Advertisement

Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered Photosystem I complexes

  • Vasily Kurashov
  • Ming-Yang Ho
  • Gaozhong Shen
  • Karla Piedl
  • Tatiana N. Laremore
  • Donald A. Bryant
  • John H. GolbeckEmail author
Original Article
  • 117 Downloads

Abstract

Certain cyanobacteria can thrive in environments enriched in far-red light (700–800 nm) due to an acclimation process known as far-red light photoacclimation (FaRLiP). During FaRLiP, about 8% of the Chl a molecules in the photosystems are replaced by Chl f and a very small amount of Chl d. We investigated the spectroscopic properties of Photosystem I (PSI) complexes isolated from wild-type (WT) Synechococcus sp. PCC 7335 and a chlF mutant strain (lacking Chl f synthase) grown in white and far-red light (WL–PSI and FRL–PSI, respectively). WT–FRL–PSI complexes contain Chl f and Chl a but not Chl d. The light-minus dark difference spectrum of the trapping center at high spectral resolution indicates that the special pair in WT–FRL–PSI consists of Chl a molecules with maximum bleaching at 703–704 nm. The action spectrum for photobleaching of the special pair showed that Chl f molecules absorbing at wavelengths up to 800 nm efficiently transfer energy to the trapping center in FRL–PSI complexes to produce a charge-separated state. This is ~ 50 nm further into the near IR than WL–PSI; Chl f has a quantum yield equivalent to that of Chl a in the antenna, i.e., ~ 1.0. PSI complexes from Synechococcus 7002 carrying 3.8 Chl f molecules could promote photobleaching of the special pair by energy transfer at wavelengths longer than WT PSI complexes. Results from these latter studies are directly relevant to the issue of whether introduction of Chl f synthase into plants could expand the wavelength range available for oxygenic photosynthesis in crop plants.

Keywords

Cyanobacteria Photosynthesis Chlorophyll f synthase Action spectrum Quantum yield Far-red light photoacclimation FaRLiP Photosystem I Chlorophyll Cyanobacteria Synechococcus sp. PCC 7002 Synechococcus sp. PCC 7335 

Notes

Acknowledgements

This work was supported by the National Science Foundation Grant MCB-1613022 to D.A.B and J.H.G. This research was also conducted under the auspices of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the DOE, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC 0001035 (D.A.B.).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2019_616_MOESM1_ESM.docx (749 kb)
Supplementary material 1 (DOCX 749 KB)

References

  1. Airs RL, Temperton B, Sambles C, Farnham G, Skill SC, Llewellyn CA (2014) Chlorophyll f and chlorophyll d are produced in the cyanobacterium Chlorogloeopsis fritschii when cultured under natural light and near-infrared radiation. FEBS Lett 588:3770–3777CrossRefGoogle Scholar
  2. Allakhverdiev SI, Tomo T, Shimada Y, Kindo H, Nagao R, Klimov VV, Mimuro M (2010) Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls. Proc Natl Acad Sci USA 107:3924–3929CrossRefGoogle Scholar
  3. Allakhverdiev SI, Kreslavski VD, Zharmukhamedov SK, Voloshin RA, Korol’kova DV, Tomo T, Shen JR (2016) Chlorophylls d and f and their role in primary photosynthetic processes of cyanobacteria. Biochemistry (Moscow) 81:201–212Google Scholar
  4. Behrendt L, Brejnrod A, Schliep M, Sørensen SJ, Larkum AWD, Kühl M (2015) Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium. ISME J 9:2108–2111CrossRefGoogle Scholar
  5. Blankenship RE, Chen M (2013) Spectral expansion and antenna reduction can enhance photosynthesis for energy production. Curr Opin Chem Biol 17:457–461CrossRefGoogle Scholar
  6. Bryant DA (2016) Improving crop yields and algal biofuel production by expanding the wavelength range for photosynthesis. Information Systems for Biotechnology News Report pp 1–6Google Scholar
  7. Chen M (2014) Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Ann Rev Biochem 83:217–340CrossRefGoogle Scholar
  8. Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431CrossRefGoogle Scholar
  9. Cherepanov DA, Shelaev IV, Gostev FE, Mamedov MD, Petrova AA, Aybush AV, Shuvalov VA, Semenov AY, Nadtochenko VA (2017a) Excitation of photosystem I by 760 nm femtosecond laser pulses: transient absorption spectra and intermediates. J Phys B 50:174001CrossRefGoogle Scholar
  10. Cherepanov DA, Shelaev IV, Gostev FE, Mamedov MD, Petrova AA, Aybush AV, Shuvalov VA, Semenov AY, Nadtochenko VA (2017b) Mechanism of adiabatic primary electron transfer in photosystem I: femtosecond spectroscopy upon excitation of reaction center in the far-red edge of the Qy band. Biochim Biophys Acta 1858:895–905CrossRefGoogle Scholar
  11. Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17:3450–3465CrossRefGoogle Scholar
  12. Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317CrossRefGoogle Scholar
  13. Golbeck J (2006) Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase. Springer, DordrechtGoogle Scholar
  14. Golbeck J, Bryant D (1991) Photosystem-I. Curr Topics Bioenerg 16:83–177CrossRefGoogle Scholar
  15. Grotjohann I, Fromme P (2005) Structure of cyanobacterial photosystem I. Photosynth Res 85:51–72CrossRefGoogle Scholar
  16. Herrera-Salgado P, Leyva-Castillo LE, Rios-Castro E, Gomez-Lojero C (2018) Complementary chromatic and far-red photoacclimations in Synechococcus ATCC 29403 (PCC 7335). I: the phycobilisomes, a proteomic approach. Photosynth Res 138:39–56CrossRefGoogle Scholar
  17. Ho M-Y (2018) Characterization of far-red light photoacclimation in cyanobacteria. Biochem Mol Biol 131:173–186Google Scholar
  18. Ho M-Y, Shen G, Canniffe DP, Zhao C, Bryant DA (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353:213–227CrossRefGoogle Scholar
  19. Ho M-Y, Gan F, Shen GZ, Bryant DA (2017a) Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II. Characterization of phycobiliproteins produced during acclimation to far-red light. Photosynth Res 131:187–202CrossRefGoogle Scholar
  20. Ho M-Y, Gan F, Shen GZ, Zhao C, Bryant DA (2017b) Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335: I. regulation of FaRLiP gene expression. Photosynth Res 131:173–186CrossRefGoogle Scholar
  21. Ho M-Y, Soulier NT, Canniffe DP, Shen G, Bryant DA (2017c) Light regulation of pigment and photosystem biosynthesis in cyanobacteria. Curr Opin Plant Biol 37:24–33CrossRefGoogle Scholar
  22. Hou JM, Boichenko VA, Wang YC, Chitnis PR, Mauzerall D (2001) Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: a pulsed photoacoustic study of electron transfer in photosystem I reveals a similarity to bacterial reaction centers in both volume change and entropy. Biochemistry 40:7109–7116CrossRefGoogle Scholar
  23. Itoh S, Mino H, Itoh K, Shigenaga T, Uzumaki T, Iwaki M (2007) Function of chlorophyll d in reaction centers of photosystems I and II of the oxygenic photosynthesis of Acaryochloris marina. Biochemistry 46:12473–12481CrossRefGoogle Scholar
  24. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three dimensional structure of Photosystem I at 2.5 Å resolution. Nature 411:909–917CrossRefGoogle Scholar
  25. Kaucikas M, Nurnberg D, Dorlhiac G, Rutherford AW, van Thor JJ (2017) Femtosecond visible transient absorption spectroscopy of chlorophyll f-containing photosystem I. Biophys J 112:234–249CrossRefGoogle Scholar
  26. Kok B (1956) On the reversible absorption change at 705 nm in photosynthetic organisms. Biochim Biophys Acta 22:399–401CrossRefGoogle Scholar
  27. Kumazaki S, Abiko K, Ikegami I, Iwaki M, Itoh S (2002) Energy equilibration and primary charge separation in chlorophyll d-based photosystem I reaction center isolated from Acaryochloris marina. FEBS Lett 530:153–157CrossRefGoogle Scholar
  28. Lambert DH, Stevens SE Jr (1986) Photoheterotrophic growth of Agmenellum quadruplicatum PR-6. J Bacteriol 165:654–656CrossRefGoogle Scholar
  29. Li Y, Scales N, Blankenship RE, Willows RD, Chen M (2012) Extinction coefficient for red-shifted chlorophylls: chlorophyll d and chlorophyll f. Biochim Biophys Acta 1817:1292–1298CrossRefGoogle Scholar
  30. Li Y, Lin Y, Loughlin PC, Chen M (2014) Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris - a filamentous cyanobacterium containing chlorophyll f. Front Plant Sci 5:67Google Scholar
  31. Li Y, Lin Y, Garvey CJ, Birch D, Corkery RW, Loughlin PC, Scheer H, Willows RD, Chen M (2016) Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim Biophys Acta 1857:107–114CrossRefGoogle Scholar
  32. Li Y, Vella N, Chen M (2018) Characterization of isolated photosystem I from Halomicronema hongdechoris, a chlorophyll f-producing cyanobacterium. Photosynthetica 56:306–315CrossRefGoogle Scholar
  33. Lichtenthaler HK (1987) Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  34. Ludwig M, Bryant DA (2011) Transcription profiling of the cyanobacterium Synechococcus sp. PCC 7002 using high-throughput cDNA sequencing. Front Microbiol 2:41CrossRefGoogle Scholar
  35. Miao D, Ding WL, Zhao BQ, Lu L, Xu QZ, Scheer H, Zhao KH (2016) Adapting photosynthesis to the near-infrared: non-covalent binding of phycocyanobilin provides an extreme spectral red-shift to phycobilisome core-membrane linker from Synechococcus sp. PCC 7335. Biochim Biophys Acta 1857:688–694CrossRefGoogle Scholar
  36. Mielke SP, Kiang NY, Blankenship RE, Mauzerall D (2013) Photosystem trap energies and spectrally-dependent energy-storage efficiencies in the Chl d-utilizing cyanobacterium, Acaryochloris marina. Biochim Biophys Acta 1827:255–265CrossRefGoogle Scholar
  37. Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402CrossRefGoogle Scholar
  38. Muller MG, Slavov C, Luthra R, Redding KE, Holzwarth AR (2010) Independent initiation of primary electron transfer in the two branches of the Photosystem I reaction center. Proc Natl Acad Sci USA 107:4123–4128CrossRefGoogle Scholar
  39. Nurnberg DJ, Morton J, Santabarbara S, Telfer A, Joliot P, Antonaru LA, Ruban AV, Cardona T, Krausz E, Boussac A, Fantuzzi A, Rutherford AW (2018) Photochemistry beyond the red limit in chlorophyll f-containing photosystems. Science 360:1210–1213CrossRefGoogle Scholar
  40. Ortega-Ramos M, Canniffe DP, Radle M, Neil Hunter C, Bryant DA, Golbeck JH (2018) Engineered biosynthesis of bacteriochlorophyll g F in Rhodobacter sphaeroides. Biochim Biophys Acta 1859:501–509CrossRefGoogle Scholar
  41. Razeghifard MR, Chen M, Hughes JL, Freeman J, Krausz E, Wydrzynski T (2005) Spectroscopic studies of photosystem II in chlorophyll d-containing Acaryochloris marina. Biochemistry 44:11178–11187CrossRefGoogle Scholar
  42. Rippka R, Deuuelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  43. Schlodder E, Cetin M, Eckert HJ, Schmitt FJ, Barber J, Telfer A (2007) Both chlorophylls a and d are essential for the photochemistry in photosystem II of the cyanobacteria, Acaryochloris marina. Biochim Biophys Acta 1767:589–595CrossRefGoogle Scholar
  44. Schluchter WM, Shen GH, Zhao JD, Bryant DA (1996) Characterization of psaI and psaL mutants of Synechococcus sp strain PCC 7002: a new model for state transitions in cyanobacteria. Photochem Photobiol 64:53–66CrossRefGoogle Scholar
  45. Schmitt FJ, Campbell ZY, Bui MV, Huls A, Tomo T, Chen M, Maksimov EG, Allakhverdiev SI, Friedrich T (2018) Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light. Photosynth Res.  https://doi.org/10.1007/s11120-11018-10556-11122 Google Scholar
  46. Shen GZ, Bryant DA (1995) Characterization of a Synechococcus sp strain PCC 7002 mutant lacking Photosystem I. Protein assembly and energy distribution in the absence of the Photosystem I reaction center core complex. Photosynth Res 44:41–53CrossRefGoogle Scholar
  47. Shen G, Zhao J, Reimer SK, Antonkine ML, Cai Q, Weiland SM, Golbeck JH, Bryant DA (2002) Assembly of Photosystem I. I. Inactivation of the rubA gene encoding a membrane-associated rubredoxin in the cyanobacterium Synechococcus sp. PCC 7002 causes a loss of Photosystem I activity. J Biol Chem 277:20343–20354CrossRefGoogle Scholar
  48. Shen G, Schluchter WM, Bryant DA (2008) Biogenesis of phycobiliproteins: I. cpcS-I and cpcU mutants of the cyanobacterium Synechococcus sp. PCC 7002 define a heterodimeric phyococyanobilin lyase specific for beta-phycocyanin and allophycocyanin subunits. J Biol Chem 283:7503–7512CrossRefGoogle Scholar
  49. Shen G, Gan F, Bryant DA (2016) The siderophilic cyanobacterium Leptolyngbya sp. strain JSC-1 acclimates to iron starvation by expressing multiple isiA-family genes. Photosynth Res 128:325–340CrossRefGoogle Scholar
  50. Shen G, Canniffe DP, Ho M-Y, Kurashov V, Golbeck JH, Bryant DA (2019) Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002. Photosynth Res.  https://doi.org/10.1007/s11120-018-00610-9 Google Scholar
  51. Sivakumar V, Wang R, Hastings G (2003) Photo-oxidation of P740, the primary electron donor in photosystem I from Acaryochloris marina. Biophys J 85:3162–3172CrossRefGoogle Scholar
  52. Tomo T, Okubo T, Akimoto S, Yokono M, Miyashita H, Tsuchiya T, Noguchi T, Mimuro M (2007) Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc Natl Acad Sci USA 104:7283–7288CrossRefGoogle Scholar
  53. Tomo T, Kato Y, Suzuki T, Akimoto S, Okubo T, Noguchi T, Hasegawa K, Tsuchiya T, Tanaka K, Fukuya M, Dohmae N, Watanabe T, Mimuro M (2008) Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. J Biol Chem 283:18198–18209CrossRefGoogle Scholar
  54. Webber AN, Lubitz W (2001) P700: the primary electron donor of Photosystem I. Biochim Biophys Acta 1507:61–79CrossRefGoogle Scholar
  55. Xu QZ, Han JX, Tang QY, Ding WL, Miao D, Zhou M, Scheer H, Zhao KH (2016) Far-red light photoacclimation: Chromophorylation of FR induced alpha- and beta-subunits of allophycocyanin from Chroococcidiopsis thermalis sp. PCC7203. Biochim Biophys Acta 1857:1607–1616CrossRefGoogle Scholar
  56. Xu QZ, Tang QY, Han JX, Ding WL, Zhao BQ, Zhou M, Gartner W, Scheer H, Zhao KH (2017) Chromophorylation (in Escherichia coli) of allophycocyanin B subunits from far-red light acclimated Chroococcidiopsis thermalis sp. PCC7203. Photochem Photobiol Sci 16:1153–1161CrossRefGoogle Scholar
  57. Zhao C, Gan F, Shen G, Bryant DA (2015) RfpA, RfpB, and RfpC are the master control elements of far-red light photoacclimation (FaRLiP). Front Microbiol 6:1303Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Vasily Kurashov
    • 1
  • Ming-Yang Ho
    • 1
    • 2
  • Gaozhong Shen
    • 1
  • Karla Piedl
    • 1
  • Tatiana N. Laremore
    • 4
  • Donald A. Bryant
    • 1
    • 2
    • 5
  • John H. Golbeck
    • 1
    • 3
    • 6
    Email author
  1. 1.Department of Biochemistry and Molecular BiologyThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Intercollege Graduate Degree Program in Plant BiologyThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Department of ChemistryThe Pennsylvania State UniversityUniversity ParkUSA
  4. 4.Proteomics and Mass Spectrometry Core Facility, The Huck Institutes for the Life SciencesThe Pennsylvania State UniversityUniversity ParkUSA
  5. 5.Department of Chemistry and BiochemistryMontana State UniversityBozemanUSA
  6. 6.328 South Frear Laboratory, Department of Biochemistry and Molecular BiologyThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations