, Volume 56, Issue 1, pp 306–315 | Cite as

Characterization of isolated photosystem I from Halomicronema hongdechloris, a chlorophyll f-producing cyanobacterium

  • Y. Li
  • N. Vella
  • M. ChenEmail author


Halomicronema hongdechloris is a chlorophyll (Chl) f-producing cyanobacterium. Chl f biosynthesis is induced under far-red light, extending its photosynthetically active radiation range to 760 nm. In this study, PSI complexes were isolated and purified from H. hongdechloris, grown under white light (WL) and far-red light (FR), by a combination of density gradient ultracentrifugation and chromatographic separation. WL-PSI showed similar pigment composition as that of Synechocystis 6803, using Chl a in the reaction center. Both Chl a and f were detected in the FR-PSI, although Chl f was a minor component (~8% of total Chl). The FR-PSI showed a maximal fluorescence emission peak of 750 nm at 77 K, which is red-shifted ~20 nm compared to the 730 nm recorded from the WL-PSI. The absorption peaks of P700 for WLPSI and FR-PSI were 699 nm and 702 nm, respectively. The function of Chl f in FR-PSI is discussed.

Additional key words

cyanobacteria far-red light photoacclimation oxygenic photosynthesis red-shifted chlorophyll 





complementary chromatic adaptation




730 nm light-emitting diodes


β-dodecyl maltoside


far-red light photoacclimation


far-red light


isolated PSI from 730 nm LED-illuminated culture








white fluorescent light


isolated PSI from white light culture


purified PSI complexes from Synechocystis 6803


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

11099_2018_776_MOESM1_ESM.pdf (138 kb)
Fig. 1S. The HPLC chromatographs for the sucrose density band isolated from white light (WL) and far red light (FR) grown Halomicronema hongdechloris. The solid black (FR-2) and grey line (FR-1) represent the chromatographs for the FR band 2 and 1 (Fig.1), respectively. The dash black (WL-2) and grey line (WL-1) represent the chromatographs for the WL band 2 and 1 (Fig.1), respectively. Carotenoids, Chl f, Chl a, Chl a’, β-carotene and pheophytin a are assigned based on their retention time and online spectra.
11099_2018_776_MOESM2_ESM.pdf (134 kb)
Fig. 2S. Sequence alignment for PsaL’s detected from isolated PSI complexes of H. hongdechloris. PsaL (1JB0_L) from PSI crystal structure of Synechococcus elongates is used as a reference. The residues ligating chlorophyll a’s are highlighted by asterisk “*”.
11099_2018_776_MOESM3_ESM.pdf (94 kb)
Table 1S. LC-MS/MS peptide determinations for polypeptides resolved on SDS-PAGE (Fig. 3)


  1. Airs R.L., Temperton B., Sambles C. et al.: Chlorophyll f and chlorophyll d are produced in the cyanobacterium Chlorogloeopsis fritschii when cultured under natural light and nearinfrared radiation.–FEBS Lett. 588: 3770–3777, 2014.CrossRefPubMedGoogle Scholar
  2. Akutsu S., Fujinuma D., Furukawa H. et al.: Pigment analysis of a chlorophyll f-containing cyanobacterium strain KC1isolated from Lake Biwa.–Photochem. Photobiol. 33: 35–40, 2011.Google Scholar
  3. Amunts A., Toporik H., Borovikova A. et al.: Structure determination and improved model of plant photosystem I.–J. Biol. Chem. 285: 3478–3486, 2010.CrossRefPubMedGoogle Scholar
  4. Barber J.: Photosynthetic generation of oxygen.–Philos. T. R. Soc. B 363: 2665–2674, 2008.CrossRefGoogle Scholar
  5. Barth P., Lagoutte B., Sétif P.: Ferredoxin reduction by photosystem I from Synechocystis sp. PCC 6803: toward an understanding of the respective roles of subunits PsaD and PsaE in ferredoxin binding.–Biochemistry 37: 16233–16241, 1998.CrossRefPubMedGoogle Scholar
  6. Ben-Shem A., Frolow F., Nelson N.: Crystal structure of plant photosystem I.–Nature 426: 630–635, 2003.CrossRefPubMedGoogle Scholar
  7. Chen M., Blankenship R.: Expanding the solar spectrum used by photosynthesis.–Trends Plant Sci. 16: 427–431, 2011.CrossRefPubMedGoogle Scholar
  8. Chen M., Li Y., Birch D. et al: A cyanobacterium that contains chlorophyll f–a red-absorbing photopigment.–FEBS Lett. 586: 3249–3254, 2012.CrossRefPubMedGoogle Scholar
  9. Chen M., Schliep M., Willows R. et al: A red-shifted chlorophyll.–Science 329: 1318–1319, 2010.CrossRefPubMedGoogle Scholar
  10. Croce R., van Amerongen H.: Light-harvesting in photosystem I.–Photosynth. Res. 116: 153–166, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  11. El-Khouly M.E., El-Mohsnawy E., Fukuzumi S.: Solar energy conversion: From natural to artificial photosynthesis.–J. Photoch. Photobio. C 31: 36–83, 2017.CrossRefGoogle Scholar
  12. El-Mohsnawy E., Kopczak M.J., Schlodder E. et al.: Structure and function of intact photosystem I monomers from the cyanobacterium Thermosynechococcus elongatus.–Biochemistry49: 4740–4751, 20CrossRefPubMedGoogle Scholar
  13. Fromme P., Jordan P., Krauß N.: Structure of photosystem I.–BBA-Bioenergetics 1507: 5–31, 2001.CrossRefPubMedGoogle Scholar
  14. Gan F., Bryant D.A.: Adaptive and acclimative responses of cyanobacteria to far-red light.–Environ. Microbiol. 17: 3450–3465, 2015.CrossRefPubMedGoogle Scholar
  15. Gan F., Zhang S., Rockwell N.C. et al.: Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light.–Science 345: 1312–1317, 2014.CrossRefPubMedGoogle Scholar
  16. Golbeck, J.H.: Photosystem I in cyanobacteria.–In: Bryant D.A. (ed.): The Molecular Biology of Cyanobacteria. Pp. 319–360. Springer, Dordrecht 1994.CrossRefGoogle Scholar
  17. Golub M., Hejazi M., Kölsch A. et al.: Solution structure of monomeric and trimeric photosystem I of Thermosynechococcus elongatus investigated by small-angle X-ray scattering.–Photosynth. Res. 133: 163–173, 2017.CrossRefPubMedGoogle Scholar
  18. Goodwint W.: Biochemistry of pigments.–In Waterman T.H. (ed.): The Physiology of Crustacea. Pp. 101–140. Academic Press, New York and London 1960.Google Scholar
  19. Grotjohann I., Fromme P.: Structure of cyanobacterial photosystem I.–Photosynth. Res. 85: 51–72, 2005.CrossRefPubMedGoogle Scholar
  20. Hiyama T., Ke B.: Difference spectra and extinction coefficients of P 700.–BBA-Bioenergetics. 267: 160–171, 1972.CrossRefPubMedGoogle Scholar
  21. Hou H.J., Allakhverdiev S.I., Najafpour M.M. et al.: Current challenges in photosynthesis: from natural to artificial.–Front Plant Sci. 5: 232, 2014.PubMedPubMedCentralGoogle Scholar
  22. Hu Q., Miyashita H., Iwasaki I. et al: A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis.–P. Natl. Acad. Sci. USA 95: 13319–13323, 1998.CrossRefGoogle Scholar
  23. Jordan P., Fromme P., Witt H.T. et al.: Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution.–Nature 411: 909–917, 2001.CrossRefPubMedGoogle Scholar
  24. Kruip J., Boekema E.J., Bald D. et al.: Isolation and structural characterization of monomeric and trimeric photosystem I complexes (P700. FA/FB and P700. FX) from the cyanobacterium Synechocystis PCC 6803.–J. Biol. Chem. 268: 23353–23360, 1993.PubMedGoogle Scholar
  25. Li M, Semchonok D.A., Boekema E.J., Bruce B.D.: Characterization and evolution of tetrameric photosystem I from the thermophilic cyanobacterium Chroococcidiopsis sp TS-821.–Plant Cell 26: 1230–1245, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Li Y., Cai Z.-L. Chen M.: Spectroscopic properties of chlorophyll f.–J. Phys. Chem. B 117: 11309–11317, 2013.CrossRefPubMedGoogle Scholar
  27. Li Y., Chen M.: Novel chlorophylls and new directions in photosynthesis research.–Funct. Plant Biol. 42: 493–501, 2015.CrossRefGoogle Scholar
  28. Li Y., Lin Y., Garvey C.J. et al.: Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris.–BBABioenergetics 1857: 107–114, 20CrossRefGoogle Scholar
  29. Li Y., Lin Y., Loughlin P. et al.: Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris–a filamentous cyanobacterium containing chlorophyll f.–Front. Plant Sci. 5: 67, 2014.PubMedPubMedCentralGoogle Scholar
  30. Li Y., Scales N., Blankenship R. E. et al.: Extinction coefficient for red-shifted chlorophylls: chlorophyll d and chlorophyll f.–BBA-Bioenergetics 1817: 1292–1298, 2012.CrossRefPubMedGoogle Scholar
  31. Miyashita H., Ikemoto H., Kurano N. et al.: Chlorophyll d as a major pigment.–Nature 383: 402, 1996.CrossRefGoogle Scholar
  32. Mühlenhoff U., Zhao J., Bryant D.A.: Interaction between photosystem I and flavodoxin from the cyanobacterium Synechococcus sp. PCC 7002 as revealed by chemical crosslinking.–Eur. J. Biochem. 235: 324–331, 1996.CrossRefPubMedGoogle Scholar
  33. Nelson N., Junge W.: Structure and energy transfer in photosystems of oxygenic photosynthesis.–Annu. Rev. Biochem. 84: 659–683, 2015.CrossRefPubMedGoogle Scholar
  34. Nyhus K.J., Ikeuchi M., Inoue Y. et al.: Purification and characterization of the photosystem I complex from the filamentous cyanobacterium Anabaena variabilis ATCC 29413.–J. Biol. Chem. 267: 12489–12495, 1992.PubMedGoogle Scholar
  35. Ohkubo S., Miyashita H.: A niche for cyanobacteria producing chlorophyll f within a microbial mat.–ISME J. 11: 2368–2378, 2017.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rögner M., Nixon P.J., Diner B.A.: Purification and characterization of photosystem I and photosystem II core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC 6803.–J. Biol. Chem. 265: 6189–6196, 1990.PubMedGoogle Scholar
  37. Schluchter W.M., Shen G., Zhao J., Bryant D.A.: Characterization of psal and psaL mutants of Synechococcus sp. strain PCC 7002: a new model for state transitions in cyanobacteria.–Photochem. Photobiol. 64: 53–66, 1996.CrossRefPubMedGoogle Scholar
  38. Sivakumar V., Wang R., Hastings G.: Photo-oxidation of P740, the primary electron donor in photosystem I from Acaryochloris marina.–Biophys. J. 85: 3162–3172, 20CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tomo T., Kato Y., Suzuki T. et al.: Characterization of highly purified photosystem I complexes from the chlorophyll ddominated cyanobacterium Acaryochloris marina MBIC 11017.–J. Biol. Chem. 283: 18198–18209, 2008.CrossRefPubMedGoogle Scholar
  40. Xu Q., Hoppe D., Chitnis V.P. et al.: Mutational analysis of photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. Targeted inactivation of psaI reveals the function of psaI in the structural organization of psaL.–J. Biol. Chem. 270: 16243–16250, 1995.CrossRefPubMedGoogle Scholar
  41. Xu W., Chitnis P., Valieva A. et al.: Electron transfer in cyanobacterial photosystem I: I. Physiological and spectroscopic characterization of site-directed mutants in a putative electron transfer pathway from A0 through A1 to FX.–J. Biol. Chem. 278: 27864–27875, 2003.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.School of Life and Environmental ScienceUniversity of SydneyNSWAustralia

Personalised recommendations