, Volume 813, Issue 1, pp 1–17 | Cite as

Far-red light photoadaptations in aquatic cyanobacteria

  • Svetlana Averina
  • Natalia Velichko
  • Ekaterina Senatskaya
  • Alexander Pinevich
Review Paper


Aquatic ecosystems depend on photosynthetic bacteria that use various strategies of adaptation to light quantity and quality; the qualitative strategies include far-red/near infrared (> 700 nm) light adaptations. The usage of > 700 nm light as energy source is disadvantageous for photosynthesis (long-wavelength quanta are poorer in energy than short-wavelength quanta, and such light is largely screened out by water). Nevertheless, some bacteria produce long-wavelength absorbing “red-shifted” chlorophylls (Chls) that extend the range of photosynthetically active radiation to the infrared region. The majority of cyanobacteria use 400–700 nm light, with excited state being ultimately entrapped by Chl a at a long-wavelength maximal absorbance of ~ 700 nm. This photoadaptation to far-red light was unknown until the discovery of strains producing Chls d and f in 1996 and 2010, respectively. Today, there is much data on cyanobacteria utilizing Chl d as their main pigment and many studies on accessory Chls d and/or f produced under exposure to far-red light. Further analysis of the photosynthetic apparatuses of cyanobacteria that produce red-shifted Chls will contribute to a better understanding of primary productivity in aquatic communities. In this review, we report on the diversity, distribution, physiological ecology, taxonomy and evolution of aquatic cyanobacteria producing red-shifted Chls.


Acaryochloris Halomicronema hongdechloris Chlorophyll d Chlorophyll f FaRLiP 





Chlorophyll-binding protein




Far-red light photoacclimation


Light-harvesting complex


Photosynthetically active radiation








Polymerase chain reaction







Q band (absorbance “red” maximum)

The Qy vector of energy transition in long-wavelength area


Reaction centre



The work was supported by St. Petersburg State University Grant № 1.40.540.2017. We thank St. Petersburg State University research centres “Molecular and Cell Technologies” and “Culture Collection of Microorganisms” for technical assistance. We especially thank the anonymous reviewers for their criticism and for offering many valuable suggestions that have strongly improved the manuscript.


  1. Airs, R. L., B. Temperton, C. Sambles, G. Farnham, S. C. Skill & C. A. Llewellyn, 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.CrossRefPubMedGoogle Scholar
  2. Akimoto, S., T. Shinoda, M. Chen, S. I. Allakhverdiev & T. Tomo, 2015. Energy transfer in the chlorophyll f-containing cyanobacterium, Halomicronema hongdechloris, analyzed by time-resolved fluorescence spectroscopies. Photosynthesis Research 125: 115–122.CrossRefPubMedGoogle Scholar
  3. Akiyama, M., H. Miyashita, H. Kise, T. Watanabe, M. Mimuro, S. Miyachi & M. Kobayashi, 2002. Quest for minor but key chlorophyll molecules in photosynthetic reaction centers—unusual pigment composition in the reaction centers of the chlorophyll d dominated cyanobacterium Acaryochloris marina. Photosynthesis Research 74: 97–107.CrossRefPubMedGoogle Scholar
  4. Akutsu, S., D. Fujinuma, H. Furukawa, T. Watanabe, M. Ohnishi-Kameyama, H. Ono, S. Ohkubo, H. Miyashita & M. Kobayashi, 2011. Pigment analysis of a chlorophyll f-containing cyanobacterium strain KC1 isolated from Lake Biwa. Photomedicine and Photobiology 33: 35–40.Google Scholar
  5. Al-Bader, D., M. Eliyas, R. Rayan & S. Radwan, 2013. Subsurface associations of Acaryochloris-related picocyanobacteria with oil-utilizing bacteria in the Arabian Gulf water body: promising consortia in oil sediment bioremediation. Microbial Ecology 65: 555–565.CrossRefPubMedGoogle Scholar
  6. Allakhverdiev, S. I., V. D. Kreslavski, S. K. Zharmukhamedov, R. A. Voloshin, D. V. Korol’kova & J. R. Shen, 2016. Chlorophylls d and f and their role in primary photosynthetic processes of cyanobacteria. Biochemistry (Moscow) 81: 201–212.CrossRefGoogle Scholar
  7. Allen, J. F., 1992. Protein phosphorylation in regulation of photosynthesis. Biochimica et Biophysica Acta 1098: 275–335.CrossRefPubMedGoogle Scholar
  8. Bauer, C. E., D. W. Bollivar & J. Y. Suzuki, 1993. Genetic analyses of photopigment biosynthesis in eubacteria: a guiding light for algae and plants. Journal of Bacteriology 175: 3919–3925.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Behrendt, L., A. W. D. Larkum, A. Norman, K. Qvortrup, M. Chen, P. Ralph, S. J. Sørensen, E. Trampe & M. Kühl, 2011. Endolithic chlorophyll d-containing phototrophs. The ISME Journal 5: 1072–1076.CrossRefPubMedGoogle Scholar
  10. Behrendt, L., M. Staal, S. M. Cristescu, F. J. M. Harren, M. Schliep, A. W. D. Larkum & M. Kuhl, 2013. Reactive oxygen production induced by near-infrared radiation in three strains of the Chl d-containing cyanobacterium Acaryochloris marina. F1000Research 2. Scholar
  11. Behrendt, L., J. L. Nielsen, S. J. Sørensen, A. W. D. Larkum, J. R. Winther & M. Kühl, 2014. Rapid TaqMan-based quantification of chlorophyll d-containing cyanobacteria in the genus Acaryochloris. Applied and Environmental Microbiology 80: 3244–3249.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Behrendt, L., A. Brejnrod, M. Schliep, S. J. Sørensen, A. W. D. Larkum & M. Kühl, 2015. Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium. The ISME Journal 9: 2108–2111.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Burger-Wiersma, T., L. Stal & L. R. Mur, 1989. Prochlorothrix hollandica gen. nov., sp. nov., a filamentous oxygenic photoautotrophic prokaryote containing chlorophylls a and b: assignment to Prochlorotrichaceae fam. nov. and order Prochlorotrichales Florenzano, Balloni, and Materassi 1986, with emendation of the ordinal description. International Journal of Systematic Bacteriology 39: 250–257.CrossRefGoogle Scholar
  14. Cardona, T., J. W. Murray & A. W. Rutherford, 2015. Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Molecular Biology and Evolution 32: 1310–1328.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Castenholz, R. W., 2015. General characteristics of the cyanobacteria. In DeVos, P., et al. (eds.), Bergey’s Manual of Systematics of Archaea and Bacteria. Wiley, Hobolken, NJ. Scholar
  16. Chen, M. & R. E. Blankenship, 2011. Expanding the solar spectrum used by photosynthesis. Trends in Plant Science 16: 427–431.CrossRefPubMedGoogle Scholar
  17. Chen, M., T. S. Bibby, J. Nield, A. W. D. Larkum & J. Barber, 2005a. Iron deficiency induces a chlorophyll d-binding Pcb antenna system around photosystem I in Acaryochloris marina. Biochimica et Biophysica Acta 1708: 367–374.CrossRefPubMedGoogle Scholar
  18. Chen, M., T. S. Bibby, J. Nield, A. W. D. Larkum & J. Barber, 2005b. Structure of a large photosystem II supercomplex from Acaryochloris marina. FEBS Letters 579: 1306–1310.CrossRefPubMedGoogle Scholar
  19. Chen, M., R. G. Hiller, C. J. Howe & A. W. D. Larkum, 2005c. Unique origin and lateral transfer of prokaryotic chlorophyll-b and chlorophyll-d light-harvesting systems. Molecular Biology and Evolution 22: 21–28.CrossRefPubMedGoogle Scholar
  20. Chen, M., A. Telfer, S. Lin, A. Pascal, A. W. D. Larkum, J. Barber & R. E. Blankenship, 2005d. The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. Photochemical and Photobiological Sciences 4: 1060–1064.CrossRefPubMedGoogle Scholar
  21. Chen, M., Y. Zhang & R. E. Blankenship, 2008. Nomenclature for membrane bound light harvesting complexes of cyanobacteria. Photosynthesis Research 95: 147–154.CrossRefPubMedGoogle Scholar
  22. Chen, M., M. Floetenmeyer & T. Bibby, 2009. Supramolecular organization of phycobiliproteins in the chlorophyll d-containing cyanobacterium Acaryochloris marina. FEBS Letters 583: 2535–2539.CrossRefPubMedGoogle Scholar
  23. Chen, M., M. Schliep, R. D. Willows, Z. L. Cai, B. A. Neilan & H. Scheer, 2010. A red-shifted chlorophyll. Science 329: 1318–1319.CrossRefPubMedGoogle Scholar
  24. Chen, M., Y. Li, D. Birch & R. D. Willows, 2012. A cyanobacterium that contains chlorophyll f—a red-absorbing photopigment. FEBS Letters 586: 3249–3254.CrossRefPubMedGoogle Scholar
  25. Chisholm, S. W., S. L. Frankel, R. Goericke, R. J. Olson, B. Palenik, J. B. Waterbury, L. West-Johnsrud & E. R. Zettler, 1992. Prochlorococcus marinus nov. gen., nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Archives of Microbiology 157: 297–300.CrossRefGoogle Scholar
  26. Deisenhofer, J., H. Michel & R. Huber, 1985. The structural basis of photosynthetic light reactions in bacteria. Trends in Biochemical Sciences 10: 243–248.CrossRefGoogle Scholar
  27. de los Rios, A., M. Grube, L. G. Sancho & C. Ascaso, 2007. Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiology Ecology 59: 386–395.CrossRefPubMedGoogle Scholar
  28. Drews, G. & R. A. Niederman, 2002. Membrane biogenesis in anoxygenic photosynthetic prokaryotes. Photosynthesis Research 73: 87–94.CrossRefPubMedGoogle Scholar
  29. Fleming, E. D. & L. Prufert-Bebout, 2010. Characterization of cyanobacterial communities form high-elevation lakes in the Bolivian Andes. Journal of Geophysical Research. Scholar
  30. French, C. S., 1960. The chlorophyll in vivo and in vitro. In Ruhland, W. (ed.), Encyclopedia of Plant Physiology. Springer, Berlin: 252–297.Google Scholar
  31. Gan, F. & D. A. Bryant, 2015. Adaptive and acclimative responses of cyanobacteria to far-red light. Environmental Microbiology 17: 3450–3465.CrossRefPubMedGoogle Scholar
  32. Gan, F., S. Zhang, N. C. Rockwell, S. S. Martin, J. C. Lagarias & D. A. Bryant, 2014. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345: 1312–1317.CrossRefPubMedGoogle Scholar
  33. Gan, F., G. Shen & D. Bryant, 2015. Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life (Basel) 5: 4–24.Google Scholar
  34. Gindt, Y. M., J. Zhou, D. A. Bryant & K. Sauer, 1994. Spectroscopic studies of phycobilisome subcore preparations lacking key core chromophores: assignment of excited state energies to the Lcm, β18 and αAP-B chromophores. Biochimica et Biophysica Acta 1186: 153–162.CrossRefPubMedGoogle Scholar
  35. Glazer, A. N. & D. A. Bryant, 1975. Allophycocyanin B (λmax 671, 618 nm)—a new cyanobacterial phycobiliprotein. Archiv für Mikrobiologie 104: 15–22.CrossRefGoogle Scholar
  36. Grossman, A. R., M. R. Schaefer, G. G. Chiang & J. L. Collier, 1993. The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiological Reviews 57: 725–749.PubMedPubMedCentralGoogle Scholar
  37. Ho, M.-Y., F. Gan, G. Shen & D. A. Bryant, 2016a. 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.CrossRefPubMedGoogle Scholar
  38. Ho, M.-Y., F. Gan, G. Shen, C. Zhao & D. A. Bryant, 2016b. Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335: I. Regulation of FaRLiP gene expression. Photosynthesis Research 131: 173–186.CrossRefPubMedGoogle Scholar
  39. Ho, M.-Y., G. Shen, D. P. Canniffe, C. Zhao & D. A. Bryant, 2016c. Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science. Scholar
  40. Holt, A. S., 1961. Further evidence of the relation between 2-desvinyl-2-formyl-chlorophyll a and d. Canadian Journal of Botany 39: 327–331.CrossRefGoogle Scholar
  41. Hu, Q., J. Marquardt, I. Iwasaki, H. Miyashita, N. Kurano, E. Mörschel & S. Miyachi, 1999. Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. Biochimica et Biophysica Acta 1412: 250–261.CrossRefPubMedGoogle Scholar
  42. Hu, Q., H. Miyashita, I. Iwasaki, N. Kurano, S. Miyachi, M. Iwaki & S. Itoh, 1998. A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proceedings of National Academy of Sciences of USA 95: 13319–13323.CrossRefGoogle Scholar
  43. Itoh, S., H. Mino, K. Itoh, T. Shigenaga, T. Uzumaki & M. Iwaki, 2007. Function of chlorophyll d in reaction centers of photosystems I and II of the oxygenic photosynthesis of Acaryochloris marina. Biochemistry 46: 12473–12481.CrossRefPubMedGoogle Scholar
  44. Itoh, S., T. Ohno, T. Noji, H. Yamakawa, H. Komatsu, K. Wada, M. Kobayashi & H. Miyashita, 2015. Harvesting far-red light by chlorophyll f in photosystems I and II of unicellular cyanobacterium strain KC1. Plant and Cell Physiology 56: 2024–2034.CrossRefPubMedGoogle Scholar
  45. Kashiyama, Y., H. Miyashita, S. Ohkubo, N. O. Ogawa, Y. Chikaraishi, Y. Takano, H. Suga, T. Toyofuku, H. Nomaki, H. Kitazato, T. Nagata & N. Ohkouchi, 2008. Evidence for global chlorophyll d. Science. Scholar
  46. Kirk, J. T. O., 1994. Light and Photosynthesis in Aquatic Ecosystems, 2nd ed. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  47. Koehne, B., G. Elli, R. C. Jennings, C. Wilhelm & H.-W. Trissl, 1999. Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochimica et Biophysica Acta 1412: 94–107.CrossRefPubMedGoogle Scholar
  48. Kotabová, E., J. Jarešová, R. Kaňa, R. Sobotka, D. Bína & O. Prášil, 2014. Novel type of red-shifted chlorophyll a antenna complex in Chromera velia. I. Physiological relevance and functional connection to photosynthesis. Biochimica et Biophysica Acta 1837: 734–743.CrossRefPubMedGoogle Scholar
  49. Kühl, M., M. Chen, P. J. Ralph, U. Schreiber & A. W. D. Larkum, 2005. A niche for cyanobacteria containing chlorophyll d. Nature. Scholar
  50. Larkum, A. W. D., M. Chen, Y. Li, M. Schliep, E. Trampe, J. West, A. Salih & M. Kühl, 2012. A novel epiphytic chlorophyll d-containing cyanobacterium isolated from mangrove-associated red alga. Journal of Phycology 48: 1320–1327.CrossRefPubMedGoogle Scholar
  51. La Roche, J., G. W. M. van der Staay, F. Partensky, A. Ducret, R. Aebersold, R. Li, S. S. Golden, R. G. Hiller, P. M. Wrench, A. W. D. Larkum & B. R. Green, 1996. Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proceedings of National Academy of Sciences of USA 93: 15244–15248.CrossRefGoogle Scholar
  52. Lewin, R. A., 1976. Prochlorophyta as a proposed new division of algae. Nature 261: 697–698.CrossRefPubMedGoogle Scholar
  53. Li, Y. & M. Chen, 2015. Novel chlorophylls and new directions in photosynthesis research. Functional Plant Biology 42: 493–501.CrossRefGoogle Scholar
  54. Li, Y., A. Larkum, M. Schliep, M. Kühl, B. Neilan & M. Chen, 2013. Newly isolated Chl d-containing cyanobacteria. In Photosynthesis Research for Food, Fuel and the Future: Proceedings of 15th International Conference on Photosynthesis, Kuang, T., C. Lu & L. Zhang (Eds.), Springer Science + Business Media B.V., pp. 686–690.Google Scholar
  55. Li, Y., Y. Lin, C. J. Garvey, D. Birch, R. W. Corkery, P. C. Loughlin, H. Scheer, R. D. Willows & M. Chen, 2016. Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochimica et Biophysica Acta 1857: 107–114.CrossRefPubMedGoogle Scholar
  56. Lin, Y., B. Crossett & M. Chen, 2013. Effects of anaerobic conditions on photosynthetic units of Acaryochloris marina. In Photosynthesis Research for Food, Fuel and the Future: 15th International Conference on Photosynthesis, Kuang, T., C. Lu & L. Zhang (Eds.), Springer Science + Business Media B.V., pp. 121–124.Google Scholar
  57. López-Legentil, S., B. Song, M. Bosch, J. R. Pawlik & X. Turon, 2011. Cyanobacterial diversity and a new Acaryochloris-like symbiont from Bahamian sea-squirts. PLoS ONE. Scholar
  58. Loughlin, P., Y. Lin & M. Chen, 2013. Chlorophyll d and Acaryochloris marina: current status. Photosyntesis Research 116: 277–293.CrossRefGoogle Scholar
  59. MacColl, R., 1998. Cyanobacterial phycobilisomes. Journal of Structural Biology 124: 311–334.CrossRefPubMedGoogle Scholar
  60. Manning, W. M. & H. H. Strain, 1943. Chlorophyll d, a green pigment of red algae. Journal of Biological Chemistry 151: 1–19.Google Scholar
  61. Martinez-Garcia, M., M. Koblizek, S. Lopez-Legentil & J. Anton, 2011. Epibiosis of oxygenic phototrophs containing chlorophylls a, b, c and d on the colonial ascidian Cystodytes dellechiajei. Microbial Ecology 61: 13–19.CrossRefPubMedGoogle Scholar
  62. McNamara, C. J., T. D. Perry, K. A. Bearce, G. Hernandez-Duque & R. Mitchell, 2006. Epilithic and endolithic bacterial communities in limestone from a Mayan archaeological site. Microbial Ecology 51: 51–64.CrossRefPubMedGoogle Scholar
  63. Miller, S. R., S. Augustine, T. L. Olson, R. E. Blankenship, J. Selker & A. M. Wood, 2005. Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proceedings of National Academy of Sciences of USA 102: 850–855.CrossRefGoogle Scholar
  64. Miller, S. R., A. M. Wood, R. E. Blankenship, M. Kim & S. Ferriera, 2011. Dynamics of gene duplication in the genomes of chlorophyll d-producing cyanobacteria: implications for the ecological niche. Genome Biology and Evolution 3: 601–613.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Mimuro, M., S. Akimoto, I. Yamazaki, H. Miyashita & S. Miyachi, 1999. Fluorescence properties of chlorophyll d-dominating prokaryotic alga, Acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells. Biochimica et Biophysica Acta 1412: 37–46.CrossRefPubMedGoogle Scholar
  66. Mimuro, M., K. Hirayama, K. Uezono, H. Miyashita & S. Miyachi, 2000. Uphill energy transfer in a chlorophyll d-dominating oxygenic photosynthetic prokaryote, Acaryochloris marina. Biochimica et Biophysica Acta 1456: 27–34.CrossRefPubMedGoogle Scholar
  67. Mimuro, M., S. Akimoto, T. Gotoh, M. Yokono, M. Akiyama, T. Tsuchiya, H. Miyashita, M. Kobayashi & I. Yamazaki, 2004. Identification of the primary electron donor in PS II of the Chl d-dominated cyanobacterium Acaryochloris marina. FEBS Letters 556: 95–98.CrossRefPubMedGoogle Scholar
  68. Miyashita, H., H. Ikemoto, N. Kurano, K. Adachi, M. Chihara & S. Miyachi, 1996. Chlorophyll d as a major pigment. Nature. Scholar
  69. Miyashita, H., K. Adachi, N. Kurano, H. Ikemoto, M. Chihara & S. Miyachi, 1997. Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant and Cell Physiology 38: 274–281.CrossRefGoogle Scholar
  70. Miyashita, H., H. Ikemoto, N. Kurano, S. Miyachi & M. Chihara, 2003. Acaryochloris marina gen. et sp. nov. (Cyanobacteria), an oxygenic photosynthetic prokaryote containing chl d as a major pigment. Journal of Phycology 39: 1247–1253.CrossRefGoogle Scholar
  71. Miyashita, H., S. Ohkubo, H. Komatsu, Y. Sorimachi, D. Fukayama, D. Fujinuma, S. Akitsu & M. Kobayashi, 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 and Biophysics. Scholar
  72. Mohr, R., B. Voß, M. Schliep, T. Kurz, I. Maldener, D. G. Adams, A. W. D. Larkum, M. Chen & W. R. Hess, 2010. A new chlorophyll d-containing cyanobacterium: evidence for niche adaptation in the genus Acaryochloris. The ISME Journal 4: 1456–1469.CrossRefPubMedGoogle Scholar
  73. Murakami, A., H. Miyashita, M. Iseki, K. Adachi & M. Mimuro, 2004. Chlorophyll d in an epiphytic cyanobacterium of red algae. Science. Scholar
  74. Murray, J. W., 2012. Sequence variation at the oxygen evolving centre of photosystem II: a new class of ‘rogue’ cyanobacterial D1 proteins. Photosynthesis Research 110: 177–184.CrossRefPubMedGoogle Scholar
  75. Nowack, S., M. T. Olsen, G. A. Schaible, E. D. Becraft, G. Shen, I. Klapper, D. A. Bryant & D. M. Ward, 2015. The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes inhabiting different depths in the Mushroom Spring microbial mat exhibit different adaptive and acclimative responses to light. Frontiers in Microbiology. Scholar
  76. Ohkubo, S. & H. Miyashita, 2012. Selective detection and phylogenetic diversity of Acaryochloris spp. that exist in association with didemnid ascidians and sponge. Microbes and Environments 27: 217–225.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Ohkubo, S., H. Miyashita, A. Murakami, H. Takeyama, T. Tsuchiya & M. Mimuro, 2006. Molecular detection of epiphytic Acaryochloris spp. on marine macroalgae. Applied and Environmental Microbiology 72: 7912–7915.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Olsen, M. T., S. Nowack, J. M. Wood, E. D. Becraft, K. LaButti, A. Lipzen, J. Martin, W. S. Schackwitz, D. B. Rusch, F. M. Cohan, D. A. Bryant & D. M. Ward, 2015. The molecular dimension of microbial species: 3.Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat. Frontiers. Scholar
  79. Pinevich, A. V., K. A. Mamkaeva, N. N. Titova, O. V. Gavrilova, E. V. Ermilova, K. V. Kvitko, A. V. Pljusch, L. N. Voloshko & S. G. Averina, 2004. St. Petersburg Culture Collection (CALU): four decades of storage and research with microscopic algae, cyanobacteria and other microorganisms. Nova Hedwigia 79: 115–126.CrossRefGoogle Scholar
  80. Pinevich, A. V., S. G. Averina & N. V. Velichko, 2010. Essays in the Biology of Prochlorophytes. St.Petersburg University Publishing House, St. Petersburg(in Russian).Google Scholar
  81. Razeghifard, M. R., M. Chen, J. L. Hughes, J. Freeman, E. Krausz & T. Wydrzynski, 2005. Spectroscopic studies of photosystem II in chlorophyll d-containing Acaryochloris marina. Biochemistry 44: 11178–11187.CrossRefPubMedGoogle Scholar
  82. Renger, T. & E. Schlodder, 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. Journal of Physical Chemistry B 112: 7351–7354.CrossRefGoogle Scholar
  83. Schliep, M., B. Crossett, R. D. Willows & M. Chen, 2010. 18O labeling of chlorophyll d in Acaryochloris marina reveals that chlorophyll a and molecular oxygen are precursors. The Journal of Biological Chemistry 285: 28450–28456.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Swingley, W. D., M. F. Hohmann-Marriott, T. L. Olson & R. E. Blankenship, 2005. Effect of iron on growth and ultrastructure of Acaryochloris marina. Applied and Environmental Microbiology 71: 8606–8610.CrossRefPubMedPubMedCentralGoogle Scholar
  85. Swingley, W. D., M. Chen, P. C. Cheung, A. L. Conrad, L. C. Dejesa, J. Hao, B. M. Honchak, L. E. Karbach, A. Kurdoglu, S. Lahiri, S. D. Mastrian, H. Miyashita, L. Page, P. Ramakrishna, S. Satoh, W. M. Sattley, Y. Shimada, H. L. Taylor, T. Tomo, T. Tsuchiya, Z. T. Wang, J. Raymond, M. Mimuro, R. E. Blankenship & J. W. Touchman, 2008. Niche adaptation and genome expansion in the chlorophyll d producing cyanobacterium Acaryochloris marina. Proceedings of National Academy of Sciences of USA 105: 2005–2010.CrossRefGoogle Scholar
  86. Tomo, T., T. Okubo, S. Akimoto, M. Yokono, H. Miyashita, T. Tsuchiya, T. Noguchi & M. Mimuro, 2007. Identification of the special pair of photosystem II in a chlorophyll d dominated cyanobacterium. Proceedings of National Academy of Sciences of USA 104: 7283–7288.CrossRefGoogle Scholar
  87. Tomo, T., Y. Kato, T. Suzuki, S. Akimoto, T. Okubo, T. Noguchi, K. Hasegawa, T. Tsuchiya, K. Tanaka, M. Fukuya, N. Dohmae, T. Watanabe & M. Mimuro, 2008. Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. Journal of Biological Chemistry 283: 18198–18209.CrossRefPubMedGoogle Scholar
  88. Tomo, T., T. Shinoda, M. Chen, S. I. Allakhverdiev & S. Akimoto, 2014. Energy transfer processes in chlorophyll f- containing cyanobacteria using time-resolved fluorescence spectroscopy on intact cells. Biochimica et Biophysica Acta 1837: 1484–1489.CrossRefPubMedGoogle Scholar
  89. Trampe, E. & M. Kühl, 2016. Chlorophyll f distribution and dynamics in cyanobacterial beachrock biofilms. Journal of Phycology 52: 990–996.CrossRefPubMedGoogle Scholar
  90. Wolf, B. M., D. M. Niedzwiedzki, N. C. M. Magdaong, R. Roth, U. Goodenough & R. E. Blankenship, 2017. Characterization of a newly isolated freshwater Eustigmatophyte alga capable of utilizing far-red light as its sole light source. Photosynthesis Research. Scholar
  91. Wood, A. M., 2012. Acaryochloris—explaining the riddle of chlorophyll d in red algae and expanding PAR for oxygenic photosynthesis. Journal of Phycology 48: 1317–1319.CrossRefGoogle Scholar
  92. Yoneda, A., B. J. Wittmann, J. D. King, R. E. Blankenship & G. Dantas, 2016. Transcriptomic analysis illuminates genes involved in chlorophyll synthesis after nitrogen starvation in Acaryochloris sp. CCMEE 5410. Photosynthesis Research 129: 171–182.CrossRefPubMedGoogle Scholar
  93. Zeng, Y., F. Feng, H. Medová, J. Dean & M. Kobližek, 2014. Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proceedings of National Academy of Sciences of USA 111: 7780–7795.Google Scholar
  94. Zhao, C., F. Gan, G. Shen & D. A. Bryant, 2015. RfpA, RfpB, and RfpC are the master control elements of far-red light photoacclimation (FaRLiP). Frontiers in Microbiology. Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Microbiology, Faculty of BiologySt. Petersburg State UniversitySt. PetersburgRussia

Personalised recommendations