Photosynthesis Research

, Volume 128, Issue 3, pp 325–340 | Cite as

The siderophilic cyanobacterium Leptolyngbya sp. strain JSC-1 acclimates to iron starvation by expressing multiple isiA-family genes

  • Gaozhong Shen
  • Fei Gan
  • Donald A. Bryant
Original Article


In the evolution of different cyanobacteria performing oxygenic photosynthesis, the core complexes of the two photosystems were highly conserved. However, cyanobacteria exhibit significant diversification in their light-harvesting complexes and have flexible regulatory mechanisms to acclimate to changes in their growth environments. In the siderophilic, filamentous cyanobacterium, Leptolyngbya sp. strain JSC-1, five different isiA-family genes occur in two gene clusters. During acclimation to Fe limitation, relative transcript levels for more than 600 genes increased more than twofold. Relative transcript levels were ~250 to 300 times higher for the isiA1 gene cluster (isiA1-isiB-isiC), and ~440- to 540-fold for the isiA2-isiA3-isiA4-cpcG2-isiA5 gene cluster after 48 h of iron starvation. Chl-protein complexes were isolated and further purified from cells grown under Fe-replete and Fe-depleted conditions. A single class of particles, trimeric PSI, was identified by image analysis of electron micrographs of negatively stained PSI complexes from Fe-replete cells. However, three major classes of particles were observed for the Chl-protein supercomplexes from cells grown under iron starvation conditions. Based on LC–MS–MS analyses, the five IsiA-family proteins were found in the largest supercomplexes together with core components of the two photosystems; however, IsiA5 was not present in complexes in which only the core subunits of PSI were detected. IsiA5 belongs to the same clade as PcbC proteins in a phylogenetic classification, and it is proposed that IsiA5 is most likely involved in supercomplexes containing PSII dimers. IsiA4, which is a fusion of an IsiA domain and a C-terminal PsaL domain, was found together with IsiA1, IsiA2, and IsiA3 in complexes with monomeric PSI. The data indicate that horizontal gene transfer, gene duplication, and divergence have played important roles in the adaptive evolution of this cyanobacterium to iron starvation conditions.


Cyanobacteria Fe homeostasis Photosystem IsiA Light harvesting Supercomplexes 



The authors thankfully acknowledge the contributions of Patrick Saboe from Department of Chemical Engineering for TEM image collection and Dr. Tracy Nixon from Department of Biochemistry and Molecular Biology for assisting EVAN2 particle refinement analysis, both of The Pennsylvania State University, University Park. We would like to thank Dr. Hao Zhang from PARC LC–MS facility in Washington University in St. Louis for assistance with the mass spectrometric analyses. This work was supported by the National Science Foundation grant MCB-1021725 to D.A.B. This research was also conducted under the auspices of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the DOE, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC 0001035.

Supplementary material

11120_2016_257_MOESM1_ESM.pptx (6.8 mb)
Supplementary material 1 (PPTX 6926 kb)
11120_2016_257_MOESM2_ESM.xlsx (529 kb)
Supplementary material 2 (XLSX 530 kb)


  1. Andrizhiyevskaya EG, Schwabe TM, Germano M, D’Haene S, Kruip J, van Grondelle R, Dekker JP (2002) Spectroscopic properties of PSI-IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942. Biochim Biophys Acta 1556:265–272CrossRefPubMedGoogle Scholar
  2. Barber J, Nield J, Duncan J (2006) Accessory chlorophyll proteins in cyanobacterial photosystem I. In: Golbeck JH (ed) Advances in photosynthesis and respiration, volume 24, photosystem I: the light-driven plastocyanin: ferredoxin oxidoreductase. Springer, Dordrecht, pp 99–117Google Scholar
  3. Behrenfeld MJ, Kolber ZS (1999) Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283:840–843CrossRefPubMedGoogle Scholar
  4. Bes MT, Hernandez JA, Peleato ML, Fillat MF (2001) Cloning, overexpression and interaction of recombinant Fur from the cyanobacterium Anabaena PCC 7119 with isiB and its own promoter. FEMS Microbiol Lett 194:187–192CrossRefPubMedGoogle Scholar
  5. Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745CrossRefPubMedGoogle Scholar
  6. Bibby TS, Mary I, Nield J, Partnesky F, Barber J (2003a) Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature 424:1051–1055CrossRefPubMedGoogle Scholar
  7. Bibby TS, Nield J, Chen M, Larkum AWD, Barber J (2003b) Structure of a photosystem II supercomplex isolated from Prochloron didemni retaining its chlorophyll a/b light-harvesting system. Proc Natl Acad Sci USA 100:9050–9054CrossRefPubMedPubMedCentralGoogle Scholar
  8. Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Miichel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748CrossRefPubMedGoogle Scholar
  9. Boichenko VA, Pinevich AV, Stadnichuk IN (2007) Association of chlorophyll a/b-binding Pcb with photosystem I and II in Prochlorothrix hollandica. Biochim Biophys Acta 1767:801–806CrossRefPubMedGoogle Scholar
  10. Bröcker MJ, Schomburg S, Heinz DW, Jahn D, Schubert W-D, Moser J (2010) Crystal structure of the nitrogenase-like dark operative protochlorophyllide oxidoreductase catalytic complex (ChlN/ChlB)2. J Biol Chem 285:27336–27345CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brown II, Bryant DA, Casamatta D, Thomas-Keprta KL, Sarkisova SA, Shen G, Graham JE, Boyd ES, Peters JW, Garrison DH, McKay DS (2010) Polyphasic characterization of a thermotolerant siderophilic filamentous cyanobacterium that produces intracellular iron deposits. Appl Environ Microbiol 76:6664–6672CrossRefPubMedPubMedCentralGoogle Scholar
  12. Burnap RL, Troyan T, Sherman LA (1993) The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC 7942 (CP43′) is encoded by the isiA gene. Plant Physiol 103:893–902CrossRefPubMedPubMedCentralGoogle Scholar
  13. Castenholz RW (2001) General characteristics of the cyanobacteria. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. Springer, New York, pp 474–487Google Scholar
  14. Chauhan D, Folea IM, Jolley CC, Kouřil R, Lubner CE, Lin S, Kolber D, Wolfe-Simon F, Golbeck JH, Boekema EJ, Fromme P (2010) A novel photosynthetic strategy for adaptation to low-iron aquatic environments. Biochemistry 50:686–692CrossRefGoogle Scholar
  15. Chen M, Bibby TS, Nield J, Larkum AWD, Barber J (2005) Structure of a large photosystem II supercomplex from Acaryochloris marina. FEBS Lett 579:1306–1310CrossRefPubMedGoogle Scholar
  16. Chitnis VP, Chitnis PR (1993) PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336:330–334CrossRefPubMedGoogle Scholar
  17. De Lorenzo V, Wee S, Herrero M, Neilands JB (1987) Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol 169:2624–2630PubMedPubMedCentralGoogle Scholar
  18. Dubbs JM, Bryant DA (1991) Molecular cloning and transcriptional analysis of the cpeBA operon of the cyanobacterium Pseudanabaena sp. PCC 7409. Mol Microbiol 5:3073–3085CrossRefPubMedGoogle Scholar
  19. Dupont CL, Neupane K, Shearer J, Palenik B (2008) Diversity, function and evolution of genes coding for putative Ni-containing superoxide dismutases. Environ Microbiol 10:1831–1843CrossRefPubMedGoogle Scholar
  20. Escolar L, Pérez-Martin J, de Lorenzo V (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181:6223–6229PubMedPubMedCentralGoogle Scholar
  21. Falk S, Samson G, Bruce D, Huner NA, Laudenbach D (1995) Functional analysis of the iron-stress induced CP43′ polypeptide of PS II in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 45:51–60CrossRefPubMedGoogle Scholar
  22. Fromme P, Jordan P, Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31CrossRefPubMedGoogle Scholar
  23. Fujita Y (1996) Protochlorophyllide reduction: a key step in the greening of plants. Plant Cell Physiol 37:411–421CrossRefPubMedGoogle Scholar
  24. Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17:3450–3465CrossRefPubMedGoogle Scholar
  25. Gan F, Shen G, Bryant DA (2014a) Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life 5:4–24CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014b) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317CrossRefPubMedGoogle Scholar
  27. Garczarek L, Hess WR, Holtzendoff J, van der Staay GWM, Partensky F (2000) Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proc Natl Acad Sci USA 97:4098–4101CrossRefPubMedPubMedCentralGoogle Scholar
  28. Garczarek L, van der Staay GWM, Hess WR, Le Gall F, Partensky F (2001) Expression and phylogeny of the multiple antenna genes of the low-light-adapted strain Prochlorococcus marinus SS120. Plant Mol Biol 46:683–693CrossRefPubMedGoogle Scholar
  29. Geider R, La Roche J (1994) The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynth Res 39:275–301CrossRefPubMedGoogle Scholar
  30. Geiss U, Vinnemeier J, Schoor A, Hagemann M (2001) The iron-regulated isiA gene of Fischerella muscicola strain PCC 73103 is linked to a likewise regulated gene encoding a Pcb-like chlorophyll-binding protein. FEMS Microbiol Lett 197:123–129CrossRefPubMedGoogle Scholar
  31. Ghassemian M, Straus NA (1996) Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142:1469–1476CrossRefPubMedGoogle Scholar
  32. Green BR (2003) The evolution of light-harvesting antennas. In: Green BR, Parson WW (eds) Advances in photosynthesis and respiration, volume 13, light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 129–168CrossRefGoogle Scholar
  33. Grossman AR, Schael R, Chiang GG, Collier JL (1994) The responses of cyanobacteria to environmental conditions: light and nutrients. In: Bryant DA (ed) Advances in photosynthesis and respiration, volume 1, the molecular biology of cyanobacteria. Kluwer Academic, Dordrecht, pp 641–675Google Scholar
  34. Guikema JA, Sherman LA (1983) Chlorophyll-protein organization of membranes from the cyanobacterium Anacystis nidulans. Arch Biochem Biophys 220:155–166CrossRefPubMedGoogle Scholar
  35. Hiller RG, Larkum AWD (1985) Chlorophyll-protein complexes of Prochloron (Prochlorophyta). Biochim Biophys Acta 806:107–115CrossRefGoogle Scholar
  36. Ihalainen JA, D’Haene S, Yeremenko N, van Roon H, Arteni AA, Boekema EJ, van Grondelle R, Matthijs HC, Dekker JP (2005) Aggregates of the chlorophyll-binding protein IsiA (CP43′) dissipate energy in cyanobacteria. Biochemistry 44:10846–10853CrossRefPubMedGoogle Scholar
  37. Järvi S, Suorsa M, Paakkarinen V, Aro E-M (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem J 439:207–214CrossRefPubMedGoogle Scholar
  38. Karapetyan N (2008) Protective dissipation of excess absorbed energy by photosynthetic apparatus of cyanobacteria: role of antenna terminal emitters. Photosynth Res 97:195–204CrossRefPubMedGoogle Scholar
  39. Kehoe DM, Gutu A (2006) Responding to color: the regulation of complementary chromatic adaptation. Annu Rev Plant Biol 57:127–150CrossRefPubMedGoogle Scholar
  40. Keren N, Aurora R, Pakrasi HB (2004) Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiol 135:1666–1673CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kojima K, Suzuki-Maenaka T, Kikuchi T, Nakamoto H (2006) Roles of the cyanobacterial isiABC operon in protection from oxidative and heat stresses. Physiol Plant 128:507–519CrossRefGoogle Scholar
  42. Kouřil R, Arteni AA, Lax J, Yeremenko N, D’Haene S, Rögner M, Matthijs HCP, Dekker JP, Boekema EJ (2005a) Structure and functional role of supercomplexes of IsiA and photosystem I in cyanobacterial photosynthesis. FEBS Lett 579:3253–3257CrossRefPubMedGoogle Scholar
  43. Kouřil R, Yeremenko N, D’Haene S, Oostergetel GT, Matthijs HCP, Dekker JP, Boekema EJ (2005b) Supercomplexes of IsiA and photosystem I in a mutant lacking subunit PsaL. Biochim Biophys Acta 1706:262–266CrossRefPubMedGoogle Scholar
  44. La Roche L, van der Staay GWM, Partensky F, Ducret A, Aebersold R, Li R, Golden SS, Hiller RG, Wrech PM, Larkum AWD, Green BR (1996) Independent evolution of prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93:15244–15248CrossRefPubMedPubMedCentralGoogle Scholar
  45. Laudenbach DE, Straus NA (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170:5018–5026PubMedPubMedCentralGoogle Scholar
  46. Laudenbach DE, Reith ME, Straus NA (1988) Isolation, sequence-analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bacteriol 170:258–265PubMedPubMedCentralGoogle Scholar
  47. Leonhardt K, Straus NA (1994) Photosystem II genes isiA, psbDI and psbC in Anabaena sp. PCC 7120: cloning, sequencing and the transcriptional regulation in iron-stressed and iron-repleted cells. Plant Mol Biol 24:63–73CrossRefPubMedGoogle Scholar
  48. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128:82–97CrossRefPubMedGoogle Scholar
  50. Ludwig M, Bryant DA (2011) Transcription profiling of the model cyanobacterium Synechococcus sp. strain 7002 by Next-Gen (SOLiD™) sequencing of cDNA. Front Microbiol 2:41CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ludwig M, Bryant DA (2012) Synechococcus sp. strain PCC 7002 transcriptome: acclimation to temperature, salinity, oxidative stress, and mixotrophic growth conditions. Front Microbiol 3:354PubMedPubMedCentralGoogle Scholar
  52. Ludwig M, Chua TT, Chew CY, Bryant DA (2015) Fur-type transcription repressors and metal homeostasis in the cyanobacterium Synechococcus sp. PCC 7002. Front Microbiol 6:1217CrossRefPubMedPubMedCentralGoogle Scholar
  53. Martin JH, Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331:341–343CrossRefGoogle Scholar
  54. Martin JH, Coale KH, Johnson KS, Fitzwater SE, Gordon RM, Tanner SJ (1994) Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371:123–129CrossRefGoogle Scholar
  55. Matthijs HC, van der Staay G, Mar LR (1994) Prochlorophytes: the ‘other’ cyanobacteria. In: Bryant DA (ed) Advances in photosynthesis and respiration, volume 1, the molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 49–64Google Scholar
  56. Melkozernov AN, Bibby TS, Lin S, Barber J, Blankenship RE (2003) Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed Synechocystis sp. PCC 6803 is efficiently coupled to the photosystem I reaction center core. Biochemistry 42:3893–3903CrossRefPubMedGoogle Scholar
  57. Moser J, Lange C, Krausze J, Rebelein J, Schubert W-D, Ribbe MW, Heinz DW, Jahn D (2013) Structure of ADP-aluminum fluoride-stabilized protochlorophyllide oxidoreductase complex. Proc Natl Acad Sci USA 110:2094–2098CrossRefPubMedPubMedCentralGoogle Scholar
  58. Muraki N, Nomata J, Ebata K, Mizoguchi T, Shiba T, Tamiaki H, Kurisu G, Fujita Y (2010) X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature 465:110–114CrossRefPubMedGoogle Scholar
  59. Murray JW, Duncan J, Barber J (2006) CP43-like chlorophyll binding proteins: structural and evolutionary implication. Trends Plant Sci 11:152–158CrossRefPubMedGoogle Scholar
  60. Nield J, Morris EP, Bibby TS, Barber J (2003) Structural analysis of the photosystem I supercomplex of cyanobacteria induced by iron deficiency. Biochemistry 42:3180–3188CrossRefPubMedGoogle Scholar
  61. Nowack S, Olsen MT, Schaible GA, Becraft ED, Shen G, Klapper I, Bryant DA, Ward DM (2015) The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes in habiting different depths in the Mushroom Spring microbial mat acclimative response to light. Front Microbiol 6:626CrossRefPubMedPubMedCentralGoogle Scholar
  62. Olsen MT, Nowack S, Wood JM, Becraft ED, LaButti K, Lipzen A, Martin J, Schackwitz WS, Rusch DB, Cohan FM, Bryant DA, Ward DM (2015) The molecular dimension of microbial species: 3, comparative genomics of Synechococcus strains with different light responses and in situ diel transcription pattern in the Mushroom Spring microbial mat. Front Microbiol 6:604CrossRefPubMedPubMedCentralGoogle Scholar
  63. ÖQuist G (1971) Changes in pigment composition and photosynthesis induced by iron-deficiency in the blue-green alga Anacystis nidulans. Physiol Plant 25:188–191CrossRefGoogle Scholar
  64. ÖQuist G (1974) Iron deficiency in the blue-green alga Anacystis nidulans: changes in pigmentation and photosynthesis. Physiol Plant 30:30–37CrossRefGoogle Scholar
  65. Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941CrossRefPubMedGoogle Scholar
  66. Ryan-Keogh TJ, Macey AI, Cockshutt AM, Moore CM, Bibby TS (2012) The cyanobacterial chlorophyll-binding-protein IsiA acts to increase the in vivo effective absorption cross-section of PS I under iron limitation. J Phycol 48:145–154CrossRefPubMedGoogle Scholar
  67. Schluchter WM, Shen G, Zhao J, Bryant DA (1996) Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC 7002: a new model for state transitions in cyanobacteria. Photochem Photobiol 64:53–66CrossRefPubMedGoogle Scholar
  68. Shen G, Bryant DA (1995) Characterization of a Synechococcus sp. strain PCC 7002 mutant lacking photosystem I. Protein assembly and energy distribution in the absence of the photosystem I reaction center core complex. Photosynth Res 44:41–53CrossRefPubMedGoogle Scholar
  69. Shen G, Zhao J, Reimer SK, Antonkine ML, Cai Q, Weiland SM, Golbeck JH, Bryant DA (2002) Assembly of photosystem II. Inactivation of the rubA gene encoding a membrane-associated rubredoxin in the cyanobacterium Synechococcus sp. PCC 7002 causes a loss of photosystem I activity. J Biol Chem 277:20343–20354CrossRefPubMedGoogle Scholar
  70. Sherman DM, Sherman LA (1983) Effect of iron deficiency and iron restoration on ultrastructure of Anacystis nidulans. J Bacteriol 156:393–401PubMedPubMedCentralGoogle Scholar
  71. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, 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 KW, Han CS, Rubin EM, Eisen JA, Woyke T, Gugger M, Kerfeld CA (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 110:1053–1058CrossRefPubMedPubMedCentralGoogle Scholar
  72. Straus NA (1994) Iron deprivation: physiology and gene regulation. In: Bryant DA (ed) Advances in photosynthesis and respiration, volume 1, the molecular biology of cyanobacteria. Kluwer Academic, Dordrecht, pp 731–750Google Scholar
  73. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ (2007) EMAN2: an extensible image-processing suite for electron microscopy. J Struct Biol 157:38–46CrossRefPubMedGoogle Scholar
  74. Van der Staay GW, Staehelin LA (1994) Biochemical characterization of protein composition and protein phosphorylation patterns in stacked and unstacked thylakoid membranes of the prochlorophyte Prochlorothrix hollandica. J Biol Chem 269:24834–24844PubMedGoogle Scholar
  75. Van der Staay GW, Yorkova N, Green B (1998) The 38 kDa chlorophyll a/b protein of the prochlorophyte Prochlorothrix hollandica encoded by a divergent pcb gene. Plant Mol Biol 36:709–716CrossRefPubMedGoogle Scholar
  76. Wang Q, Hall CL, Al-Adami MZ, He Q (2010) IsiA is required for the formation of photosystem I supercomplexes and for efficient state transition in Synechocystis PCC 6803. PLoS One 5:e10432CrossRefPubMedPubMedCentralGoogle Scholar
  77. Watanabe M, Semchonok DA, Webber-Birungi MT, Ehira S, Kondo K, Narikawa R, Ohmori M, Boekema EJ, Ikeuchi M (2014) Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc Natl Acad Sci USA 111:2512–2517CrossRefPubMedPubMedCentralGoogle Scholar
  78. Yeremenko N, Kouřil R, Ihalainen JA, D’Haene S, van Oosterwijk N, Andrizhiyevskaya EG (2004) Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43:10308–10313CrossRefPubMedGoogle Scholar
  79. Zhao J, Shen G, Bryant DA (2001) Photosystem stoichiometry and state transitions in mutant of cyanobacterium Synechococcus sp. PCC 7002 lacking phycocyanin. Biochim Biophys Acta 1505:248–257CrossRefPubMedGoogle Scholar
  80. Zhao C, Gan F, Shen G, Bryant DA (2015) RfpA, RfpB, and RfpC are the master control elements of far-red light photoacclimation. Front Microbiol 6:1303PubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular Biology, 4406 Althouse LaboratoryThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Chemistry and BiochemistryMontana State UniversityBozemanUSA

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