nuclear polarization in photosynthetic reaction centres by solid-state NMR. Indian J Biochem Biophys 37:418
Matysik J, Diller A, Roy E, Alia A (2009) The solid-state photo-CIDNP effect. Photosynth Res 102:427–435. https://doi.org/10.1007/s11120-009-9403-9
McDermott A, Zysmilich MG, Polenova T (1998) Solid state NMR studies of photoinduced polarization in photosynthetic reaction centers: mechanism and simulations. Solid State Nucl Magn Reson 11:21–47. https://doi.org/10.1016/S0926-2040(97)00094-5
Oh-oka H (2007) Type 1 reaction center of photosynthetic heliobacteria. Photochem Photobiol 83:177–186. https://doi.org/10.1562/2006-03-29-IR-860
Overmann J (2001) Chlorobi. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 601–605
Polenova T, McDermott AE (1999) A coherent mixing mechanism explains the photoinduced nuclear polarization in photosynthetic reaction centers. J Phys Chem 103:535–548. https://doi.org/10.1021/jp9822642
Prakash S, Alia A, Gast P, de Groot HJM, Jeschke G, Matysik J (2005) Magnetic field dependence of photo-CIDNP MAS NMR on photosynthetic reaction centres of Rhodobacter sphaeroides WT. J Am Chem Soc 127:14290–14298. https://doi.org/10.1021/ja0623616
Prakash S, Alia A, Gast P et al (2006) Photo-CIDNP MAS NMR in intact cells of Rhodobacter sphaeroides R26: molecular and atomic resolution at nanomolar concentration. J Am Chem Soc 128:12794–12799. https://doi.org/10.1021/ja0623616
Rassolov VA, Ratner MA, Pople JA et al (2001) 6-31G* basis set for third-row atoms. J Comput Chem 22:976–984. https://doi.org/10.1002/jcc.1058
Roy E, Alia A, Gast P et al (2007a) Photochemically induced dynamic nuclear polarization in the reaction center of the green sulphur bacterium Chlorobium tepidum observed by 13C MAS NMR. Biochim Biophys Acta 1767:610–615. https://doi.org/10.1016/j.bbabio.2006.12.012
Roy E, Diller A, Alia A et al (2007b) Magnetic field dependence of 13C photo-CIDNP MAS NMR in plant photosystems I and II. Appl Magn Reson 31:193–204. https://doi.org/10.1007/BF03166256
Roy E, Rohmer T, Gast P et al (2008) Characterization of the primary radical pair in reaction centers of Heliobacillus mobilis by 13C photo-CIDNP MAS NMR. Biochemistry 47:4629–4635. https://doi.org/10.1021/bi800030g
Ruud K, Helgaker T, Bak KL et al (1993) Hartree–Fock limit magnetizabilities from London orbitals. J Chem Phys 99:3847–3859. https://doi.org/10.1063/1.466131
Schulten EAM, Matysik J, Alia A et al (2002)) 13C MAS NMR and photo-CIDNP reveal a pronounced asymmetry in the electronic ground state of the special pair of Rhodobacter sphaeroides reaction centers. Biochemistry 41:8708–8717. https://doi.org/10.1021/bi025608u
Sosnovsky DV, Jeschke G, Matysik J, Vieth H-M, Ivanov KL (2016) Level crossing analysis of chemically induced dynamic nuclear polarization: towards a common description of liquid-state and solid-state cases. J Chem Phys 144:144202. https://doi.org/10.1063/1.4945341
Tank M, Bryant DA (2015a) Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium. Int J Syst Evol Microbiol 65:1426–1430. https://doi.org/10.1099/ijs.0.000113
Tank M, Bryant DA (2015b) Nutrient requirements and growth physiology of the photoheterotrophic acidobacterium, Chloracidobacterium thermophilum. Front Microbiol 6:226. https://doi.org/10.3389/fmicb.2015.00226
Tank M, Thiel V, Bryant DA (2017) A panoply of phototrophs: an overview of chlorophototrophs found in the microbial mats of alkaline siliceous hot springs in Yellowstone National Park, WY, USA. In: Hallenbeck PC (ed) Modern topics in the phototrophic prokaryotes: environmental and applied aspects. Springer, Berlin, pp 87–137. https://doi.org/10.1007/978-3-319-46261-5
Thamarath SS, Heberle J, Hore P et al (2010) Solid-state photo-CIDNP effect observed in phototropin LOV1-C57S by 13C magic-angle spinning NMR spectroscopy. J Am Chem Soc 132:15542–15543. https://doi.org/10.1021/ja1082969
Thamarath SS, Alia A, Daviso E et al (2012) Whole cell nuclear magnetic resonance characterization of two photochemically active states of the photosynthetic reaction center in heliobacteria. Biochemistry 51:5763–5773. https://doi.org/10.1021/bi300468y
Thiel V, Tank M, Bryant DA (2017) Diversity of chlorophototrophic bacteria revealed in the omics era. Annu Rev Plant Biol. https://doi.org/10.1146/annurev-arplant-042817-040500
Tsukatani Y, Romberger SP, Golbeck JH, Bryant DA (2012) Isolation and characterization of homodimeric type-I reaction center complex from Candidatus Chloracidobacterium thermophilum, an aerobic chlorophototroph. J Biol Chem 287:5720–5732. https://doi.org/10.1074/jbc.M111.323329
van Heukelem L, Lewitus AJ, Kana TM, Craft NE (1994) Improved separations of phytoplankton pigments using temperature-controlled high performance liquid chromatography. Mar Ecol Prog Ser 114:304–313
Wakao N, Yokoi N, Isoyama N et al (1996) Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum. Plant cell Physiol 37:889–893. https://doi.org/10.1093/oxfordjournals.pcp.a0290293
Wen J, Tsukatani Y, Cui W, Zhang H, Gross ML, Bryant DA, Blankenship RE (2011) Structural model and spectroscopic characteristics of the FMO antenna protein from the aerobic chlorophototroph, Candidatus Chloracidobacterium thermophilum. Biochim Biophys Acta 1807:157–164. https://doi.org/10.1016/j.bbabio.2010.09.008
Zeng Y, Feng F, Medová H et al (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci USA 111:7795–7800. https://doi.org/10.1073/pnas.1400295111
Zill JC (2017a) Der Festkörper photo-CIDNP-Effekt im Baum des Lebens, Dissertation, Universität Leipzig
Zill JC, Kansy M, Goss R et al (2017b) Photo-CIDNP in the reaction center of the datom Cyclotella meneghiniana observed by 13C MAS NMR. Z Phys Chem 231:347–367. https://doi.org/10.1515/zpch-2016-0806
Zysmilich MG, McDermott A (1994) Photochemically induced dynamic nuclear polarization in the solid-state 15N spectra of reaction centers from photosynthetic bacteria Rhodobacter sphaeroides R-26. J Am Chem Soc 116:8362–8363. https://doi.org/10.1021/ja00097a052
Acknowledgements
The authors thank Dr. Matthias Findeisen for technical assistence, Eva-Maria Höhn (Group of Professor Dr. Detlev Belder, Universität Leipzig) for the Raman measurements, and Prof. Dr. Stefan Berger (Leipzig) for discussions. J.M. acknowledges the generous support of the Deutsche Forschungsgemeinschaft DFG (MA4972/2-1). Studies in the laboratories of D.A.B. and J.H.G. were supported by Grants DE-FG02-94ER20137 and DE-SC0010575, respectively, from the Photosynthetic Systems Program, Division of Chemical Sciences, Geosciences, and Biosciences (CSGB), Office of Basic Energy Sciences of the U. S. Department of Energy. I.S. is supported by the ERC Starting Grant ‘PhotoMutant’ (678169). Y.L would like to thank Dr. Dror Noy (MIGAL) and his financial support from the ERC (GA 615217) and ISF (GA 558/14).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zill, J.C., He, Z., Tank, M. et al. 15N photo-CIDNP MAS NMR analysis of reaction centers of Chloracidobacterium thermophilum. Photosynth Res 137, 295–305 (2018). https://doi.org/10.1007/s11120-018-0504-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-018-0504-1