Skip to main content
SpringerLink
Log in

Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II.Characterization of phycobiliproteins produced during acclimation to far-red light

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Phycobilisomes (PBS) are antenna complexes that harvest light for photosystem (PS) I and PS II in cyanobacteria and some algae. A process known as far-red light photoacclimation (FaRLiP) occurs when some cyanobacteria are grown in far-red light (FRL). They synthesize chlorophylls d and f and remodel PS I, PS II, and PBS using subunits paralogous to those produced in white light. The FaRLiP strain, Leptolyngbya sp. JSC-1, replaces hemidiscoidal PBS with pentacylindrical cores, which are produced when cells are grown in red or white light, with PBS with bicylindrical cores when cells are grown in FRL. This study shows that the PBS of another FaRLiP strain, Synechococcus sp. PCC 7335, are not remodeled in cells grown in FRL. Instead, cells grown in FRL produce bicylindrical cores that uniquely contain the paralogous allophycocyanin subunits encoded in the FaRLiP cluster, and these bicylindrical cores coexist with red-light-type PBS with tricylindrical cores. The bicylindrical cores have absorption maxima at 650 and 711 nm and a low-temperature fluorescence emission maximum at 730 nm. They contain ApcE2:ApcF:ApcD3:ApcD2:ApcD5:ApcB2 in the approximate ratio 2:2:4:6:12:22, and a structural model is proposed. Time course experiments showed that bicylindrical cores were detectable about 48 h after cells were transferred from RL to FRL and that synthesis of red-light-type PBS continued throughout a 21-day growth period. When considered in comparison with results for other FaRLiP cyanobacteria, the results here show that acclimation responses to FRL can differ considerably among FaRLiP cyanobacteria.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Akutsu S, Fujinuma D, Furukawa H, Watanabe T, Ohnishi-Kameyama M, Ono H, Ohkubo S, Miyashita H, Kobayashi M (2011) Pigment analysis of a chlorophyll f-containing cyanobacterium isolated from Lake Biwa. Photomed Photobiol 33:36–40

    Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Zharmukhamedov SK, Voloshin RA, Korol’kova DV, Tomo T, Shen J-R (2016) Chlorophylls d and f and their role in primary photosynthetic processes of cyanobacteria. Biochemistry 81:201–212

    CAS  PubMed  Google Scholar 

  • Anderson LK, Eiserling FA (1986) Asymmetrical core structure in phycobilisomes of the cyanobacterium Synechocystis 6701. J Mol Biol 191:441–451

    Article  CAS  PubMed  Google Scholar 

  • Behrendt L, Brenjnrod A, Schliep M, Sørensen SJ, Larkum AW, Kühl M (2015) Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium. ISME J 9:2108–2111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berkelman TR, Lagarias JC (1986) Visualization of bilin-linked peptides and proteins in polyacrylamide gels. Anal Biochem 156:194–201

    Article  CAS  PubMed  Google Scholar 

  • 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 76:6664–6672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bryant DA (1981) The photoregulated expression of multiple phycocyanin species. A general mechanism for the control of phycocyanin synthesis in chromatically adapting cyanobacteria. Eur J Biochem 119:425–429

    Article  CAS  PubMed  Google Scholar 

  • Bryant DA (1982) Phycoerythrocyanin and phycoerythrin: properties and occurrence in cyanobacteria. J Gen Microbiol 128:835–844

    CAS  Google Scholar 

  • Bryant DA (1988) Genetic analysis of phycobilisome biosynthesis, assembly, structure, and function in the cyanobacterium Synechococcus sp. PCC 7002. In: Stevens SE Jr, Bryant DA (eds) Light-energy transduction in photosynthesis: higher plant and bacterial models. American Society of Plant Biologists, Rockville, pp 62–90

    Google Scholar 

  • Bryant DA (1991) Cyanobacterial phycobilisomes: progress toward complete structural and functional analysis via molecular genetics. In: Bogorad L, Vasil I (eds) Cell culture and somatic cell genetics of plants, volume 7B, the photosynthetic apparatus: molecular biology and operation. Academic Press, New York, pp 257–300

    Chapter  Google Scholar 

  • Bryant DA (1994) The molecular biology of cyanobacteria, advances in photosynthesis and respiration, vol 1. Kluwer, Dordrecht

    Book  Google Scholar 

  • Bryant DA, Cohen-Bazire G (1981) Effects of chromatic illumination on cyanobacterial phycobilisomes. Evidence for the specific induction of a second pair of phycocyanin subunits in Pseudanabaena 7409 grown in red light. Eur J Biochem 119:415–424

    Article  CAS  PubMed  Google Scholar 

  • Bryant DA, Guglielmi G, Tandeau de Marsac N, Castets AM, Cohen-Bazire G (1979) The structure of cyanobacterial phycobilisomes: a model. Arch Microbiol 123:113–127

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M (2014) Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Annu Rev Biochem 83:317–340

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Schliep M, Willows RD, Cai Z-L, Neilan BA, Scheer H (2010) A red-shifted chlorophyll. Science 329:1318–1319

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Li Y, Birch D, Willows RD (2012) A cyanobacterium that contains chlorophyll f—a red absorbing photopigment. FEBS Lett 586:3249–3254

    Article  CAS  PubMed  Google Scholar 

  • Dong C, Tang A, Zhao J, Mullineaux CW, Shen G, Bryant DA (2009) 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

    Article  CAS  PubMed  Google Scholar 

  • Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17:3450–3465

    Article  CAS  PubMed  Google Scholar 

  • Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Gindt YM, Zhou J, Bryant DA, Sauer K (1994) Spectroscopic studies of phycobilisomes subcore preparations lacking key core chromophores: assignments of excited state energies to the Lcm, and β18, and αAP-B chromophores. Biochim Biophys Acta 1186:153–162

    Article  CAS  PubMed  Google Scholar 

  • Gingrich JC, Lundell DJ, Glazer AN (1983) Core substructure in cyanobacterial phycobilisomes. J Cell Biochem 22:1–14

    Article  CAS  PubMed  Google Scholar 

  • Glazer AN (1984) Phycobilisome. A macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 768:29–51

    Article  CAS  Google Scholar 

  • Glazer AN (1985) Light harvesting by phycobilisomes. Ann Rev Biophys Biophys Chem 14:47–77

    Article  CAS  Google Scholar 

  • Glazer AN (1989) Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264:1–4

    CAS  PubMed  Google Scholar 

  • Glazer AN, Bryant DA (1975) Allophycocyanin B (λ max 671, 618 nm): a new cyanobacterial phycobiliprotein. Arch Microbiol 104:15–22

    Article  CAS  PubMed  Google Scholar 

  • Glazer AN, Lundell DJ, Yamanka G, Williams RC (1983) The structure of a “simple” phycobilisome. Ann Microbiol 134B:159–180

    CAS  Google Scholar 

  • Gómez-Lojero C, Pérez-Gómez B, Shen G, Schluchter WM, Bryant DA (2003) Interaction of ferredoxin:NADP+ oxidoreductase with phycobilisomes and phycobilisome substructures of the cyanobacterium Synechococcus sp. strain PCC 7002. Biochemistry 42:13800–13811

    Article  PubMed  Google Scholar 

  • Grotjohann I, Fromme P (2005) Structure of cyanobacterial photosystem I. Photosynth Res 85:51–72

    Article  CAS  PubMed  Google Scholar 

  • Ho M-Y, Gan F, Shen G, Zhao C, Bryant DA (2016a) Far-Red Light Photoacclimation (FaRLiP) in synechococcus sp. PCC 7335: I. regulation of FaRLiP gene expression. Photosynth Res. doi:10.1007/s11120-016-0309-z

    Google Scholar 

  • Ho M-Y, Shen G, Canniffe DP, Zhao C, Bryant DA (2016b) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of Photosystem II. Science 353:aaf9178

    Article  PubMed  Google Scholar 

  • Kühl M, Chen M, Ralph PJ, Schreiber U, Larkum AWD (2005) Ecology: a niche for cyanobacteria containing chlorophyll d. Nature 433:820

    Article  PubMed  Google Scholar 

  • Li Y, Lin Y, Loughlin PC, Chen M (2014) Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris—a filamentous cyanobacterium containing chlorophyll f. Front Plant Sci 5:67

    PubMed  PubMed Central  Google Scholar 

  • Li Y, Lin Y, Garvey CJ, Birch D, Corkery RW, Loughlin PC, Scheer H, Willows RD, Chen M (2016) Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim Biophys Acta 1857:107–114

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342:1104–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lundell DJ, Glazer AN (1983) Molecular architecture of a light-harvesting antenna. Quaternary interactions in the Synechococcus 6301 phycobilisome core as revealed by partial tryptic digestion and circular dichroism studies. J Biol Chem 258:8708–8713

    CAS  PubMed  Google Scholar 

  • Maxson P, Sauer K, Bryant DA, Glazer AN (1989) Spectroscopic studies of cyanobacterial phycobilisomes lacking core polypeptides. Biochim Biophys Acta 974:66–73

    Article  Google Scholar 

  • Miao D, Ding W-L, Zhao B-Q, Lu L, Xu Q-Z, Scheer H, Zhao K-H (2016) 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. PCC7335. Biochim Biophys Acta 1857:688–694

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Miyashita H, Ohkubo S, Komatsu H, Sorimachi Y, Fukayama D, Fujinuma D, Akutsu S, Kabayashi M (2014) Discovery of chlorophyll d in Acaryochloris marina and chlorophyll f in a unicellular cyanobacterium, strain KC1, isolated from Lake Biwa. J Phys Chem Biophys 4:149

    Article  Google Scholar 

  • Raps S (1990) Differentiation between phycobiliprotein and colorless linker polypeptides by fluorescence in the presence of ZnSO4. Plant Physiol 92:358–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rippka R (1988) Isolation and purification of cyanobacteria. Meth Enzymol 167:3–27

    Article  CAS  PubMed  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111:1–61

    Article  Google Scholar 

  • Schluchter WM, Bryant DA (1992) Molecular characterization of ferredoxin-NADP+ oxidoreductase in cyanobacteria: cloning and sequence of the petH gene of Synechococcus sp. PCC 7002 and studies on the gene product. Biochemistry 31:3092–3102

    Article  CAS  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  Google Scholar 

  • Shen J-R (2015) The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol 66:23–48

    Article  CAS  PubMed  Google Scholar 

  • 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 44:41–53

    Article  CAS  PubMed  Google Scholar 

  • Sidler WA (1994) Phycobilisome and phycobiliprotein structure. In: Bryant DA (ed) Advances in photosynthesis and respiration, volume 1, the molecular biology of cyanobacteria. Kluwer Academic, Dordrecht, pp 139–216

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Williams RC, Gingrich JC, Glazer AN (1980) Cyanobacterial phycobilisomes. Particles from Synechocystis 6701 and two pigment mutants. J Cell Biol 85:558–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhou J, Bryant DA (1992) Energy transfer processes in phycobilisomes as deduced from analyses of mutants of Synechococcus sp. PCC 7002. In: Murata N (ed) Research in photosynthesis, vol 1. Kluwer Academic Publishers, Dordrecht, pp 25–32

    Google Scholar 

  • Zhao C, Gan F, Shen G, Bryant DA (2015) RfpA, RfpB, and RfpC are the master control elements of far-red light photoacclimation (FaRLiP). Front Microbiol 6:1303

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by Grant MCB-1021725 from the National Science Foundation 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.

Author information

Authors and Affiliations

  1. 403C Althouse Laboratory, Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA, 16802, USA

    Ming-Yang Ho, Fei Gan, Gaozhong Shen & Donald A. Bryant

  2. Intercollege Graduate Degree Program in Plant Biology, The Pennsylvania State University, University Park, PA, 16802, USA

    Ming-Yang Ho & Donald A. Bryant

  3. Department of Chemistry and Biochemistry, Montana State University, Bozeman, MT, 59717, USA

    Donald A. Bryant

Authors
  1. Ming-Yang Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gaozhong Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Donald A. Bryant
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Donald A. Bryant.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ho, MY., Gan, F., Shen, G. et al. 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). https://doi.org/10.1007/s11120-016-0303-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-016-0303-5

Keywords

Search

Navigation