Skip to main content
SpringerLink
Log in

Molecular Mechanism of Photosynthesis Driven by Red-Shifted Chlorophylls

  • Chapter
  • First Online:
Microbial Photosynthesis

Abstract

Photosynthesis is the process of light-driven production of organic molecules needed as starting components for whole cellular processes and as the energy source. It is carried out by primary producers including land plants, algae, and oxygenic/anoxygenic photosynthetic bacteria. Oxygenic photosynthesis involves two stages: light-dependent reactions generating NADPH and ATP molecules with oxygen as a by-product and light-independent reactions involving utilization of NADPH and ATP as the energy source to convert carbon dioxide into organic molecules. Light-dependent processes require light-absorbing pigments categorized as carotenoids, bilins, and chlorophylls. Chlorophylls and carotenoids are ubiquitous to all photosynthetic organisms, while bilins in phycobiliprotein complexes are specific to cyanobacteria, rhodophytes, glaucophytes, and cryptophytes. Each pigment has several variations, and a particular type of organism has a specific set optimized for light-capture and photosynthetic efficiency in the given environment. The common chlorophyll to each oxygenic photosynthetic organism is chlorophyll a, with chlorophyll b, c, d, or f synthesized depending on the organism. Chlorophyll d (3-formyl-chlorophyll a) and chlorophyll f (2-formyl-chlorophyll a) have far-red long-wavelength absorption features, namely, red-shifted chlorophylls. These chlorophyll molecules enable some cyanobacterial species to grow in shaded environments and establish unique habitats. Acaryochloris marina is predominantly a chlorophyll d-containing cyanobacterium with minor (≤ 5%) amounts of chlorophyll a under all culture conditions, while all chlorophyll f-producing cyanobacteria constitute chlorophyll f as a minor chlorophyll ~2–15% of the total chlorophyll pool and only produced under far-red light conditions. This chapter will focus on summarizing the current knowledge of the light-dependent processes with particular attention on structures and functions of far-red absorbing pigments and pigment-binding protein complexes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

APC:

Allophycocyanin

CBP:

Chlorophyll a-/b-binding protein

Chl:

Chlorophyll

CHLF:

Chlorophyll f synthase

FaRLiP:

Far-red light-induced photoacclimation

FRL:

Far-red light

IsiA:

Iron-stress induced chlorophyll-binding protein

LHC:

Light-harvesting protein complex

PAR:

Photosynthetically active radiation

PBP:

Phycobiliprotein

PBS:

Phycobilisome

PC:

Phycocyanin

Pcb:

Prochlorophyte chlorophyll a-/b-binding protein complexes

PE:

Phycoerythrin

PEC:

Phycoerythrocyanin

Pheo a:

Pheophytin a

PS:

Photosystem

QA:

Plastoquinone A

RC:

Reaction center

References

  • Airs, R. L., Temperton, B., Sambles, C., Farnham, G., Skill, S. C., & Llewellyn, C. A. (2014). Chlorophyll f and chlorophyll d are produced in the cyanobacterium Chlorogloeopsis fritschii when cultured under natural light and near-infrared radiation. FEBS Letters, 588, 3770–3777.

    CAS  PubMed  Google Scholar 

  • Akiyama, M., Miyashita, H., Kise, H., Watanabe, T., Miyachi, S., & Kobayashi, M. (2001). Detection of chlorophyll d′ and pheophytin a in a chlorophyll d-dominating oxygenic photosynthetic prokaryote Acaryochloris marina. Analytical Sciences, 17, 205–208.

    CAS  PubMed  Google Scholar 

  • Akutsu, S., Fujinuma, D., Furukawa, H., Watanabe, T., Ohnishi-Kameyama, M., Ono, H., Ohkubo, S., Miyashita, H., & Kobayashi, M. (2011). Pigment analysis of a chlorophyll f-containing cyanobacterium strain KC1 isolated from Lake Biwa. Photomedicine and Photobiology, 33, 35–40.

    CAS  Google Scholar 

  • Allakhverdiev, S. I., Tomo, T., Shimada, Y., Kindo, H., Nagao, R., Klimov, V. V., & Mimuro, M. (2010). Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls. Proceedings of the National Academy of Sciences, USA, 107, 3924–3929.

    CAS  Google Scholar 

  • Allen, J. F. (2014). Origin of oxygenic photosynthesis from anoxygenic type I and type II reaction centers. In J. Golbeck & A. Van Der Est (Eds.), The biophysics of photosynthesis. New York: Springer.

    Google Scholar 

  • Allen, J. P., & Williams, J. C. (2011). The evolutionary pathway from anoxygenic to oxygenic photosynthesis examined by comparison of the properties of photosystem II and bacterial reaction centers. Photosynthesis Research, 107, 59–69.

    CAS  PubMed  Google Scholar 

  • Andrizhiyevskaya, E. G., Schwabe, T. M. E., Germano, M., D’haene, S., Kruip, J., Van Grondelle, R., & Dekker, J. P. (2002). Spectroscopic properties of PSI–IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1556, 265–272.

    CAS  Google Scholar 

  • Archibald, J. O. H. N. M. (2015). Endosymbiosis and eukaryotic cell evolution. Current Biology, 25, R911–R921.

    CAS  PubMed  Google Scholar 

  • Arnon, D. I. (1984). The discovery of photosynthetic phosphorylation. Trends in Biochemical Sciences, 9, 258–262.

    CAS  Google Scholar 

  • Ballottari, M., Girardon, J., Dall’osto, L., & Bassi, R. (2012). Evolution and functional properties of photosystem II light harvesting complexes in eukaryotes. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817, 143–157.

    CAS  Google Scholar 

  • Bautista, J. A., Hiller, R. G., Sharples, F. P., Gosztola, D., Wasielewski, M., & Frank, H. A. (1999). Singlet and triplet energy transfer in the peridinin-chlorophyll a protein from Amphidinium carterae. The Journal of Physical Chemistry. A, 103, 2267–2273.

    CAS  Google Scholar 

  • Bazzaz, M. B., & Brereton, R. G. (1982). 4-Vinyl-4-desethyl chlorophyll a: A new naturally occurring chlorophyll. FEBS Letters, 138, 104–108.

    CAS  Google Scholar 

  • Behrendt, L., Larkum, A. W. D., Norman, A., Qvortrup, K., Chen, M., Ralph, P., Sørensen, S. J., Trampe, E., & Kühl, M. (2011). Endolithic chlorophyll d-containing phototrophs. The ISME Journal, 5, 1072–1076.

    CAS  PubMed  Google Scholar 

  • Bibby, T. S., Nield, J., & Barber, J. (2001a). Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature, 412, 743–745.

    CAS  PubMed  Google Scholar 

  • Bibby, T. S., Nield, J., Partensky, F., & Barber, J. (2001b). Antenna ring around photosystem I. Nature, 413, 590–590.

    CAS  PubMed  Google Scholar 

  • Bibby, T. S., Mary, I., Nield, J., Partensky, F., & Barber, J. (2003a). Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature, 424, 1051–1054.

    CAS  PubMed  Google Scholar 

  • Bibby, T. S., Nield, J., Chen, M., Larkum, A. W. D., & Barber, J. (2003b). Structure of a photosystem II supercomplex isolated from Prochloron didemni retaining its chlorophyll a/b light-harvesting system. Proceedings of the National Academy of Sciences, USA, 100, 9050–9054.

    CAS  Google Scholar 

  • Blankenship, R. E. (2002). Molecular mechanisms of photosynthesis. Oxford: Blackwell Science.

    Google Scholar 

  • Boekema, E. J., Hifney, A., Yakushevska, A. E., Piotrowski, M., Keegstra, W., Berry, S., Michel, K.-P., Pistorius, & E. K., Kruip, J. (2001). A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria. Nature, 412, 745–748.

    Google Scholar 

  • Brejc, K., Ficner, R., Huber, R., & Steinbacher, S. (1995). Isolation, crystallization, crystal structure analysis and refinement of allophycocyanin from the cyanobacterium Spirulina platensis at 2.3 Å resolution. Journal of Molecular Biology, 249, 424–440.

    CAS  PubMed  Google Scholar 

  • Bricker, W. P., & Lo, C. S. (2015). Efficient pathways of excitation energy transfer from delocalized S2 excitons in the peridinin–chlorophyll a–protein complex. The Journal of Physical Chemistry. B, 119, 5755–5764.

    CAS  PubMed  Google Scholar 

  • Bricker, T. M., Roose, J. L., Fagerlund, R. D., Frankel, L. K., & Eaton-Rye, J. J. (2012). The extrinsic proteins of photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817, 121–142.

    CAS  Google Scholar 

  • Broderick, J. B., Duffus, B. R., Duschene, K. S., & Shepard, E. M. (2014). Radical S-adenosylmethionine enzymes. Chemical Reviews, 114, 4229–4317.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bryant, D. A. (1982). Phycoerythrocyanin and phycoerythrin: Properties and occurrence in cyanobacteria. Microbiology, 128, 835–844.

    CAS  Google Scholar 

  • Bryant, D. A., & Frigaard, N.-U. (2006). Prokaryotic photosynthesis and phototrophy illuminated. Trends in Microbiology, 14, 488–496.

    CAS  PubMed  Google Scholar 

  • Büchel, C. (2019). Light harvesting complexes in chlorophyll c-containing algae. Biochimica et Biophysica Acta (BBA) – Bioenergetics, In Press. https://doi.org/10.1016/j.bbabio.2019.05.003.

  • Burger-Wiersma, T., Veenhuis, M., Korthals, H. J., Van De Wiel, C. C. M., & Mur, L. R. (1986). A new prokaryote containing chlorophylls a and b. Nature, 320, 262–264.

    CAS  Google Scholar 

  • Burger-Wiersma, T., Stal, L. J., & Mur, L. R. (1989). Prochlorthrix hollandica gen. nov. sp. nov., a filamentous oxygenic photoautotrophic procaryote containing chlorophylls a and b: Assignment to Prochlorotrichaceae fam. nov. and order Prochlorales Florenzano, Balloni, and Materassi 1986, with emendation of the ordinal description. International Journal of Systematic and Evolutionary Microbiology, 39, 250–257.

    Google Scholar 

  • Burnap, R. L., Troyan, & T., Sherman, L. A. (1993). The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43’) is encoded by the isiA gene. Plant Physiology, 103, 893–902.

    Google Scholar 

  • Caffarri, S., Tibiletti, T., Jennings, R. C., & Santabarbara, S. (2014). A comparison between plant photosystem I and photosystem II architecture and functioning. Current Protein & Peptide Science, 15, 296–331.

    CAS  Google Scholar 

  • Cardona, T., Murray, J. W., & Rutherford, A. W. (2015). Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Molecular Biology and Evolution, 32, 1310–1328.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castenholz, R. W. (2001). Oxygenic photosynthetic Bacteria. In D. R. Boone, R. W. Castenholz, & G. Gm (Eds.), Bergey’s manual of systematic bacteriology. Volume 1: The Archaea and the deeply branching and phototrophic Bacteria. New York: Springer-Verlag.

    Google Scholar 

  • Cavalier-Smith, T. (2018). Kingdom Chromista and its eight phyla: A new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences. Protoplasma, 255, 297–357.

    CAS  PubMed  Google Scholar 

  • Chang, L., Liu, X., Li, Y., Liu, C.-C., Yang, F., Zhao, J., & Sui, S.-F. (2015). Structural organization of an intact phycobilisome and its association with photosystem II. Cell Research, 25, 726–737.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman, D. J. (1966). The pigments of the symbiotic algae (cyanomes) of Cyanophora paradoxa and Glaucocystis nostochinearum and two Rhodophyceae, Porphyridium aerugineum and Asterocytis ramosa. Archiv für Mikrobiologie, 55, 17–25.

    CAS  Google Scholar 

  • Chen, M. (2019). Chlorophylls d and f: Synthesis, occurrence, light-harvesting, and pigment organization in chlorophyll-binding protein complexes. Advances in Botanical Research, 90, 121–139.

    CAS  Google Scholar 

  • Chen, M., & Bibby, T. S. (2005). Photosynthetic apparatus of antenna-reaction centres supercomplexes in oxyphotobacteria: Insight through significance of Pcb/IsiA proteins. Photosynthesis Research, 86, 165–173.

    CAS  PubMed  Google Scholar 

  • Chen, M., & Blankenship, R. E. (2011). Expanding the solar spectrum used by photosynthesis. Trends in Plant Science, 16, 427–431.

    CAS  PubMed  Google Scholar 

  • Chen, M., & Scheer, H. (2013). Extending the limits of natural photosynthesis and implications for technical light harvesting. Journal of Porphyrins and Phthalocyanines, 17, 1–15.

    Google Scholar 

  • Chen, M., Quinnell, R. G., & Larkum, A. W. D. (2002). The major light-harvesting pigment protein of Acaryochloris marina. FEBS Letters, 514, 149–152.

    CAS  PubMed  Google Scholar 

  • Chen, M., Bibby, T. S., Nield, J., Larkum, A., & Barber, J. (2005a). Iron deficiency induces a chlorophyll d-binding Pcb antenna system around photosystem I in Acaryochloris marina. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1708, 367–374.

    CAS  Google Scholar 

  • Chen, M., Bibby, T. S., Nield, J., Larkum, A. W. D., & Barber, J. (2005b). Structure of a large photosystem II supercomplex from Acaryochloris marina. FEBS Letters, 579, 1306–1310.

    CAS  PubMed  Google Scholar 

  • Chen, M., Hiller, R. G., Howe, C. J., & Larkum, A. W. D. (2005c). Unique origin and lateral transfer of prokaryotic chlorophyll-b and chlorophyll-d light-harvesting systems. Molecular Biology and Evolution, 22, 21–28.

    PubMed  Google Scholar 

  • Chen, M., Telfer, A., Lin, S., Pascal, A., Larkum, A. W. D., Barber, J., & Blankenship, R. E. (2005d). The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. Photochemical & Photobiological Sciences, 4, 1060–1064.

    CAS  Google Scholar 

  • Chen, M., Zhang, Y., & Blankenship, R. E. (2008). Nomenclature for membrane-bound light-harvesting complexes of cyanobacteria. Photosynthesis Research, 95, 147–154.

    CAS  PubMed  Google Scholar 

  • Chen, M., Floetenmeyer, M., & Bibby, T. S. (2009). Supramolecular organization of phycobiliproteins in the chlorophyll d-containing cyanobacterium Acaryochloris marina. FEBS Letters, 583, 2535–2539.

    CAS  PubMed  Google Scholar 

  • Chen, M., Schliep, M., Willows, R. D., Cai, Z.-L., Neilan, B. A., & Scheer, H. (2010). A red-shifted chlorophyll. Science, 329, 1318–1319.

    CAS  PubMed  Google Scholar 

  • Chen, M., Li, Y., Birch, D., & Willows, R. D. (2012). A cyanobacterium that contains chlorophyll f – A red-absorbing photopigment. FEBS Letters, 586, 3249–3254.

    CAS  PubMed  Google Scholar 

  • Chen, M., Hernández-Prieto, M. A., Loughlin, P. C., Li, Y., & Willows, R. D. (2019). Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptative proteomic shifts under different light conditions. BMC Genomics, 20, 207.

    PubMed  PubMed Central  Google Scholar 

  • Chisholm, S. W., Olson, R. J., Zettler, E. R., Goericke, R., Waterbury, J. B., & Welschmeyer, N. A. (1988). A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature, 334, 340–343.

    Google Scholar 

  • Chisholm, S. W., Frankel, S. L., Goericke, R., Olson, R. J., Palenik, B., Waterbury, J. B., West-Johnsrud, L., & Zettler, E. R. (1992). Prochlorococcus marinus nov. gen. nov. sp.: An oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Archives of Microbiology, 157, 297–300.

    CAS  Google Scholar 

  • Christ, B., & Hörtensteiner, S. (2014). Mechanism and significance of chlorophyll breakdown. Journal of Plant Growth Regulation, 33, 4–20.

    CAS  Google Scholar 

  • De Los Ríos, A., Grube, M., Sancho, L. G., & Ascaso, C. (2007). Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiology Ecology, 59, 386–395.

    Google Scholar 

  • Demmig-Adams, B. (1990). Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1020, 1–24.

    CAS  Google Scholar 

  • Dolganov, N. A., Bhaya, D., & Grossman, A. R. (1995). Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: Evolution and regulation. Proceedings of the National Academy of Sciences, USA, 92, 636–640.

    CAS  Google Scholar 

  • Domonkos, I., Kis, M., Gombos, Z., & Ughy, B. (2013). Carotenoids, versatile components of oxygenic photosynthesis. Progress in Lipid Research, 52, 539–561.

    CAS  PubMed  Google Scholar 

  • Eaton-Rye, J. J., & Putnam-Evans, C. (2005). The CP47 and CP43 core antenna components. In T. J. Wydrzynski, K. Satoh, & J. A. Freeman (Eds.), Photosystem II: The light-driven water: Plastoquinone oxidoreductase. Dordrecht: Springer Netherlands.

    Google Scholar 

  • Eaton-Rye, J. J., & Sobotka, R. (2017). Editorial: Assembly of the photosystem II membrane-protein complex of oxygenic photosynthesis. Frontiers in Plant Science, 8, 1–4.

    Google Scholar 

  • Fleming, E. D., & Prufert-Bebout, L. (2010). Characterization of cyanobacterial communities from high-elevation lakes in the Bolivian Andes. Journal of Geophysical Research, 115.

    Google Scholar 

  • Frigaard, N.-U., & Dahl, C. (2008). Sulfur metabolism in phototrophic sulfur bacteria. Advances in Microbial Physiology, 54, 103–200.

    Google Scholar 

  • Gan, F., Zhang, S., Rockwell, N. C., Martin, S. S., Lagarias, J. C., & Bryant, D. A. (2014). Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science, 345, 1312–1317.

    CAS  PubMed  Google Scholar 

  • Gan, F., Shen, G., & Bryant, D. A. (2015). Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life, 5, 4–24.

    CAS  Google Scholar 

  • Gao, J., Wang, H., Yuan, Q., & Feng, Y. (2018). Structure and function of the photosystem supercomplexes. Frontiers in Plant Science, 9, 357.

    PubMed  PubMed Central  Google Scholar 

  • Garczarek, L., Hess, W. R., Holtzendorff, J., Van Der Staay, G. W., & Partensky, F. (2000). Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proceedings of the National Academy of Sciences, USA, 97, 4098–4101.

    CAS  Google Scholar 

  • Garg, H., Loughlin, P. C., Willows, R. D., & Chen, M. (2017). The C21-formyl group in chlorophyll f originates from molecular oxygen. Journal of Biological Chemistry, 292, 19279–19289.

    CAS  PubMed  Google Scholar 

  • Garrido, J. L., Otero, J., Meaestro, M. A., & Zapata, M. (2000). The main nonpolar chlorophyll c from Emiliania huxleyi (Prymnesiophyceae) is a chlorophyll c2-monogalactosyl diacylglyceride ester: A mass spectrometry study. Journal of Phycology, 36, 497–505.

    CAS  PubMed  Google Scholar 

  • Giddings, T. H., Wasmann, C., & Staehelin, L. A. (1983). Structure of the thylakoids and envelope membranes of the cyanelles of Cyanophora paradoxa. Plant Physiology, 71, 409–419.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glazer, A. N. (1977). Structure and molecular organization of the photosynthetic accessory pigments of cyanobacteria and red algae. Molecular and Cellular Biochemistry, 18, 125–140.

    CAS  PubMed  Google Scholar 

  • Glazer, A. N. (1985). Light harvesting by phycobilisomes. Annual Review of Biophysics and Biophysical Chemistry, 14, 47–77.

    CAS  PubMed  Google Scholar 

  • Glazer, A. N., & Wedemayer, G. J. (1995). Cryptomonad biliproteins — An evolutionary perspective. Photosynthesis Research, 46, 93–105.

    CAS  PubMed  Google Scholar 

  • Goericke, R., & Repeta, D. J. (1992). The pigments of Prochlorococcus marinus: The presence of divinylchlorophyll a and b in a marine procaryote. Limnology and Oceanography, 37, 425–433.

    CAS  Google Scholar 

  • Goericke, R., & Repeta, D. J. (1993). Chlorophylls a and b and divinyl chlorophylls a and b in the open subtropical North Atlantic Ocean. Marine Ecology Progress Series, 101, 307–313.

    Google Scholar 

  • Goh, F., Allen, M. A., Leuko, S., Kawaguchi, T., Decho, A. W., Burns, B. P., & Neilan, B. A. (2008). Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay. The ISME Journal, 3, 383.

    PubMed  Google Scholar 

  • Golub, M., Combet, S., Wieland, D. C. F., Soloviov, D., Kuklin, A., Lokstein, H., Schmitt, F. J., Olliges, R., Hecht, M., Eckert, H. J., & Pieper, J. (2017). Solution structure and excitation energy transfer in phycobiliproteins of Acaryochloris marina investigated by small angle scattering. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1858, 318–324.

    CAS  Google Scholar 

  • Gomelsky, M., & Hoff, W. D. (2011). Light helps bacteria make important lifestyle decisions. Trends in Microbiology, 19, 441–448.

    CAS  PubMed  Google Scholar 

  • Goss, R., & Jakob, T. (2010). Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynthesis Research, 106, 103–122.

    CAS  PubMed  Google Scholar 

  • Green, B. R. (2011). After the primary endosymbiosis: An update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynthesis Research, 107, 103–115.

    CAS  PubMed  Google Scholar 

  • Grossman, A. R., Schaefer, M. R., Chiang, G. G., & Collier, J. L. (1993). The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiological Reviews, 57, 725–749.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grossman, A. R., Schwarz, R., Bhaya, D., & Dolganov, N. (1998). Phycobilisome degradation and responses of cyanobacteria to nutrient limitation and high light. In G. Garab (Ed.), Photosynthesis: Mechanisms and effects: Volume I–V: Proceedings of the XIth international congress on photosynthesis, Budapest, Hungary, August 17–22, 1998 (pp. 2853–2858). Dordrecht: Springer.

    Google Scholar 

  • Guan, X., Qin, S., Zhao, F., Zhang, X., & Tang, X. (2007). Phycobilisomes linker family in cyanobacterial genomes: Divergence and evolution. International Journal of Biological Sciences, 3, 434–445.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guglielmi, G., Cohen-Bazire, G., & Bryant, D. A. (1981). The structure of Gloeobacter violaceus and its phycobilisomes. Archives of Microbiology, 129, 181–189.

    CAS  Google Scholar 

  • Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., & Saenger, W. (2009). Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nature Structural & Molecular Biology, 16, 334–342.

    CAS  Google Scholar 

  • Harada, J., Mizoguchi, T., Satoh, S., Tsukatani, Y., Yokono, M., Noguchi, M., Tanaka, A., & Tamiaki, H. (2013). Specific gene bciD for C7-methyl oxidation in bacteriochlorophyll e biosynthesis of brown-colored green sulfur bacteria. PLoS One, 8, e60026.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hashimoto, H., Uragami, C., & Cogdell, R. J. (2016). Carotenoids and photosynthesis. In C. Stange (Ed.), Carotenoids in nature: Biosynthesis, regulation and function. Cham: Springer.

    Google Scholar 

  • Hauska, G., Schoedl, T., Remigy, H., & Tsiotis, G. (2001). The reaction center of green sulfur bacteria. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1507, 260–277.

    CAS  Google Scholar 

  • Hecks, B., Wulf, K., Breton, J., Leibl, W., & Trissl, H.-W. (1994). Primary charge separation in photosystem I: A two-step electrogenic charge separation connected with P700+A0− and P700+A1− formation. Biochemistry, 33, 8619–8624.

    CAS  PubMed  Google Scholar 

  • Hernández-Prieto, M. A., Li, Y., Postier, B. L., Blankenship, R. E., & Chen, M. (2018). Far-red light promotes biofilm formation in the cyanobacterium Acaryochloris marina. Environmental Microbiology, 20, 535–545.

    PubMed  Google Scholar 

  • Herrera-Salgado, P., Leyva-Castillo, L. E., Ríos-Castro, E., & Gómez-Lojero, C. (2018). Complementary chromatic and far-red photoacclimations in Synechococcus ATCC 29403 (PCC 7335). I: The phycobilisomes, a proteomic approach. Photosynthesis Research, 138, 39–56.

    CAS  PubMed  Google Scholar 

  • Ho, M.-Y., Shen, G., Canniffe, D. P., Zhao, C., & Bryant, D. A. (2016). Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science, 353, aaf9178.

    PubMed  Google Scholar 

  • Ho, M.-Y., Gan, F., Shen, G., & Bryant, D. A. (2017a). Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II.Characterization of phycobiliproteins produced during acclimation to far-red light. Photosynthesis Research, 131, 187–202.

    CAS  PubMed  Google Scholar 

  • Ho, M.-Y., Soulier, N. T., Canniffe, D. P., Shen, G., & Bryant, D. A. (2017b). Light regulation of pigment and photosystem biosynthesis in cyanobacteria. Current Opinion in Plant Biology, 37, 24–33.

    CAS  PubMed  Google Scholar 

  • Holt, A. S., & Morley, H. V. (1959). A proposed structure for chlorophyll d. Canadian Journal of Chemistry, 37, 507–514.

    CAS  Google Scholar 

  • Hoober, J. K., Eggink, L. L., & Chen, M. (2007). Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts. Photosynthesis Research, 94, 387–400.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hörtensteiner, S., & Kräutler, B. (2011). Chlorophyll breakdown in higher plants. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1807, 977–988.

    Google Scholar 

  • Hörtensteiner, S., Hauenstein, M., & Kräutler, B. (2019). Chlorophyll breakdown—Regulation, biochemistry and phyllobilins as its products. Advances in Botanical Research, 90, 213–271.

    Google Scholar 

  • Hu, Q., Miyashita, H., Iwasaki, I., Kurano, N., Miyachi, S., Iwaki, M., & Itoh, S. (1998). A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proceedings of the National Academy of Sciences, USA, 95, 13319–13323.

    CAS  Google Scholar 

  • Hu, Q., Marquardt, J., Iwasaki, I., Miyashita, H., Kurano, N., Mörschel, E., & Miyachi, S. (1999). Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1412, 250–261.

    CAS  Google Scholar 

  • Hynninen, P. H. (1991). Chemistry of chlorophylls: Modifications. In H. Scheer (Ed.), Chlorophylls. Boca Raton: CRC Press.

    Google Scholar 

  • Ihalainen, J. A., D’haene, S., Yeremenko, N., Van Roon, H., Arteni, A. A., Boekema, E. J., Van Grondelle, R., Matthijs, H. C. P., & Dekker, J. P. (2005). Aggregates of the chlorophyll-binding protein IsiA (CP43‘) dissipate energy in cyanobacteria. Biochemistry, 44, 10846–10853.

    CAS  PubMed  Google Scholar 

  • Ito, H., Ohtsuka, T., & Tanaka, A. (1996). Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. Journal of Biological Chemistry, 271, 1475–1479.

    CAS  PubMed  Google Scholar 

  • Jeffrey, S. W. (1969). Properties of two spectrally different components in chlorophyll c preparations. Biochimica et Biophysica Acta, 177, 456–467.

    CAS  PubMed  Google Scholar 

  • Jeffrey, S. W. (1972). Preparation and some properties of crystalline chlorophyll c1 and c2 from marine algae. Biochimica et Biophysica Acta, 279, 15–33.

    CAS  PubMed  Google Scholar 

  • Jeffrey, S. W. (1976). The occurrence of chlorophyll c1 and c2 in algae. Journal of Phycology, 12, 349–354.

    CAS  Google Scholar 

  • Jeffrey, S. W., & Wright, S. W. (1987). A new spectrally distinct component in preparations of chlorophyll c from the micro-alga Emiliania huxleyi (Prymnesiophycease). Biochimica et Biophysica Acta (BBA) – Bioenergetics, 894, 180–188.

    CAS  Google Scholar 

  • Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., & Krauß, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature, 411, 909–917.

    CAS  PubMed  Google Scholar 

  • Kashiyama, Y., Miyashita, H., Ohkubo, S., Ogawa, N. O., Chikaraishi, Y., Takano, Y., Suga, H., Toyofuku, T., Nomaki, H., Kitazato, H., Nagata, T., & Ohkouchi, N. (2008). Evidence of global chlorophyll d. Science, 321, 658–658.

    CAS  PubMed  Google Scholar 

  • Kaucikas, M., Nürnberg, D., Dorlhiac, G., Rutherford, A. W., & VAN Thor, J. J. (2017). Femtosecond visible transient absorption spectroscopy of chlorophyll f-containing photosystem I. Biophysical Journal, 112, 234–249.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kehoe, D. M., & Gutu, A. (2006). Responding to color: The regulation of complementary chromatic adaptation. Annual Review of Plant Biology, 57, 127–150.

    CAS  PubMed  Google Scholar 

  • Kirilovsky, D., & Kerfeld, C. A. (2012). The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817, 158–166.

    CAS  Google Scholar 

  • Knoppová, J., Sobotka, R., Tichý, M., Yu, J., Konik, P., Halada, P., Nixon, P. J., & Komenda, J. (2014). Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis. The Plant Cell, 26, 1200–1212.

    PubMed  PubMed Central  Google Scholar 

  • Koizumi, H., Itoh, Y., Hosoda, S., Akiyama, M., Hoshino, T., Shiraiwa, Y., & Kobayashi, M. (2005). Serendipitous discovery of Chl d formation from Chl a with papain. Science and Technology of Advanced Materials, 6, 551–557.

    CAS  Google Scholar 

  • Koyama, K., Tsuchiya, T., Akimoto, S., Yokono, M., Miyashita, H., & Mimuro, M. (2006). New linker proteins in phycobilisomes isolated from the cyanobacterium Gloeobacter violaceus PCC 7421. FEBS Letters, 580, 3457–3461.

    CAS  PubMed  Google Scholar 

  • Kräutler, B. (2016). Breakdown of chlorophyll in higher plants--Phyllobilins as abundant, yet hardly visible signs of ripening, senescence, and cell death. Angewandte Chemie (English Edition), 55, 4882–4907.

    Google Scholar 

  • Kühl, M., Chen, M., & Ralph, P. J. (2005). A niche for cyanobacteria containing chlorophyll d. Nature, 433, 820.

    PubMed  Google Scholar 

  • La Roche, J., Van Der Staay, G. W., Partensky, F., Ducret, A., Aebersold, R., Li, R., Golden, S. S., Hiller, R. G., Wrench, P. M., Larkum, A. W., & Green, B. R. (1996). Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proceedings of the National Academy of Sciences, USA, 93, 15244–15248.

    Google Scholar 

  • Larkum, A. W., Scaramuzzi, C., Cox, G. C., Hiller, R. G., & Turner, A. G. (1994). Light-harvesting chlorophyll c-like pigment in Prochloron. Proceedings of the National Academy of Sciences, USA, 91, 679–683.

    CAS  Google Scholar 

  • Larkum, A. W. D., Chen, M., Li, Y., Schliep, M., Trampe, E., West, J., Salih, A., & Kühl, M. (2012). A novel epiphytic chlorophyll d-containing cyanobacterium isolated from a mangrove-associated red alga. Journal of Phycology, 48, 1320–1327.

    PubMed  Google Scholar 

  • Lewin, R. A. (1977). Prochloron, type genus of the Prochlorophyta. Phycologia, 16, 217–217.

    Google Scholar 

  • Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–382.

    Google Scholar 

  • Li, Y., Scales, N., Blankenship, R. E., Willows, R. D., & Chen, M. (2012). Extinction coefficient for red-shifted chlorophylls: Chlorophyll d and chlorophyll f. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1817, 1292–1298.

    Google Scholar 

  • Li, Y., Larkum, A., Schliep, M., Kühl, M., Neilan, B., & Chen, M. (2013). Newly isolated Chl d-containing cyanobacteria. In Photosynthesis research for food, fuel and future – 15th international conference on photosynthesis. Hangzhou/Heidelberg: Zhejiang University Press/Springer.

    Google Scholar 

  • Li, Y., Lin, Y., Garvey, C. J., Birch, D., Corkery, R. W., Loughlin, P. C., Scheer, H., Willows, R. D., & Chen, M. (2016). Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1857, 107–114.

    CAS  Google Scholar 

  • Li, Y., Vella, N., & Chen, M. (2018a). Characterization of isolated photosystem I from Halomicronema hongdechloris, a chlorophyll f-producing cyanobacterium. Photosynthetica, 56, 306–315.

    CAS  Google Scholar 

  • Li, Z.-K., Yin, Y.-C., Zhang, L.-D., Zhang, Z.-C., Dai, G.-Z., Chen, M., & Qiu, B.-S. (2018b). The identification of IsiA proteins binding chlorophyll d in the cyanobacterium Acaryochloris marina. Photosynthesis Research, 135, 165–175.

    CAS  PubMed  Google Scholar 

  • Li, W., Su, H.-N., Pu, Y., Chen, J., Liu, L.-N., Liu, Q., & Qin, S. (2019). Phycobiliproteins: Molecular structure, production, applications, and prospects. Biotechnology Advances, 37, 340–353.

    CAS  PubMed  Google Scholar 

  • Liu, H., Zhang, H., Niedzwiedzki, D. M., Prado, M., He, G., Gross, M. L., & Blankenship, R. E. (2013). Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science, 342, 1104–1107.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Loughlin, P., Lin, Y., & Chen, M. (2013). Chlorophyll d and Acaryochloris marina: Current status. Photosynthesis Research, 116, 277–293.

    CAS  PubMed  Google Scholar 

  • Loughlin, P. C., Willows, R. D., & Chen, M. (2014). In vitro conversion of vinyl to formyl groups in naturally occurring chlorophylls. Scientific Reports, 4, 6069.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Loughlin, P. C., Willows, R. D., & Min, C. (2015). Hydroxylation of the C132 and C18 carbons of chlorophylls by heme and molecular oxygen. Journal of Porphyrins and Phthalocyanines, 19, 1007–1013.

    CAS  Google Scholar 

  • Maccoll, R. (1998). Cyanobacterial phycobilisomes. Journal of Structural Biology, 124, 311–334.

    CAS  PubMed  Google Scholar 

  • Madigan, M. T., & Jung, D. O. (2009). An overview of purple bacteria: Systematics, physiology, and habitats. In C. N. Hunter, F. Daldal, M. C. Thurnauer, & J. T. Beatty (Eds.), The purple phototrophic bacteria. Dordrecht: Springer.

    Google Scholar 

  • Manning, W. M., & Strain, H. H. (1943). Chlorophyll d, a green pigment of red algae. Journal of Biological Chemistry, 151, 1–19.

    CAS  Google Scholar 

  • Mareš, J., Strunecký, O., Bučinská, L., & Wiedermannová, J. (2019). Evolutionary patterns of thylakoid architecture in cyanobacteria. Frontiers in Microbiology, 10, 1–22.

    Google Scholar 

  • Marquardt, J., Senger, H., Miyashita, H., Miyachi, S., & Mörschel, E. (1997). Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Letters, 410, 428–432.

    CAS  PubMed  Google Scholar 

  • Marquardt, J., Mörschel, E., Rhiel, E., & Westermann, M. (2000). Ultrastructure of Acaryochloris marina, an oxyphotobacterium containing mainly chlorophyll d. Archives of Microbiology, 174, 181–188.

    CAS  PubMed  Google Scholar 

  • Masamoto, K., & Furukawa, K.-I. (1997). Accumulation of zeaxanthin in cells of the cyanobacterium, Synechococcus sp. strain PCC 7942 grown under high irradiance. Journal of Plant Physiology, 151, 257–261.

    CAS  Google Scholar 

  • Mcewan, A. G. (1994). Photosynthetic electron transport and anaerobic metabolism in purple non-sulfur phototrophic bacteria. Antonie Van Leeuwenhoek, 66, 151–164.

    CAS  PubMed  Google Scholar 

  • Mcnamara, C. J., Perry, T. D., Bearce, K. A., Hernandez-Duque, G., & Mitchell, R. (2006). Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. Microbial Ecology, 51, 51–64.

    PubMed  Google Scholar 

  • Meguro, M., Ito, H., Takabayashi, A., Tanaka, R., & Tanaka, A. (2011). Identification of the 7-Hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. The Plant Cell, 23, 3442–3453.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mielke, S. P., Kiang, N. Y., Blankenship, R. E., & Mauzerall, D. (2013). Photosystem trap energies and spectrally-dependent energy-storage efficiencies in the Chl d-utilizing cyanobacterium, Acaryochloris marina. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1827, 255–265.

    CAS  Google Scholar 

  • Miller, S. R., Augustine, S., Olson, T. L., Blankenship, R. E., Selker, J., & Wood, A. M. (2005). Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proceedings of the National Academy of Sciences, USA, 102, 850–855.

    CAS  Google Scholar 

  • Mimuro, M., Akimoto, S., Gotoh, T., Yokono, M., Akiyama, M., Tsuchiya, T., Miyashita, H., Kobayashi, M., & Yamazaki, I. (2004). Identification of the primary electron donor in PS II of the Chl d-dominated cyanobacterium Acaryochloris marina. FEBS Letters, 556, 95–98.

    CAS  PubMed  Google Scholar 

  • Miyashita, H., Ikemoto, H., Kurano, N., Adachi, K., Chihara, M., & Miyachi, S. (1996). Chlorophyll d as a major pigment. Nature, 383, 402.

    CAS  Google Scholar 

  • Miyashita, H., Adachi, K., Kurano, N., Ikemot, H., Chihara, M., & Miyach, S. (1997). Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant & Cell Physiology, 38, 274–281.

    CAS  Google Scholar 

  • Miyashita, H., Ohkubo, S., Komatsu, H., Sorimachi, Y., Fukayama, D., Fujinuma, D., Akutsu, S., & Kobayashi, M. (2014). Discovery of chlorophyll d in Acaryochloris marina and chlorophyll f in a unicellular cyanobacterium, strain KC1, isolated from Lake Biwa. Journal of Physical Chemistry & Biophysics, 4, 149.

    Google Scholar 

  • Moss, G. P. (1987). Nomenclature of tetrapyrroles (recommendations 1986). Pure and Applied Chemistry, 59, 779.

    Google Scholar 

  • Murakami, A., Miyashita, H., Iseki, M., Adachi, K., & Mimuro, M. (2004). Chlorophyll d in an epiphytic cyanobacterium of red algae. Science, 303, 1633–1633.

    CAS  PubMed  Google Scholar 

  • Myśliwa-Kurdziel, B., Latowski, D., & Strzałka, K. (2019). Chapter three – Chlorophylls c—Occurrence, synthesis, properties, photosynthetic and evolutionary significance. Advances in Botanical Research, 90, 91–119.

    Google Scholar 

  • Nagy, J. O., Bishop, J. E., Klotz, A. V., Glazer, A. N., & Rapoport, H. (1985). Bilin attachment sites in the alpha, beta, and gamma subunits of R-phycoerythrin. Structural studies on singly and doubly linked phycourobilins. Journal of Biological Chemistry, 260, 4864–4868.

    CAS  PubMed  Google Scholar 

  • Neilson, J. A. D., & Durnford, D. G. (2010). Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynthesis Research, 106, 57–71.

    CAS  PubMed  Google Scholar 

  • Nürnberg, D. J., Morton, J., Santabarbara, S., Telfer, A., Joliot, P., Antonaru, L. A., Ruban, A. V., Cardona, T., Krausz, E., Boussac, A., Fantuzzi, A., & Rutherford, A. W. (2018). Photochemistry beyond the red limit in chlorophyll f–containing photosystems. Science, 360, 1210–1213.

    PubMed  Google Scholar 

  • Oba, T., Uda, Y., Matsuda, K., Fukusumi, T., Ito, S., Hiratani, K., & Tamiaki, H. (2011). A mild conversion from 3-vinyl- to 3-formyl-chlorophyll derivatives. Bioorganic & Medicinal Chemistry Letters, 21, 2489–2491.

    CAS  Google Scholar 

  • Ogata, T., Kodama, M., Nomura, S., Kobayashi, M., Nozawa, T., Katoh, T., & Mimuro, M. (1994). A novel peridinin—Chlorophyll a protein (PCP) from the marine dinoflagellate Alexandrium cohorticula: A high pigment content and plural spectral forms of peridinin and chlorophyll a. FEBS Letters, 356, 367–371.

    CAS  PubMed  Google Scholar 

  • Ong, L. J., & Glazer, A. N. (1987). R-phycocyanin II, a new phycocyanin occurring in marine Synechococcus species. Identification of the terminal energy acceptor bilin in phycocyanins. Journal of Biological Chemistry, 262, 6323–6327.

    CAS  PubMed  Google Scholar 

  • Oster, U., Tanaka, R., Tanaka, A., & Rüdiger, W. (2000). Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant Journal, 21, 305–310.

    CAS  PubMed  Google Scholar 

  • Overmann, J., & Garcia-Pichel, F. (2013). The phototrophic way of life. In E. Rosenberg, E. F. Delong, S. Lory, E. Stackebrandt, & F. Thompson (Eds.), The prokaryotes: Prokaryotic communities and ecophysiology. Berlin/Heidelberg: Springer.

    Google Scholar 

  • Partensky, F., Hoepffner, N., Li, W. K. W., Ulloa, O., & Vaulot, D. (1993). Photoacclimation of Prochlorococcus sp. (Prochlorophyta) strains isolated from the North Atlantic and the Mediterranean Sea. Plant Physiology, 101, 285–296.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Partensky, F., Hess, W. R., & Vaulot, D. (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiology and Molecular Biology Reviews, 63, 106–127.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Partensky, F., Six, C., Ratin, M., Garczarek, L., Vaulot, D., Probert, I., Calteau, A., Gourvil, P., Marie, D., Grébert, T., Bouchier, C., Le Panse, S., Gachenot, M., Rodríguez, F., & Garrido, J. L. (2018). A novel species of the marine cyanobacterium Acaryochloris with a unique pigment content and lifestyle. Scientific Reports, 8, 9142.

    PubMed  PubMed Central  Google Scholar 

  • Petrasek, Z., Schmitt, F.-J., Theiss, C., Huyer, J., Chen, M., Larkum, A., Eichler, H. J., Kemnitz, K., & Eckert, H.-J. (2005). Excitation energy transfer from phycobiliprotein to chlorophyll d in intact cells of Acaryochloris marina studied by time- and wavelength-resolved fluorescence spectroscopy. Photochemical & Photobiological Sciences, 4, 1016–1022.

    CAS  Google Scholar 

  • Pfreundt, U., Stal, L. J., Voß, B., & Hess, W. R. (2012). Dinitrogen fixation in a unicellular chlorophyll d-containing cyanobacterium. The ISME Journal, 6, 1367–1377.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Polívka, T., Pascher, T., & Hiller, R. G. (2008). Energy transfer in the peridinin-chlorophyll protein ccmplex reconstituted with mixed chlorophyll sites. Biophysical Journal, 94, 3198–3207.

    PubMed  PubMed Central  Google Scholar 

  • Porra, R. J., Schäfer, W., Cmiel, E., Katheder, I., & Scheer, H. (1994). The derivation of the formyl-group oxygen of chlorophyll b in higher plants from molecular oxygen. European Journal of Biochemistry, 219, 671–679.

    CAS  PubMed  Google Scholar 

  • Renger, T., & Schlodder, E. (2008). The primary electron donor of photosystem II of the cyanobacterium Acaryochloris marina is a chlorophyll d and the water oxidation is driven by a chlorophyll a/chlorophyll d heterodimer. The Journal of Physical Chemistry. B, 112, 7351–7354.

    CAS  PubMed  Google Scholar 

  • Reyes-Prieto, A., Weber, A. P. M., & Bhattacharya, D. (2007). The origin and establishment of the plastid in algae and plants. Annual Review of Genetics, 41, 147–168.

    CAS  PubMed  Google Scholar 

  • Ritter, S., Hiller, R. G., Wrench, P. M., Welte, W., & Diederichs, K. (1999). Crystal structure of a phycourobilin-containing phycoerythrin at 1.90-Å resolution. Journal of Structural Biology, 126, 86–97.

    CAS  PubMed  Google Scholar 

  • Rockwell, N. C., Martin, S. S., & Lagarias, J. C. (2016). Identification of cyanobacteriochromes detecting far-red light. Biochemistry, 55, 3907–3919.

    CAS  PubMed  Google Scholar 

  • Rodríguez, F., Garrido, J. L., Sobrino, C., Johnsen, G., Riobó, P., Franco, J., Aamot, I., Ramilo, I., Sanz, N., & Kremp, A. (2016). Divinyl chlorophyll a in the marine eukaryotic protist Alexandrium ostenfeldii (Dinophyceae). Environmental Microbiology, 18, 627–643.

    PubMed  Google Scholar 

  • Sawicki, A., Willows, R. D., & Chen, M. (2019). Spectral signatures of five hydroxymethyl chlorophyll a derivatives chemically derived from chlorophyll b or chlorophyll f. Photosynthesis Research, 140, 115–127.

    CAS  PubMed  Google Scholar 

  • Schagerl, M., & Müller, B. (2006). Acclimation of chlorophyll a and carotenoid levels to different irradiances in four freshwater cyanobacteria. Journal of Plant Physiology, 163, 709–716.

    CAS  PubMed  Google Scholar 

  • Scheer, H. (1991). Structure and occurrence of chlorophylls. In H. Scheer (Ed.), Chlorophylls. Boca Raton: CRC Press.

    Google Scholar 

  • Scheer, H. (2006). An overview of chlorophylls and bacteriochlorophylls: Biochemistry, biophysics, functions and applications. In B. Grimm, R. J. Porra, W. Rüdiger, & H. Scheer (Eds.), Chlorophylls and bacteriochlorophylls: Biochemistry, biophysics, functions and applications. Dordrecht: Springer.

    Google Scholar 

  • Scheer, H., & Zhao, K. H. (2008). Biliprotein maturation: The chromophore attachment. Molecular Microbiology, 68, 263–276.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scheumann, V., Ito, H., Tanaka, A., Schoch, S., & Rüdiger, W. (1996). Substrate specificity of chlorophyll(ide) b reductase in etioplasts of barley (Hordeurn Vulgare L.). European Journal of Biochemistry, 242, 163–170.

    CAS  PubMed  Google Scholar 

  • Schirmer, T., Bode, W., Huber, R., Sidler, W., & Zuber, H. (1985). X-ray crystallographic structure of the light-harvesting biliprotein C-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures. Journal of Molecular Biology, 184, 257–277.

    CAS  PubMed  Google Scholar 

  • Schliep, M., Chen, M., Larkum, A., & Quinnell, R. (2007). The function of MgDVP in a chlorophyll d-containing organism. In J. F. Allen, E. Gantt, J. H. Golbeck, & B. Osmond (Eds.), Photosynthesis: Energy from the sun (pp. 262–263). Dordrecht: Springer.

    Google Scholar 

  • Schliep, M., Crossett, B., Willows, R. D., & Chen, M. (2010). 18O labeling of chlorophyll d in Acaryochloris marina reveals that chlorophyll a and molecular oxygen are precursors. Journal of Biological Chemistry, 285, 28450–28456.

    CAS  PubMed  Google Scholar 

  • Schlodder, E., Çetin, M., Eckert, H.-J., Schmitt, F.-J., Barber, J., & Telfer, A. (2007). Both chlorophylls a and d are essential for the photochemistry in photosystem II of the cyanobacteria, Acaryochloris marina. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1767, 589–595.

    CAS  Google Scholar 

  • Schmidt, M., Krasselt, A., & Reuter, W. (2006). Local protein flexibility as a prerequisite for reversible chromophore isomerization in α-phycoerythrocyanin. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics, 1764, 55–62.

    CAS  Google Scholar 

  • Schmitt, F.-J., Campbell, Z. Y., Bui, M. V., Hüls, A., Tomo, T., Chen, M., Maksimov, E. G., Allakhverdiev, S. I., & Friedrich, T. (2018). Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light. Photosynthesis Research, 139, 185–201.

    PubMed  Google Scholar 

  • Shedbalkar, V. P., & Rebeiz, C. A. (1992). Chloroplast biogenesis: Determination of the molar extinction coefficients of divinyl chlorophyll a and b and their pheophytins. Analytical Biochemistry, 207, 261–266.

    Google Scholar 

  • Shen, G., Canniffe, D. P., Ho, M.-Y., Kurashov, V., Van Der Est, A., Golbeck, J. H., & Bryant, D. A. (2019). Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002. Photosynthesis Research, 140, 77–92.

    CAS  PubMed  Google Scholar 

  • Shi, L.-X., Hall, M., Funk, C., & Schröder, W. P. (2012). Photosystem II, a growing complex: Updates on newly discovered components and low molecular mass proteins. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817, 13–25.

    CAS  Google Scholar 

  • Shih, P. M., Wu, D., Latifi, A., Axen, S. D., Fewer, D. P., Talla, E., Calteau, A., Cai, F., Tandeau DE Marsac, N., Rippka, R., Herdman, M., Sivonen, K., Coursin, T., Laurent, T., Goodwin, L., Nolan, M., Davenport, K. W., Han, C. S., Rubin, E. M., Eisen, J. A., Woyke, T., Gugger, M., & Kerfeld, C. A. (2013). Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proceedings of the National Academy of Sciences, USA, 110, 1053–1058.

    CAS  Google Scholar 

  • Shuvalov, V. A., Yakovlev, A. G., Vasileva, L. G., & Ya, S. A. (2006). Primary charge separation between P700∗ and the primary electron acceptor complex A-A0: A comparison with bacterial reaction centers. In J. H. Golbeck (Ed.), Photosystem I: The light-driven plastocyanin: Ferredoxin oxidoreductase. Dordrecht: Springer.

    Google Scholar 

  • Sidler, W. A. (1994). Phycobilisome and phycobiliprotein structures. In D. A. Bryant (Ed.), The molecular biology of cyanobacteria. Advances in photosynthesis. Dordrecht: Springer.

    Google Scholar 

  • Six, C., Thomas, J.-C., Garczarek, L., Ostrowski, M., Dufresne, A., Blot, N., Scanlan, D. J., & Partensky, F. (2007). Diversity and evolution of phycobilisomes in marine Synechococcus spp.: A comparative genomics study. Genome Biology, 8, R259–R259.

    PubMed  PubMed Central  Google Scholar 

  • Sonani, R. R., Roszak, A. W., Ortmann De Percin Northumberland, C., Madamwar, D., & Cogdell, R. J. (2018). An improved crystal structure of C-phycoerythrin from the marine cyanobacterium Phormidium sp. A09DM. Photosynthesis Research, 135, 65–78.

    CAS  PubMed  Google Scholar 

  • Steiger, S., Schäfer, L., & Sandmann, G. (1999). High-light-dependent upregulation of carotenoids and their antioxidative properties in the cyanobacterium Synechocystis PCC 6803. Journal of Photochemistry and Photobiology B: Biology, 52, 14–18.

    CAS  Google Scholar 

  • Stomp, M., Huisman, J., Stal, L. J., & Matthijs, H. C. P. (2007). Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule. The ISME Journal, 1, 271–282.

    CAS  PubMed  Google Scholar 

  • Swingley, W. D., Chen, M., Cheung, P. C., Conrad, A. L., Dejesa, L. C., Hao, J., Honchak, B. M., Karbach, L. E., Kurdoglu, A., Lahiri, S., Mastrian, S. D., Miyashita, H., Page, L., Ramakrishna, P., Satoh, S., Sattley, W. M., Shimada, Y., Taylor, H. L., Tomo, T., Tsuchiya, T., Wang, Z. T., Raymond, J., Mimuro, M., Blankenship, R. E., & Touchman, J. W. (2008). Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proceedings of the National Academy of Sciences, USA, 105, 2005–2010.

    CAS  Google Scholar 

  • Takaichi, S. (2011). Carotenoids in algae: Distributions, biosyntheses and functions. Marine Drugs, 9, 1101–1118.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takaichi, S., & Mochimaru, M. (2007). Carotenoids and carotenogenesis in cyanobacteria: Unique ketocarotenoids and carotenoid glycosides. Cellular and Molecular Life Sciences, 64, 2607–2619.

    CAS  PubMed  Google Scholar 

  • Takaichi, S., Mochimaru, M., Uchida, H., Murakami, A., Hirose, E., Maoka, T., Tsuchiya, T., & Mimuro, M. (2012). Opposite chilarity of α-carotene in unusual cyanobacteria with unique chlorophylls, Acaryochloris and Prochlorococcus. Plant & Cell Physiology, 53, 1881–1888.

    CAS  Google Scholar 

  • Tang, K.-H., Yue, H., & Blankenship, R. E. (2010). Energy metabolism of Heliobacterium modesticaldum during phototrophic and chemotrophic growth. BMC Microbiology, 10, 150.

    PubMed  PubMed Central  Google Scholar 

  • Thweatt, J. L., Ferlez, B. H., Golbeck, J. H., & Bryant, D. A. (2017). BciD is a radical S-Adenosyl-l-methionine (SAM) enzyme that completes bacteriochlorophyllide e biosynthesis by oxidizing a methyl group into a formyl group at C-7. Journal of Biological Chemistry, 292, 1361–1373.

    CAS  PubMed  Google Scholar 

  • Tomi, T., Shibata, Y., Ikeda, Y., Taniguchi, S., Haik, C., Mataga, N., Shimada, K., & Itoh, S. (2007). Energy and electron transfer in the photosynthetic reaction center complex of Acidiphilium rubrum containing Zn-bacteriochlorophyll a studied by femtosecond up-conversion spectroscopy. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1767, 22–30.

    CAS  Google Scholar 

  • 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. Proceedings of the National Academy of Sciences, USA, 104, 7283–7288.

    CAS  Google Scholar 

  • Tomo, T., Shinoda, T., Chen, M., Allakhverdiev, S. I., & Akimoto, S. (2014). Energy transfer processes in chlorophyll f-containing cyanobacteria using time-resolved fluorescence spectroscopy on intact cells. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1837, 1484–1489.

    CAS  Google Scholar 

  • Toporik, H., Li, J., Williams, D., Chiu, P.-L., & Mazor, Y. (2019). The structure of the stress-induced photosystem I–IsiA antenna supercomplex. Nature Structural & Molecular Biology, 26, 443–449.

    CAS  Google Scholar 

  • Tóth, T. N., Chukhutsina, V., Domonkos, I., Knoppová, J., Komenda, J., Kis, M., Lénárt, Z., Garab, G., Kovács, L., Gombos, Z., & Van Amerongen, H. (2015). Carotenoids are essential for the assembly of cyanobacterial photosynthetic complexes. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1847, 1153–1165.

    Google Scholar 

  • Tsuchiya, T., Akimoto, S., Mizoguchi, T., Watabe, K., Kindo, H., Tomo, T., Tamiaki, H., & Mimuro, M. (2012a). Artificially produced [7-formyl]-chlorophyll d functions as an antenna pigment in the photosystem II isolated from the chlorophyllide a oxygenase-expressing Acaryochloris marina. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817, 1285–1291.

    CAS  Google Scholar 

  • Tsuchiya, T., Mizoguchi, T., Akimoto, S., Tomo, T., Tamiaki, H., & Mimuro, M. (2012b). Metabolic engineering of the Chl d-dominated cyanobacterium Acaryochloris marina: Production of a novel Chl species by the introduction of the chlorophyllide a oxygenase gene. Plant & Cell Physiology, 53, 518–527.

    CAS  Google Scholar 

  • Umena, Y., Kawakami, K., Shen, J.-R., & Kamiya, N. (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Å. Nature, 473, 55–60.

    CAS  PubMed  Google Scholar 

  • Van Der Staay, G. W., & Staehelin, L. A. (1994). Biochemical characterization of protein composition and protein phosphorylation patterns in stacked and unstacked thylakoid membranes of the prochlorophyte Prochlorothrix hollandica. Journal of Biological Chemistry, 269, 24834–24844.

    PubMed  Google Scholar 

  • Vavilin, D., & Vermaas, W. (2007). Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta, 1767, 920–929.

    CAS  PubMed  Google Scholar 

  • Wakao, N., Yokoi, N., Isoyama, N., Hiraishi, A., Shimada, K., Kobayashi, M., Kise, H., Iwaki, M., Itoh, S., & Takaichi, S. (1996). Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum. Plant & Cell Physiology, 37, 889–893.

    CAS  Google Scholar 

  • Watanabe, M., Semchonok, D. A., Webber-Birungi, M. T., Ehira, S., Kondo, K., Narikawa, R., Ohmori, M., Boekema, E. J., & Ikeuchi, M. (2014). Attachment of phycobilisomes in an antenna–photosystem I supercomplex of cyanobacteria. Proceedings of the National Academy of Sciences, USA, 111, 2512–2517.

    CAS  Google Scholar 

  • Wiltbank, L. B., & Kehoe, D. M. (2019). Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. Nature Reviews. Microbiology, 17, 37–50.

    CAS  PubMed  Google Scholar 

  • Wolf, B. M., & Blankenship, R. E. (2019). Far-red light acclimation in diverse oxygenic photosynthetic organisms. Photosynthesis Research, 142(3), 349–359. https://doi.org/10.1007/s11120-019-00653-6.

    Article  CAS  PubMed  Google Scholar 

  • Yu, L., Huang, Y., Bai, Z., Zhu, B., Ding, K., Chen, T., Ding, Y., & Wang, Y. (2015). The aerobic oxidation and C=C bond cleavage of styrenes catalyzed by Cerium(IV) ammonium nitrate (CAN). Journal of the Chinese Chemical Society, 62, 479–482.

    CAS  Google Scholar 

  • Yurkov, V. V., & Beatty, J. T. (1998). Aerobic anoxygenic phototrophic bacteria. Microbiology and Molecular Biology Reviews, 62, 695–724.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zakar, T., Laczko-Dobos, H., Toth, T. N., & Gombos, Z. (2016). Carotenoids assist in cyanobacterial photosystem II assembly and function. Frontiers in Plant Science, 7, 295–295.

    PubMed  PubMed Central  Google Scholar 

  • Zamzam, N., Kaucikas, M., Nürnberg, D. J., Rutherford, A. W., & Van Thor, J. J. (2019). Femtosecond infrared spectroscopy of chlorophyll f-containing photosystem I. Physical Chemistry Chemical Physics, 21, 1224–1234.

    CAS  PubMed  Google Scholar 

  • Zapata, M., Garrido, J. L., & Jeffrey, S. W. (2006). Chlorophyll c pigments: Current status. In B. Grimm, R. J. Porra, W. Rüdiger, & H. Scheer (Eds.), Chlorophylls and bacteriochlorophylls: Biochemistry, biophysics, functions and applications. Dordrecht: Springer Netherlands.

    Google Scholar 

  • Zapata, M., Rodríguez, F., & Garrido, J. L. (2000). Separation of chlorophylls and carotenoids from marine phytoplankton: A new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Marine Ecology Progress Series, 195, 29–45.

    Google Scholar 

  • Zhang, J., Ma, J., Liu, D., Qin, S., Sun, S., Zhao, J., & Sui, S.-F. (2017). Structure of phycobilisome from the red alga Griffithsia pacifica. Nature, 551, 57–63.

    PubMed  Google Scholar 

  • Zhang, Z.-C., Li, Z.-K., Yin, Y.-C., Li, Y., Jia, Y., Chen, M., & Qiu, B.-S. (2019). Widespread occurrence and unexpected diversity of red-shifted chlorophyll producing cyanobacteria in humid subtropical forest ecosystems. Environmental Microbiology, 21, 1497–1510.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

AS and MC gratefully acknowledge the financial support of the Australian Research Council Centre of Excellence for Translational Photosynthesis (CE140100015).

Author information

Authors and Affiliations

  1. School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia

    Artur Sawicki & Min Chen

Authors
  1. Artur Sawicki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Min Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Min Chen .

Editor information

Editors and Affiliations

  1. Key laboratory of Plant Stress Biology, State Key Laboratory of Cotton Biology, School of Life Sciences, Henan University, Kaifeng, Henan, China

    Qiang Wang

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sawicki, A., Chen, M. (2020). Molecular Mechanism of Photosynthesis Driven by Red-Shifted Chlorophylls. In: Wang, Q. (eds) Microbial Photosynthesis. Springer, Singapore. https://doi.org/10.1007/978-981-15-3110-1_1

Download citation

Publish with us

Policies and ethics

Search

Navigation