Photosynthetica, 2018 (vol. 56), issue 1

Photosynthetica 2018, 56(1):342-353 | DOI: 10.1007/s11099-018-0774-z

Leptolyngbya CCM 4, a cyanobacterium with far-red photoacclimation from Cuatro Ciénegas Basin, México

C. Gómez-Lojero1,*, L. E. Leyva-Castillo1, P. Herrera-Salgado1, J. Barrera-Rojas1, E. Ríos-Castro2, E. B. Gutiérrez-Cirlos3
1 Departmento de Bioquímica, Centro de Investigación y Estudios Avanzados del IPN, CdMx, Mexico
2 Laboratorio Nacional de Servicios Experimentales Centro de Investigación y Estudios Avanzados del IPN, Tlanepantla, Mexico
3 Unidad de Biomedicina, FES-Iztacala UNAM, Tlanepantla, Mexico

A cyanobacterium containing phycobiliproteins with far-red acclimation was isolated from Pozas Rojas, Cuatro Ciénegas, México. It was named Leptolyngbya CCM 4 after phylogenetic analysis and a description of its morphological characteristics. Leptolyngbya was grown in far-red light. Sucrose-gradient analysis of the pigments revealed two different colored bands of phycobiliproteins. A band at 60% sucrose was a phycocyanin containing phycobilisome; at 35% sucrose, a new type of phycobiliprotein absorbed at 710 nm. SDS-PAGE revealed the presence of two types of core-membrane linkers. Analysis of the hydrophobic pigments extracted from the thylakoid membranes revealed Chl a, d, and f. The ratio of Chl f/a was reversibly changed from 1:12-16 under far-red light to an undetectable concentration of Chl f under white light. Cuatro Ciénegas, a place surrounded by the desert, is a new ecosystem where a cyanobacterium, which grows in farred light, was discovered.

Keywords: chlorophyll f; Cuatro Ciénegas Basin; far-red light; photosynthesis; phycobilisomes

Received: June 28, 2017; Accepted: December 5, 2017; Published: March 1, 2018Show citation

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Gómez-Lojero, C., Leyva-Castillo, L.E., Herrera-Salgado, P., Barrera-Rojas, J., Ríos-Castro, E., & Gutiérrez-Cirlos, E.B. (2018). Leptolyngbya CCM 4, a cyanobacterium with far-red photoacclimation from Cuatro Ciénegas Basin, México. Photosynthetica56(1), 342-353. doi: 10.1007/s11099-018-0774-z.
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References

  1. Adir N.: Elucidation of the molecular structures of components of the phycobilisome: Reconstructing a giant.-Photosynth. Res. 85: 15-32, 2005. Go to original source...
  2. Airs R.L., Temperton B., Sambles C. et al.: Chl f and Chl d are produced in the cyanobacterium Chlorogloeopsis fritschii when cultured under natural light and near-infrared radiation.-FEBS Lett. 588: 3770-3777, 2014. Go to original source...
  3. Akutsu S., Fujinuma D., Furukawa H. et al.: Pigment analysis of a Chl f-containing cyanobacterium strain KC1 isolated from Lake Biwa.-Photomed. Photobiol. 33: 35-40, 2011.
  4. Alcántara-Sánchez F., Leyva-Castillo L.E., Chagolla-López A. et al.: Distribution of isoforms of ferredoxin-NADP+ reductase (FNR) in cyanobacteria in two growth conditions.-Int. J. Biochem. Cell B. 85: 123-134, 2017. Go to original source...
  5. Alcaraz L.D., Olmedo G., Bonilla G.: The genome of Bacillus cohauilensis reveals adaptations essential for survival in the relic of an ancient marine environment.-P. Natl. Acad. Sci. USA 105: 5803-5808, 2008. Go to original source...
  6. Anderson L., Eiserling F.A.: Asymmetrical core structure in phycobilisomes of the cyanobacterium Synechocystis sp. PCC 6701.-J. Mol. Biol. 191: 441-451, 1986. Go to original source...
  7. Behrendt L., Brejnrod A., Schliep M. et al.: Chl f-driven photosynthesis in a cavernous cyanobacterium.-ISME J. 9: 2108-2111, 2015. Go to original source...
  8. Bryant D.A., Guglielmi G., de Marsac N.T. et al.: The structure of the cyanobacterial phycobilisomes: a model.-Arch. Microbiol. 123: 113-127, 1979. Go to original source...
  9. Cárabez-Trejo A., Sandoval F.: A mitochondrial inner membrane preparation that sediments at 100 g.-J. Cell Biol. 62: 877-881, 1974. Go to original source...
  10. Castenholtz R.W., Rippka R., Herdman M., Wilmotte A.: Formgenus V. Leptolyngbya Anagnostidis and Komarek 1988.-In: Boone D.R., Castenholtz R.W. (ed.): Bergey's Manual of Systematic Bacteriology, Vol. 1. Pp. 544-546. Springer-Verlag, New York 2001.
  11. Chang L., Liu X., Li Y. et al.: Structural organization of an intact phycobilisome and its association with photosystem II.-Cell Res. 25: 726-737, 2015. Go to original source...
  12. Chen M., Schliep M., Willows R.D. et al: A red-shifted chlorophyl.-Science 329: 1318-1319, 2010. Go to original source...
  13. Chen M., Blankenship R.E.: Expanding the solar spectrum used by photosynthesis.-Trends Plant Sci 16: 427-431, 2011. Go to original source...
  14. Chen M., Li Y., Birch D., Willows R.D.: A cyanobacterium that contains Chl far red absorbing photopigment.-FEBS Lett. 586: 3249-3254, 2012. Go to original source...
  15. Chen M., Floetenmeyer M., Bibby T.S.: Supramolecular organization of phycobiliproteins in the chlorophyll d-containing cyanobacterium Acariochloris marina.-FEBS Lett. 583: 2535-2539, 2009. Go to original source...
  16. Chisholm S.W., Olson R.J., Zettler E.R. et al: A novel free living prochlorophyte abundant in the oceanic euphotic zone.-Nature 334: 340-343, 1988. Go to original source...
  17. Couradeau E., Benzerara K., Moreira D. et al.: Prokaryotic and Eucaryotic communite structure in field and cultured microbialites from alkaline Lake Alchichica (Mexico).-PLoS ONE 6: e28767, 2011. Go to original source...
  18. Curtis S.E., Haselkorn R.: Isolation and sequence of the gene for large subunit of ribulose-1,5-bisphosphate carboxylase from the cyanobacterium Anabaena 7120.-P. Natl. Acad. Sci. USA 80: 1835-1839, 1983.
  19. Dong C., Tang A., Zhao J. et al.: ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002.-Biochim. Biophys. Acta. 1787: 1122-1128, 2009. Go to original source...
  20. Gan F., Bryant D.A.: Adaptive and acclimative responses of cyanobacteria to far-red light.-Environ. Microbiol. 17: 3450-3465, 2015. Go to original source...
  21. Gan F., Shen G., Bryant D.A.: Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria.-Life 5: 4-24, 2014b. Go to original source...
  22. Gan F., Zhang S., Rockwell N.C. et al.: Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light.-Science 345: 1312-1317, 2014a. Go to original source...
  23. Glazer A.N.: Phycobilisome a macromolecular complex optimized for light energy transfer.-BBA-Bioenergetics 768: 29-51, 1984. Go to original source...
  24. Glazer A.N.: Light guides.-J. Biol. Chem. 264: 1-4, 1989.
  25. Gómez-Lojero C., Pérez-Gómez B., Krogmann D.W. et al.: The tricylindrical core of the phycobilisome Arthrospira (Spirulina) maxima.-Int. J. Biochem. Cell. B. 29: 959-970, 19
  26. Gómez-Lojero C., Pérez-Gómez B., Shen G. et al.: Interaction of ferredoxin:NADP+ oxidoreductase with phycobilisomes and phycobilisome substructures of the cyanobacterium Synechococcus sp. Strain PCC 7002.-Biochemistry 42: 13800-13811, 2003. Go to original source...
  27. Grossman A.R.: A molecular understanding of complementary chromatic adaptation.-Photosynth. Res. 76: 207-215, 2003. Go to original source...
  28. Guglielmi G., Cohen-Bazire G., Bryant D.A.: The structure of Gloeobacter violaceus and its phycobilisome.-Arch. Microbiol. 129: 181-189, 1981. Go to original source...
  29. 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. 131: 187-202, 2017. Go to original source...
  30. Ho M.Y., Shen G., Canniffe D.P. et al.: Light-dependent Chl f synthase is a highly divergent paralog of PsbA of photosystem II.-Science 353: 886, 2016. Go to original source...
  31. Houmard J., Capuano V., Colombano M.V. et al.: Molecular characterization of the terminal energy acceptor of cyanobacterial phycobilisomes.-P. Natl. Acad. Sci. USA 87: 2152-2156, 1990. Go to original source...
  32. Hu Q., Marquardt J., Iwasaki I. et al.: Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic procaryote Acaryochloris marina.-Biochim Biophys Acta 1412: 250-261, 19 Go to original source...
  33. Itoh S., Ohno T., Noji T. et al.: Harvesting far-red light by chl f in photosystems I and II of unicellular cyanobacterium strain KC1.-Plant Cell Physiol. 56: 2024-2034, 2015. Go to original source...
  34. Jordan P., Fromme P., Witt H.T. et al.: Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution.-Nature 411: 909-917, 2001. Go to original source...
  35. Kehoe D.M., Gutu A.: Responding to color: the regulation of complementary chromatic adaptation.-Annu. Rev. Plant Biol. 57: 127-150, 2006. Go to original source...
  36. Li Y., Scales N., Blakenship R.E. et al.: Extinction coefficient for red-shifted Chls: Chl d and Chl f.-BBA-Bioenergetics 1817: 1292-1298, 2012.
  37. Li Y., Lin Y., Loughlin P.C., Chen M.: Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris a filamentous cyanobacterium containing Chl f.-Front. Plant Sci. 5: 67, 2014.
  38. Li Y., Lin Y., Garvey C.J. et al.: Characterization of red-shifted phycobilisomes isolated from the Chl f-containing cyanobacterium Halomicronema hongdechloris.-Biochim. Biophys. Acta 1857: 107-114, 20 Go to original source...
  39. Liu H., Zhang H., Niedzwiedzki D.M. et al.: Phycobilisomes supply excitations to both photosystems in a megacomplexes in cyanobacteria.-Science 342: 1104-1107, 2013. Go to original source...
  40. Loughlin P., Lin Y., Chen M.: Chlorophyl d and Acaryochloris marina: current status.-Photosynth. Res. 116: 277-293, 2013. Go to original source...
  41. Lundell D.J., Yamanaka G., Glazer A.N.: A terminal energy acceptor of the phycobilisome: the 75,000-dalton polypeptide of Synechococcus 6301 phycobilisome a new biliprotein.-J. Cell Biol. 91: 315-319, 1981. Go to original source...
  42. Mendoza-Hernández G., Pérez-Gómez B., Krogmann D.W. et al.: Interaction of linker proteins with the phycobiliproteins in the phycobilisome substructures of Gloeobacter violaceus.-Photosynth. Res. 106: 247-261, 20
  43. Mielke S., Kiang N., Blankenship R. et al.: Efficiency of photosynthesis in a Chl d-utilizing oxygenic species.-Biochim. Biophys. Acta 1807: 1231-1236, 2011.
  44. Mielke S.P. Kiang N.Y., Blankenship R.E., Mauzerall D.: Photosystem trap energies and spectrally-dependent energy storage efficiencies in the chl d-utilizing cyanobacterium, Acaryochloris marina.-BBA-Bioenergetics 1827: 255-265, 20 Go to original source...
  45. Mimuro M., Lipschultz C.A., Gantt E.: Energy flow in the phycobilisome core of Nostoc sp. (MAC): two independent terminal pigment.-BBA-Bioenergetics 852: 307-319, 1986. Go to original source...
  46. Moore L.R., Goericke R., Chisholm S.W.: Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties.-Mar. Ecol. Prog. Ser. 116: 250-275, 1995. Go to original source...
  47. Pérez-Gómez B., Mendoza-Hernández G., Cabellos-Avelar T. et al: A proteomic approach to the analysis of the components of the phycobilisomes from two cyanobacteria with complementary chromatic adaptation: Fremyella diplosiphon UTEX B590 and Tolypothrix PCC 7601.-Photosynth. Res. 114: 43-58, 2012. Go to original source...
  48. Perkerson III R.B., Johansen J.R., Kovácik L. et al: A unique Pseudanabaenalean (cyanobacteria) genus Nodosilinean gen. nov. based on morphological and molecular data.-J. Phycol. 47: 1397-1412, 2011. Go to original source...
  49. Reuter W., Wehrmeyer W.: Core structure in Mastigocladus laminosus phycobilisomes: II the central part of the tricylindrical core-APCM-contain the anchor polypeptide and no allophycocyanin B.-Arch. Microbiol. 153: 111-117, 1990. Go to original source...
  50. Schägger H., von Jagow G.: Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.-Anal. Biochem. 166: 368-379, 1987. Go to original source...
  51. Sidler W.A. Phycobilisome a phycobiliprotein Structures.-In: Bryant D.A. (ed.): The Molecular Biology of Cyanobacteria. Pp. 139-216. Kluwer Academic Publishers, Dordrecht 1994. Go to original source...
  52. Schluchter W.M., Bryant D.A.: Molecular characterization of ferredoxin NADP+ oxidoreductase in cyanobacteria: cloning and sequence of the petH gene of Synechococcus sp. PCC 7002 and studies in the gene product.-Biochemistry 31: 3092-3102, 1992. Go to original source...
  53. Souza V., Eguiarte L.E., Siefert J., Elser J.: Microbial endemism: does phosphorus limitation enhance speciation?-Nat. Rev. Microbiol. 6: 559-564, 2008. Go to original source...
  54. Souza V., Siefert J.L., Escalante A.E. et al.: The Cuatrociénegas Basin in Coahuila, México: An astrobiologial precambrian park.-Astrobiology 12: 641-647, 2012. Go to original source...
  55. Stackebrandt E., Goebel B.M.: Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology.-Int. J. Syst. Bacteriol. 44: 846-849, 1994. Go to original source...
  56. Stanier G. (Cohen-Bazire): Fine structure of cyanobacteria.-Methods Enzymol. 167: 157-172, 1988. Go to original source...
  57. Stevens Jr S.E., Pat Patterson C.O., Myers J.: The production of hydrogen peroxide by blue-green algae: A survey.-J. Phycol. 9: 427-430, 1973. Go to original source...
  58. Tandeau de Marsac N., Houmard J.: Complementary chromatic adaptation: Physiological conditions and action spectra.-Methods Enzymol. 167: 318-328, 1988.
  59. Taton A., Grubisic S., Brambilla E. et al.: Cyanobacterial diversity in natural and artificial microbial mat of Lake Fryxell (Mc Murdo Dry Valleys Antarctica): A morphological and molecular approach.-Appl. Environ. Microbiol. 69: 5157-5169, 2003. Go to original source...
  60. Umena Y., Kawakami K., Shen J.R., Kamiya N.: Crystal structure of oxygen evolving photosystem II at a resolution of 1.2 A.-Nature 473: 55-60, 2011. Go to original source...
  61. Wittig I., Karas M., Schägger H.: High resolution clear native electrophoresis for In-gel functional assays and fluorescence studies of membrane protein complexes.-Mol. Cell. Proteomics 6: 1215-1225, 2007. Go to original source...
  62. Yamanaka G., Glazer A.N., Williams R.C.: Cyanobacterial phycobilisomes. Characterization of the phycobilisomes of Synechococcus sp. 6301.-J. Biol. Chem. 253: 8303-8310, 1978.
  63. Zhang Z., Schwartz S., Wagner L., Miller W.: A greedy algorithm for aligning DNA sequences.-J. Comput. Biol. 7: 203-214, 2000. Go to original source...
  64. Zuker M.: Mfold web server for nucleic acid folding and hybridization prediction.-Nucleic Acids Res. 31: 3406-3415, 2003. Go to original source...