Микробиология, 2022, T. 91, № 6, стр. 666-684

На краю радуги: длинноволновые хлорофиллы и фотосинтетическая адаптация цианобактерий к дальнему красному свету

А. В. Пиневич a*, С. Г. Аверина a

a Санкт-Петербургский государственный университет
199034 Санкт-Петербург, Россия

* E-mail: Pinevich.A@mail.ru

Поступила в редакцию 25.05.2022
После доработки 11.07.2022
Принята к публикации 12.07.2022

Аннотация

Феномен фотосинтетической адаптации цианобактерий к дальнему красному свету (ДКС; 700‒750 нм) тесно связан с такими фундаментальными вопросами, как фототрофия, микробная экология и разнообразие бактерий. В практическом плане данная биоэнергетическая стратегия важна для биотехнологии фотосинтеза, с перспективой получить доступ к дополнительному ресурсу световой энергии. Как известно, большинство цианобактерий использует свет длиной волны 400‒700 нм; возбужденное состояние поступает от светособирающего комплекса к хлорофиллу a (Хл a) реакционных центров двух фотосистем с красными максимумами поглощения ∼700 нм. После выделения первых штаммов с хлорофиллами d и f выяснилось, что цианобактерии могут использовать и ДКС. В настоящее время получен значительный объем данных о цианобактериях, конститутивно образующих Хл d, а также о тех, которые синтезируют Хл f или Хл f/Хл d при фотоакклиматизации к ДКС (англ. far-red light photoacclimation; FaRLiP). Включение этих пигментов в состав фотосинтетического аппарата, в частности с использованием механизма FaRLiP, повышает адаптационный потенциал и расширяет границы распространения цианобактерий. В обзоре приводятся сведения о фотосинтетическом аппарате с Хл d или Хл d/Хл f, о генном кластере FaRLiP, о разнообразии и филогении цианобактерий с конститутивным или индуцированным синтезом длинноволновых хлорофиллов, об использовании хлорофиллов в качестве хемотаксономического признака и отражении этого признака в номенклатуре цианобактерий.

Ключевые слова: дальний красный свет, кластер FaRLiP, реакционный центр, светособирающий комплекс, фикобилисома, фотоадаптация, фотосинтетический аппарат, хлорофилл d, хлорофилл f, цианобактерии

Список литературы

  1. Пиневич А.В., Аверина С.Г., Величко Н.В. Очерки биологии прохлорофитов. С.-Петербург: Изд-во С.-Петерб. ун-та, 2010. 198 с.

  2. Airs R.L., Temperton B., Sambles C., Farnham G., Skill S.C., Llewellyn C.A. Chlorophyll f and chlorophyll d are produced in the cyanobacterium Chlorogloeopsis fritschii when cultured under natural light and near-infrared radiation // FEBS Lett. 2014. V. 588. P. 3770‒3777.

  3. Akimoto S., Shinoda T., Chen M., Allakhverdiev S.I., Tomo T. Energy transfer in the chlorophyll f-containing cyanobacterium, Halomicronema hongdechloris, analyzed by time-resolved fluorescence spectroscopies // Photosynth. Res. 2015. V. 125. P. 115–122.

  4. Akiyama M., Miyashita H., Kise H., Watanabe T., Mimuro M., Miyachi S., Kobayashi, M. 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 // Photosynth. Res. 2002. V. 74. P. 97–107.

  5. Akutsu S., Fujinuma D., Furukawa H., Watanabe T., Ohnishi-Kameyama M., Ono S., Ohkubo S., Miyashita H., Kobayashi M. Pigment analysis of a chlorophyll f-containing cyanobacterium strain KC1 isolated from Lake Biwa // Photomed. Photobiol. 2011. V. 33. P. 35–40.

  6. Al-Bader D., Eliyas M., Rayan R., Radwan S. Subsurface associations of Acaryochloris-related picocyanobacteria with oil-utilizing bacteria in the Arabian Gulf water body: promising consortia in oil sediment bioremediation // Microb. Ecol. 2013. V. 65. P. 555–565.

  7. Allakhverdiev S.I., Kreslavski V.D., Zharmukhamedov S.K., Voloshin R.A., Korol’kova D.V., Tomo T., Shen J.R. Chlorophylls d and f and their role in primary photosynthetic processes of cyanobacteria // Biochemistry (Moscow). 2016. V. 81. P. 201–212.

  8. Allen J.F. Protein phosphorylation in regulation of photosynthesis // Biochim. Biophys. Acta. 1992. V. 1098. P. 275‒335.

  9. Amesz J., Neerken S. Excitation energy trapping in anoxygenic photosynthetic bacteria // Photosynth. Res. 2002. V. 73. P. 73‒81.

  10. Antonaru L.A., Cardona T., Larkum A.W.D., Nürnberg D.J. Global distribution of a chlorophyll f cyanobacterial marker // ISME J. 2020. V. 14. P. 2275–2287. https://doi.org/10.1038/s41396-020-0670-y

  11. Averina S., Polyakova E., Senatskaya E., Pinevich A. A new cyanobacterial genus Altericista and three species Altericista lacusladogae sp. nov., Altericista violacea sp. nov., and Altericista variichlora sp. nov., described using a polyphasic approach // J. Phycol. 2021. V. 57. P. 1517‒1529.

  12. Averina S.G., Velichko N.V., Pinevich A.A., Senatskaya E.V., Pinevich A.V. 2019. Non-a chlorophylls in cyanobacteria // Photosynthetica. 2019. V. 57. P. 1109‒1118.

  13. Averina S., Velichko N., Senatskaya E., Pinevich A. Far-red photoadaptations in aquatic cyanobacteria // Hydrobiologia. 2018. V. 813. P. 1‒17.

  14. Badshah S.L., Mabkhot Y., Al-Showiman S.S. Photosynthesis at the far-red region of the spectrum in Acaryochloris marina // Badshah and Mabkhot Biol. Res. 2017. V. 50. Art. 16. https://doi.org/10.1186/s40659-017-0120-0

  15. Bar-Zvi S., Lahav A., Harris D., Niedzwiedzki D.M., Blankenship R.E., Adir N. Structural heterogeneity leads to functional homogeneity in A. marina phycocyanin // Biochim. Biophys. Acta Bioenerg. 2018. V. 1859. P. 544‒553.

  16. Bauer C.E., Bollivar D.W., Suzuki J.Y. Genetic analyses of photopigment biosynthesis in eubacteria: a guiding light for algae and plants // J. Bacteriol. 1993. V. 175. P. 3919‒3925.

  17. Behrendt L., Brejnrod A.S., Schliep M., Sørensen S.J., Larkum A.W.D., Kühl M. Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium // ISME J. 2015. V. 9. P. 2108–2111.

  18. Behrendt L., Larkum A.W.D., Norman A., Qvortrup R., Chen M., Ralph P., Sørensen S.J., Trampe E., Kühl M. Endolithic chlorophyll d-containing phototrophs // ISME J. 2011. V. 5. P. 1072–1076.

  19. Behrendt L., Nielsen J.L., Sørensen S.J., Larkum A.W.D., Winther J.R., Kühl M. Rapid TaqMan-based quantification of chlorophyll d-containing cyanobacteria in the genus Acaryochloris // Appl. Environ. Microbiol. 2014. V. 80. P. 3244–3249.

  20. Behrendt L., Staal M., Cristescu S.M., Harren F.J.M., Schliep M., Larkum A.W.D., Kühl M. Reactive oxygen production induced by near-infrared radiation in three strains of the Chl d-containing cyanobacterium Acaryochloris marina // F1000Research. 2013. V. 2. Art. 44. https://doi.org/10.12688/f1000research.2-44.v.2

  21. Blankenship R.E., Chen M. Spectral expansion and antenna reduction can enhance photosynthesis for energy production // Curr. Opin. Chem. Biol. 2013. V. 17. P. 457‒461.

  22. Bryant D.A., Garcia-Costas A.M., Maresca J.A., Chew A.G.M., Klatt C.G., Bateson M.M., Tallon L.J., Hostetler J., Nelson W.C., Heidelberg J.F., Ward D.W. Candidatus Chloracidobacterium thermofilum: an aerobic phototrophic acidobacterium // Science. 2007. V. 317. P. 523‒526.

  23. Bryant D.A., Shen G., Turner G.M., Soulier N., Laremore T.N., Ho M.-Y. Far-red light allophycocyanin subunits play a role in chlorophyll d accumulation in far-red light // Photosynth. Res. 2020. V. 143. P. 81–95.

  24. Burger-Wiersma T., Stal L., Mur L.R. 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 // Int. J. Syst. Evol. Microbiol. 1989. V. 39. P. 250‒257.

  25. Cardona T., Murray J.W., Rutherford A.W. Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria // Mol. Biol. Evol. 2015. V. 32. P. 1310‒1328.

  26. Castenholz R.W. General characteristics of the cyanobacteria // Bergey’s Manual of Systematics of Archaea and Bacteria / Eds. DeVos P. et al. Hobolken, NJ: Wiley and Sons, Inc., 2015. https://doi.org/10.1002/9781118960608.cbm00019

  27. Chen M., Bibby T.S., Nield J., Larkum A.W.D., Barber J. Iron deficiency induces a chlorophyll d-binding Pcb antenna system around photosystem I in Acaryochloris marina // Biochim. Biophys. Acta. 2005a. V. 1708. P. 367–374.

  28. Chen M., Bibby T.S., Nield J., Larkum A.W.D., Barber J. Structure of a large photosystem II supercomplex from Acaryochloris marina // FEBS Letters. 2005b. V. 579. P. 306–1310.

  29. Chen M., Blankenship R.E. Expanding the solar spectrum used by photosynthesis // Trends Plant Sci. 2011. V. 16. P. 427‒431.

  30. Chen M., Floetenmeyer M., Bibby T. Supramolecular organization of phycobiliproteins in the chlorophyll d-containing cyanobacterium Acaryochloris marina // FEBS Lett. 2009. V. 583. P. 2535‒2539.

  31. Chen M., Hernandez-Prieto M.A., Loughlin P.C., Li Y., Willows R.D. Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptive proteomic shifts under different light conditions // Genomics. 2019. V. 20. Art. 207. https://doi.org/10/1186/s12864-019-5587-3

  32. Chen M., Hiller R.G., Howe C.J., Larkum A.W.D. Unique origin and lateral transfer of prokaryotic chlorophyll-b and chlorophyll-d light-harvesting systems // Mol. Biol. Evol. 2005c. V. 22. P. 21–28.

  33. Chen M., Li Y., Birch D., Willows R.D. A cyanobacterium that contains chlorophyll f ‒ a red-absorbing photopigment // FEBS Lett. 2012. V. 586. P. 3249–3254.

  34. Chen M., Schliep M., Willows R.D., Cai Z.L., Neilan B.A., Scheer H. A red-shifted chlorophyll // Science. 2010. V. 329. P. 1318–1319.

  35. Chen M., Telfer A., Lin S., Pascal A., Larkum A.W.D., Barber J., Blankenship R.E. The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina // Photochem. Photobiol. Sci. 2005d. V. 4. P. 1060–1064.

  36. Chen M., Zhang Y., Blankenship R.E. Nomenclature for membrane bound light harvesting complexes of cyanobacteria // Photosynth. Res. 2008. V. 95. P. 147–154.

  37. Cherepanov D.A., Shelaev I.V., Gostev F.E., Aybush A.V., Mamedov M.D., Shen G., Nadtochenko V.A., Bryant D.A., Semenov A.Y., Golbeck J.H. Evidence that chlorophyll f functions solely as an antenna pigment in far-red-light photosystem I from Fischerella thermalis PCC 7521 // Biochim. Biophys. Acta Bioenerg. 2020. V. 1861. Art. 148184. https://doi.org/10.1016/j.bbabio.2020.148184

  38. Chisholm S.W., Frankel S.L., Goericke R., Olson J.R., Palenik B., Waterbury J.B., West-Johnsrud L., Zettler E.R. Prochlorococcus marinus nov. gen., nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chloro-phyll a and b // Arch. Microbiol. 1992. V. 157. P. 297–300.

  39. Deisenhofer J., Michel H., Huber R. The structural basis of photosynthetic light reactions in bacteria // Trends Biochem. Sci. 1985. V. 10. P. 243‒248.

  40. Drews G., Niederman R.A. Membrane biogenesis in anoxygenic photosynthetic prokaryotes // Photosynth. Res. 2002. V. 73. P. 87‒94.

  41. Fleming E.D., Prufert-Bebout L. Characterization of cyanobacterial communities from high-elevation lakes in the Bolivian Andes // J. Geophys. Res. 2010. V. 115. Art. 00D07. https://doi.org/10.1029/2008JG000817

  42. French C.S. The chlorophyll in vivo and in vitro // Encyclopedia of Plant Physiology / Ed. Ruhland W. Berlin: Springer-Verlag. 1960. V. 5. Pt. 1. P. 252–297.

  43. Friedrich T., Schmitt F.J. Red-shifted and red chlorophylls in photosystems: entropy as a driving force for uphill energy transfer // Photosynthesis: Molecular Approaches to Solar Energy Conversion. Advances in Photosynthesis and Respiration / Eds. Shen J.R. et al. Cham: Springer. 2021https://doi.org/10.1007/978-3-030-67407-6_9

  44. Fukusumi T., Matsuda K., Mizoguchi T., Miyatake T., Ito S., Ikeda T., Tamiaki H., Oba T. Non-enzymatic conversion of chlorophyll-a into chlorophyll-d in vitro: a model oxidation pathway for chlorophyll-d biosynthesis // FEBS Lett. 2012. V. 586. P. 2338–2341.

  45. Gan F., Bryant D.A. Adaptive and acclimative responses of cyanobacteria to far-red light // Environ. Microbiol. 2015. V. 17. P. 3450–3465.

  46. Gan F., Shen G., Bryant D. Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria // Life (Basel). 2015. V. 5. P. 4–24.

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

  48. Gisriel C.J., Cardona T., Bryant D.A., Brudvig C.W. Molecular evolution of far-red light-acclimated photosystem II // Microorganisms. 2022. V. 10. Art. 1270. https://doi.org/10.3390/microorganisms10071270

  49. Gisriel C.J., Shen G., Ho M.-Y., Kurashov V., Flesher D.A., Wang J., Armstrong W.H., Golbeck J.H., Gunner M.R., Vinyard D.J., Debus R.J., Brudvig G.W., Bryant D.A. Structure of a monomeric photosystem II core complex from a cyanobacterium acclimated to far-red-light reveals the functions of chlorophylls d and f // J. Biol. Chem. 2021. V. 298. Art. 101424. https://doi.org/10.1016/j.jbc.2021.101424

  50. Gisriel C., Shen G., Kurashov V., Ho M.-Y., Zhang S., Williams D., Golbeck J.H., Fromme P., Bryant D.A. The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis // Sci. Adv. 2020. V. 6. Art. aay6415. https://doi.org/10.1126/sciadv.aay6415

  51. Glazer A.N., Bryant D.A. Allophycocyanin B (λmax 671, 618 nm) – a new cyanobacterial phycobiliprotein // Arch. Mikrobiol. 1975. V. 104. P. 15–22.

  52. Gómez-Lojero C., Leyva-Castillo L.E., Herrera-Salgado P., Barrera-Rojas J., Ríos-Castro E., Gutiérrez-Cirlos E.B. Leptolyngbya CCM 4, a cyanobacterium with far-red photoacclimation from Cuatro Ciénegas Basin, México // Photosynthetica. 2018. V. 56. P. 342–353.

  53. Gorka M., Baldansuren A., Malnati A., Gruszecki E., Golbeck J.H., Lakshmi K.V. Shedding light on primary donors in photosynthetic reaction centers // Front. Microbiol. 2021. V. 12. Art. 735666. https://doi.org/10.3389/fmicb.2021.735666

  54. Grossman A.R., Schaefer M.R., Chiang G.G., Collier J.L. The phycobilisome, a light-harvesting complex responsive to environmental conditions // Microbiol. Rev. 1993. V. 57. P. 725‒749.

  55. Hamaguchi T., Kawakami K., Shinzawa-Itoh K., Inoue-Kasino N., Itoh S., Ifuku K., Yamashita E., Maeda K., Yonekura K., Kasino Y. Structure of the far-red light utilizing photosystem I of Acaryochloris marina // Nat. Commun. 2021. V. 12. Art. 2333. https://doi.org/10.1038/s41467-021-22502-8

  56. Hastings H., Makita H., Agarwala N., Rohani L., Shen G., Bryant D.A. Fourier transform visible and infrared difference spectroscopy for the study of P700 in photosystem I from Fischerella thermalis PCC 7521 cells grown under white light and far-red light: Evidence that the A–1 cofactor is chlorophyll f // Biochim. Biophys. Acta – Bioenerg. 2019. V. 1860. P. 452‒460.

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

  58. Ho M.-Y., Bryant D.A. Global transcriptional profiling of the cyanobacerium Chlorogloeopsis fritschii PCC 9212 in far-red light: insights into the regulation of chlorophyll d synthesis // Front. Microbiol. 2019. V. 10. Art. 465. https://doi.org/10.3389/fmicb.2019.00465

  59. Ho M.-Y., Gan F., Shen G., Bryant D.A. Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II. Characterization of phycobiliproteins produced during acclimation to far-red light // Photosynth. Res. 2017a. V. 131. P. 187‒202.

  60. Ho M.-Y., Gan F., Shen G., Zhao C., Bryant D.A. Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. I. Regulation of FaRLiP gene expression // Photosynth. Res. 2017b. V. 131. P. 173‒186.

  61. Ho M.-Y., Shen G., Canniffe D.P., Zhao C., Bryant D.A. Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II // Science. 2016. V. 353. Art. aaf9178. https://doi.org/10.1126/science.aaf.9178

  62. Holt A.S. Further evidence of the relation between 2-desvinyl-2-formyl-chlorophyll a and d // Can. J. Bot. 1961. V. 39. P. 327–331.

  63. Hu Q., Marquardt J., Iwasaki I., Miyashita H., Kurano N., Mörschel E., Miyachi S. Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina // Biochim. Biophys. Acta. 1999. V. 1412. P. 250–261.

  64. Hu Q., Miyashita H., Iwasaki I., Kurano N., Miyachi S., Iwaki M., Itoh S. A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis // Proc. Natl. Acad. Sci. USA. 1998. V. 95. P. 13319–13323.

  65. Hunter C.N., van Grondelle R., Olsen J.D. Photosynthetic antenna proteins: 100 ps before photochemistry starts // Trends Biochem. Sci. 1989. V. 14. P. 72‒76.

  66. Itoh S., Mino H., Itoh K., Shigenaga T., Uzumaki T., Iwaki M. Function of chlorophyll d in reaction centers of photosystems I and II of the oxygenic photosynthesis of Acaryochloris marina // Biochemistry. 2007. V. 46. P. 12473–12481.

  67. Itoh S., Ohno T., Noji T., Yamakawa H., Komatsu H., Wada K., Kobayashi M., Miyashita Y. Harvesting far-red light by chlorophyll f in photosystems I and II of unicellular cyanobacterium strain KC1 // Plant Cell Physiol. 2015. V. 56. P. 2024–2034.

  68. Judd M., Mortona J., Nürnberg D., Fantuzzi A., Rutherford A.W., Purchase R., Cox N., Krausz E. The primary donor of far-red photosystem II: ChlD1 or PD2? // Biochim. Biophys. Acta – Bioenerg. 2020. V. 1861. Art. 1482. https://doi.org/10.1016/j.bbabio.2020.148248

  69. Kashiyama Y., Miyashita H., Ohkubo S., Ogawa N.O., Chikaraishi Y., Takano Y., Suga H., Toyofuku T., Nomaki H., Kitazato H., Nagata T., Ohkouchi K. Evidence for global chlorophyll d // Science. 2008. V. 321. P. 658.

  70. Kiang N.Y., Swingley W.D., Gautam D., Broddrick J.T., Repeta D.J., Stolz J.F., Blankenship R.E., Wolf B.M., Detweiler A.M., Miller K.A., Schladweiler J.J., Lindeman R., Parenteau M.N. Discovery of chlorophyll d: isolation and characterization of a far-red cyanobacterium from the original site of Manning and Strain (1943) at Moss Beach, California // Microorganisms. 2022. V. 10. Art. 819. https://doi.org/10.3390microorganisms10040819

  71. Kimura A., Kitoh-Nishioka H., Aota T., Hamaguchi T., Yonekura K., Kawakami K., Shinzawa-Itoh K., Inoue-Kasino N., Ifuku K., Yamasita E., Kasino Y., Itoh S. Theoretical model of the far-red-light-adapted photosystem I reaction center of cyanobacterium Acaryochloris marina using chlorophyll d and the effect of chlorophyll exchange // J. Phys. Chem. 2022. V. 126. P. 4009‒4021.

  72. Kirk J.T.O. Light and Photosynthesis in Aquatic Ecosystems, 2nd ed. Cambridge e.a.: Cambridge Univ. Press, 1994. 509 p.

  73. Koizumi H., Itoh Y., Hosoda S., Akiyama M., Hoshino T., Shiraiwa Y., Kobayashi M. Serendipitous discovery of Chl d formation from Chl a with papain // Sci. Technol. Adv. Mater. 2005. V. 6. P. 551–557.

  74. Kühl M., Chen M., Ralph P.J., Schreiber U., Larkum A.W.D. A niche for cyanobacteria containing chlorophyll d // Nature. 2005. V. 433. P. 820.

  75. Larkum A.W.D., Chen M., Li Y., Schliep M., Trampe E., West J., Salih A., Kühl M. A novel epiphytic chlorophyll d-containing cyanobacterium isolated from mangrove-associated red alga // J. Phycol. 2012. V. 48. P. 1320–1327.

  76. Larkum A.W.D., Ritchie R.J., Raven J.A. Living off the Sun: chlorophylls, bacteriochlorophylls and rhodopsins // Photosynthetica. 2018. V. 56. P. 11‒43.

  77. La Roche J., van der Staay G.W.M., Partensky F., Ducret A., Aebersold R., Li R., Golden S.S., Hiller R.G., Wrench P.M., Larkum A.W.D., Green B.R. Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins // Proc. Natl. Acad. Sci. USA. 1996. V. 93. P. 15244–15248.

  78. Lewin R.A. Prochlorophyta as a proposed new division of algae // Nature. 1976. V. 261. P. 697–698.

  79. Li Y., Chen M. Novel chlorophylls and new directions in photosynthesis research // Funct. Plant Biol. 2015. V. 42. P. 493‒501.

  80. Li Y., Larkum A., Schliep M., Kühl M., Neilan B., Chen M. Newly isolated Chl d-containing cyanobacteria // Photosynthesis Research for Food, Fuel and the Future. Proc. 15th Int. Conf. on Photosynthesis / Eds. Kuang T., Lu C., Zhang L. Springer Science + Business Media B.V., 2013. P.  686‒690.

  81. Li Y., Lin Y., Garvey C.J., Birch D., Corkery R.W., Loughlin P.C., Scheer H., Willows R.D., Chen M. Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris // Biochim. Biophys. Acta. 2016. V. 1857. P. 107–114.

  82. Lin Y., Crossett B., Chen M. Effects of anaerobic conditions on photosynthetic units of Acaryochloris marina // Photosynthesis Research for Food, Fuel and the Future: 15th Int. Conf. on Photosynthesis / Eds. Kuang T., Lu C., Zhang L. Springer Science + Business Media B.V., 2013. P. 121‒124.

  83. López-Legentil S., Song B., Bosch M., Pawlik J.R., Turon X. Cyanobacterial diversity and a new Acaryochloris-like symbiont from Bahamian sea-squirts // PLoS One. 2011. V. 6. Art. e23938. https://doi.org/10.1371/journal.pone.0023938

  84. Loughlin P., Lin Y., Chen M. Chlorophyll d and Acaryochloris marina: current status // Photosynth. Res. 2013. V. 116. P. 277–293.

  85. MacColl R. Cyanobacterial phycobilisomes // J. Struct. B-iol. 1998. V. 124. P. 311−334.

  86. Manning W.M., Strain H.H. Chlorophyll d, a green pigment of red algae // J. Biol. Chem. 1943. V. 151. P. 1‒19.

  87. Martinez-Garcia M., Koblızek M., Lopez-Legentil S., Anton J. Epibiosis of oxygenic phototrophs containing chlorophylls a, b, c and d on the colonial ascidian Cystodytes dellechiajei // Microb. Ecol. 2011. V. 61. P. 13–19.

  88. Mascoli V., Bhatti A.F., Bersanini L., van Amerongen H., Croce R. The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficieny of Photosystem II // Nat. Commun. 2022. V. 13. Art. 3562. https://doi.org/10.1038/s41467-022-31099-5

  89. McNamara C.J., Perry-VI T.D., Bearce K.A., Hernandez-Duque G., Mitchell R. Epilithic and endolithic bacterial communities in limestone from a Mayan archaeological site // Microb. Ecol. 2006. V. 51. P. 51–64.

  90. Miao D., Ding W.-L., Zhao B.-Q., Lu L., Xu Q.-Z., Scheer H., Zhao K.-H. Adapting photosynthesis to the near-infrared: non-covalent binding of phycocyanobilin provides an extreme spectral red-shift to phycobilisome core-membrane linker from Synechococcus sp. PCC 7335 // Biochim. Biophys. Acta. 2016. V. 1857. P. 688–694.

  91. Miller S.R., Augustine S., Olson T.L., Blankenship R.E., Selker J., Wood A.M. Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial cyanobacterial small-subunit rRNA gene // Proc. Natl. Acad. Sci. USA. 2005. V. 102. P. 850‒855.

  92. Miller S.R., Wood A.M., Blankenship R.E., Kim M.N., Ferriera S. Dynamics of gene duplication in the genomes of chlorophyll d-producing cyanobacteria: implications for the ecological niche // Genome Biol. Evol. 2011. V. 3. P. 601–613. https://doi.org/10.1093/gbe/evr060

  93. Mimuro M., Akimoto S., Gotoh T., Yokono M., Akiyama M., Tsuchiya T., Miyashita H., Kobayashi M., Yamazaki I. Identification of the primary electron donor in PS II of the Chl d-dominated cyanobacterium Acaryochloris marina // FEBS Lett. 2004. V. 556. P. 95–98.

  94. Mimuro M., Akimoto S., Yamazaki I., Miyashita H., Miyachi S. Fluorescence properties of chlorophyll d-dominating prokaryotic alga, Acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells // Biochim. Biophys. Acta. 1999. V. 1412. P. 37–46.

  95. Mimuro M., Hirayama K., Uezono K., Miyashita H., Miyachi S. Uphill energy transfer in a chlorophyll d-dominating oxygenic photosynthetic prokaryote, Acaryochloris marina // Biochim. Biophys. Acta. 2000. V. 1456. P. 27–34.

  96. Miyashita H., Adachi K., Kurano N., Ikemoto H., Chihara M., Miyachi S. Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll // Plant Cell Physiol. 1997. V. 38. P. 274–281.

  97. Miyashita H., Ikemoto H., Kurano N., Adachi K., Chihara M., Miyachi S. Chlorophyll d as a major pigment // Nature. 1996. V. 383. P. 402.

  98. Miyashita H., Ikemoto H., Kurano N., Miyachi S., Chihara M. Acaryochloris marina gen. et sp. nov. (Cyanobacteria), an oxygenic photosynthetic prokaryote containing chlorophyll d as a major pigment // J. Phycol. 2003. V. 39. P. 1247‒1253.

  99. Miyashita H., Ohkubo S., Komatsu H., Sorimachi Y., Fukayama D., Fujinuma D., Akitsu S., Kobayashi M. Discovery of chlorophyll d in Acaryochloris marina and chlorophyll f in a unicellular cyanobacterium, strain KC1, isolated from Lake Biwa // J. Phys. Chem. Biophys. 2014. V. 4. Art. 149. https://doi.org/10.4172/2161-0348.1000149

  100. Mohr R., Voß B., Schliep M., Kurz T., Maldener I., Adams D.G., Larkum A.W.D., Chen M., Hess W.R. A new chlorophyll d-containing cyanobacterium: evidence for niche adaptation in the genus Acaryochloris // ISME J. 2010. V. 4. P. 1456–1469.

  101. Murakami A., Miyashita H., Iseki M., Adachi K., Mimuro M. Chlorophyll d in an epiphytic cyanobacterium of red algae // Science. 2004. V. 303. P. 1633.

  102. Murray J.W. Sequence variation at the oxygen evolving centre of photosystem II: a new class of ‘rogue’ cyanobacterial D1 proteins // Photosynth. Res. 2012. V. 110. P. 177–184.

  103. Neerken S., Amesz J. The antenna reaction center complex of heliobacteria: composition, energy conversion and electron transfer // Biochim. Biophys. Acta. 2001. V. 1507. P. 278‒290.

  104. Niedzwiedzki D.M., Bar-Zvi S., Blankenship R.E., Adir N. Mapping the excitation energy migration pathways in phycobilisomes from the cyanobacterium Acaryochloris marina // Biochim. Biophys. Acta Bioenerg. 2019. V. 1860. P. 286‒296.

  105. Niedzwiedzki D.M., Liu H., Chen M., Blankenship R.E. Excited state properties of chlorophyll f in organic solvents at ambient and cryogenic temperatures // Photosynth. Res. 2014. V. 121. P. 25‒34.

  106. Nürnberg D.J., Morton J., Santabarbara S., Telfer A., Joliot P., Antonaru L., Ruban A., Cardona T., Krausz F., Bousac A., Fantuzzi A., Rutherford A.W. Photochemistry beyond the red limit in chlorophyll f-containing photosystems // Science. 2018. V. 360. P. 1210‒1213.

  107. Ohkubo S., Miyashita H. Selective detection and phylogenetic diversity of Acaryochloris spp. that exist in association with didemnid ascidians and sponge // Microb. Environ. 2012. V. 27. P. 217–225.

  108. Ohkubo S., Miyashita Y., Murakami A., Takeyama H., Tsuchiya T., Mimuro M. Molecular detection of epiphytic Acaryochloris spp. on marine macroalgae // Appl. Environ. Microbiol. 2006. V. 72. P. 7912–7915.

  109. Partensky F., Six C., Ratin M., Garczarek L., Vaulot D., Probert I., Calteu A., Gourvil P., Marie D., Grébert T., Bouchier C., Le Panse S., Gachenot M., Rodriguez F., Garrido J.L. A novel species of the marine cyanobacterium Acaryochloris with a unique pigment content and lifestyle // Sci. Rep. 2018. V. 8. Art. 9142. https://doi.org/10.1038/s41598-018-27542-7

  110. Pinevich A., Averina S. New life for old discovery: amazing story about how bacterial predation on Chlorella resolved a paradox of dark cyanobacteria and gave the key to early history of oxygenic photosynthesis and aerobic respiration // Protistology. 2021. V. 15. P. 107‒126.

  111. Renger T., Schlodder E. 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 // J. Phys. Chem. 2008. V. 112. P. 7351–7354.

  112. de los Rios A., Grube M., Sancho L.G., Ascaso C. Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks // FEMS Microb. Ecol. 2007. V. 59. P. 386–395.

  113. Sawicki A., Chen M. Molecular mechanism of photosynthesis driven by red-shifted chlorophylls // Microbial Photosynthesis / Eds. Wang Q. et al. Singapore: Springer, 2020. https://doi.org/0.1007/978-981-15-3110-1_1

  114. Schiller H., Senger H., Miyashita H., Miyachi S., Dau H. Light-harvesting in Acaryochloris marina ‒ spectroscopic characterization of a chlorophyll d-dominated photosynthetic antenna system // FEBS Lett. 1997. V. 30. P. 433‒436.

  115. Schliep M., Chen M., Larkum A., Quinnell R. The function of MgDVP in a chlorophyll d-containing organism // Photosynthesis. Energy from the Sun / Eds. Allen J.F. et al. Dordrecht: Springer, 2008. P. 1125‒1128.

  116. Schliep M., Crossett B., Willows R.D., Chen M. 18O labeling of chlorophyll d in Acaryochloris marina reveals that chlorophyll a and molecular oxygen are precursors // J. Biol. Chem. 2010. V. 285. P. 28450–28456.

  117. Schmitt F.-J., Campbell Z.Y., Bui M.V., Hüls A., Tomo T., Chen M., Maksimov E.G., Allakhverdiev S.I., Friendrich T. Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light // Photosynth. Res. 2019. V. 139. P. 185‒201.

  118. Shen G., Canniffe D.P., Ho M.Y., Kurashov V., van der Est A., Golbeck J.Y., Bryant D.A. Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002 // Photosynth. Res. 2019. V. 140. P. 77–92.

  119. Shen L.-Q., Zhang Z.-C., Shang J.-L., Li Z.-K., Chen M., Li R., Qiu B.-S. Kovacikia minuta sp. nov. (Leptolyngbyaceae, Cyanobacteria), a new freshwater chlorophyll f-producing cyanobacterium // J. Phycol. 2022. Accepted. https://doi.org/10.1111/jpy.13248

  120. Soulier N., Laremore T.N., Bryant D.A. Characterization of cyanobacterial allophycocyanins absorbing far-red light // Photosynth. Res. 2020. V. 145. P. 189–207.

  121. 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. Niche adaptation and genome expansion in the chlorophyll d producing cyanobacterium Acaryochloris marina // Proc. Natl. Acad. Sci. USA. 2008. V. 105. P. 2005–2010.

  122. Swingley W.D., Hohmann-Marriott M.F., Olson T.L., Blankenship R.E. Effect of iron on growth and ultrastructure of Acaryochloris marina // Appl. Environ. Microbiol. 2005. V. 71. P. 8606‒8610.

  123. Tomo T., Kato Y., Suzuki T., Akimoto S., Okubo T., Noguchi T., Hasegawa K., Tsuchiya T., Tanaka K., Fukuya M., Dohmae N., Watanabe T., Mimuro M. Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017 // J. Biol. Chem. 2008. V. 283. P. 18198–18209.

  124. Tomo T., Okubo T., Akimoto S., Yokono M., Miyashita H., Tsuchiya T., Noguchi T., Mimuro M. Identification of the special pair of photosystem II in a chlorophyll d dominated cyanobacterium // Proc. Natl. Acad. Sci. USA. 2007. V. 104. P. 7283–7288.

  125. Tomo T., Shinoda T., Chen M., Allakhverdiev S.I., Akimoto S. Energy transfer processes in chlorophyll f-containing cyanobacteria using time-resolved fluorescence spectroscopy on intact cells // Biochim. Biophys. Acta. 2014. V. 1837. P. 1484–1489.

  126. Trampe E., Kühl M. Chlorophyll f distribution and dynamics in cyanobacterial beachrock biofilms // J. Phycol. 2016. V. 52. P. 990‒996.

  127. Trinugroho J.P., Bečková M., Shao S., Yu J., Zhao Z., Murray J.W., Sobotka R., Komenda J., Nixon P.J. Chlorophyll f synthesis by a super-rogue photosystem II complex // Nat. Plants. 2020. V. 6. P. 238–244.

  128. Tsuzuki Y., Tsukatani Y., Yamakawa H., Itoh S., Fujita Y., Yamamoto H. Effects of light and oxygen on chlorophyll d biosynthesis in a marine cyanobacterium Acaryochloris marina // Plants. 2022. V. 11. Art. 915. https://doi.org/10.3390/plants11070915

  129. Ulrich N.J., Uchida H., Kanesaki Y., Hirose E., Murakami A., Miller S.R. Reacquisition of light-harvesting genes in a marine cyanobacterium confers a broader solar niche // Curr. Biol. 2021. V. 31. P. 1539‒1546.

  130. Wood A.M. Acaryochloris ‒ explaining the riddle of chlorophyll d in red algae and expanding PAR for oxygenic photosynthesis // J. Phycol. V. 48. P. 1317‒1319.

  131. Xu C., Zhu Q., Chen J.-H., Shen L., Yi X., Huang Z., Wang W., Chen M., Kuang T., Shen J.-R., Zhang X., Han G. A unique photosystem I reaction center from a chlorophyll d-containing cyanobacterium Acaryochloris marina // J. Integr. Plant Biol. 2021. V. 63. P. 1740‒1752. https://doi.org/10.1111/jipb.13113

  132. Yoneda A., Wittmann B.J., King J.D., Blankenship R.E., Dantas G. Transcriptomic analysis illuminates genes involved in chlorophyll synthesis after nitrogen starvation in Acaryochloris sp. CCMEE 5410 // Photosynth. Res. 2016. V. 129. P. 171–182.

  133. Zhang Z.-C., Li Z.-K., Yin Y.-C., Li Y., Jia Y., Chen M., Qiu B.-S. Widespread occurrence and unexpected diversity of red-shifted chlorophyll-producing cyanobacteria in humid subtropical forest ecosystems // Environ. Microbiol. 2019. V. 21. P. 1497‒1510. https://doi.org/10.1111/1462-2920.14582

  134. Zhao C., Gan F., Shen G., Bryant D.A. RfpA, RfpB, and Rf-pC are the master control elements of far-red light photoacclimation (FaRLiP) // Front. Microbiol. 2015. V. 6. Art. 1303. https://doi.org/10.3389/fmicb.2015.01303

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