Skip to main content
SpringerLink
Log in

Fluorescence recovery after photobleaching: analyses of cyanobacterial phycobilisomes reveal intrinsic fluorescence recovery

  • Research Paper
  • Published:
Marine Life Science & Technology Aims and scope Submit manuscript

A Correction to this article was published on 25 June 2021

This article has been updated

Abstract

Fluorescence recovery after photobleaching (FRAP) has been used to study the dynamics of the cyanobacterial photosynthesis apparatus since 1997. Fluorescence recovery of cyanobacteria during FRAP was conventionally interpreted as a result of phycobilisome (PBS) diffusion on the surface of the thylakoid membrane. The mechanism of state transition in cyanobacteria has been widely attributed to PBS diffusion. However, in red algae, another PBS-containing group, the intrinsic photoprocess was found to contribute greatly to the fluorescence recovery of PBS, which raises questions concerning the role of FRAP in red algal PBS. Therefore, it is important to re-evaluate the nature of PBS fluorescence recovery in cyanobacteria. In the present study, four cyanobacterial strains with different phenotypes and PBS compositions were used to investigate their FRAP characteristics. Fluorescence recovery of PBS was observed in wholly photobleached cells in all four cyanobacterial strains, in which the contribution of PBS diffusion to the fluorescence recovery was not possible. Moreover, the fluorescence recovered in isolated PBSs and PBS-thylakoid membranes after photobleaching further demonstrated the intrinsic photoprocess nature of fluorescence recovery. These findings suggest that the intrinsic photoprocess contributed to the fluorescence recovery following photobleaching when measured by the FRAP method.

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

Similar content being viewed by others

Change history

References

  • Adir N, Bar-Zvi S, Harris D (2020) The amazing phycobilisome. Biochim Biophys Acta 1861:148047

    Article  CAS  Google Scholar 

  • Allen MM (1968) Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4:1–4

    Article  CAS  Google Scholar 

  • Arteni AA, Liu LN, Aartsma TJ, Zhang YZ, Zhou BC, Boekema EJ (2008) Structure and organization of phycobilisomes on membranes of the red alga Porphyridium cruentum. Photosynth Res 95:169–174

    Article  CAS  Google Scholar 

  • Aspinwall CL, Sarcina M, Mullineaux CW (2004) Phycobilisome mobility in the cyanobacterium Synechococcus sp. PCC7942 is influenced by the trimerisation of photosystem I. Photosynth Res 79:179

    Article  CAS  Google Scholar 

  • Glazer AN (1988) Phycobilisomes. In: Packer L, Glazer AN (eds) Methods in enzymology. Academic Press, San Diego, pp 304–312

    Google Scholar 

  • Goedheer JC (1960) Spectral and redox properties of bacteriochlorophyll in its natural state. Biochim Biophys Acta 38:389–399

    Article  CAS  Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749

    Article  CAS  Google Scholar 

  • Henderson JN, Ai H-W, Campbell RE, Remington SJ (2007) Structural basis for reversible photobleaching of a green fluorescent protein homologue. Proc Natl Acad Sci USA 104:6672–6677

    Article  CAS  Google Scholar 

  • Joshua S, Mullineaux CW (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135:2112–2119

    Article  CAS  Google Scholar 

  • Kaňa R, Kotabová E, Lukeš M, Papáček Š, Matonoha C, Liu L-N, Prášil O, Mullineaux CW (2014) Phycobilisome mobility and its role in the regulation of light harvesting in red algae. Plant Physiol 165:1618–1631

    Article  Google Scholar 

  • Li W, Su H-N, Pu Y, Chen J, Liu L-N, Liu Q, Qin S (2019) Phycobiliproteins: molecular structure, production, applications, and prospects. Biotechnol Adv 37:340–353

    Article  CAS  Google Scholar 

  • Lippincott-Schwartz J, Snapp EL, Phair RD (2018) The development and enhancement of FRAP as a key tool for investigating protein dynamics. Biophys J 115:1146–1155

    Article  CAS  Google Scholar 

  • Liu LN, Chen XL, Zhang YZ, Zhou BC (2005) Characterization, structure and function of linker polypeptides in phycobilisomes of cyanobacteria and red algae: an overview. Biochim Biophys Acta 1708:133–142

    Article  CAS  Google Scholar 

  • Liu L-N, Aartsma TJ, Thomas J-C, Lamers GEM, Zhou B-C, Zhang Y-Z (2008) Watching the native supramolecular architecture of photosynthetic membrane in red algae: topography of phycobilisomes and their crowding, diverse distribution patterns. J Biol Chem 283:34946–34953

    Article  CAS  Google Scholar 

  • Liu LN, Aartsma TJ, Thomas JC, Zhou BC, Zhang YZ (2009) FRAP analysis on red alga reveals the fluorescence recovery is ascribed to intrinsic photoprocesses of phycobilisomes than large-scale diffusion. PLoS ONE 4:e5295

    Article  Google Scholar 

  • Livingston R, Stockman D (1962) A further study of the phototropy of chlorophyll in solution. J Phys Chem 66:2533–2537

    Article  CAS  Google Scholar 

  • MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334

    Article  CAS  Google Scholar 

  • McConnell MD, Koop R, Vasil’ev S, Bruce D (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria: a structure-based model for the light state transition. Plant Physiol 130:1201–1212

    Article  CAS  Google Scholar 

  • Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393

    Article  CAS  Google Scholar 

  • Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390:421–424

    Article  CAS  Google Scholar 

  • Mustardy L, Cunningham FX Jr, Gantt E (1992) Photosynthetic membrane topography: quantitative in situ localization of photosystems I and II. Proc Natl Acad Sci USA 89:10021–10025

    Article  CAS  Google Scholar 

  • Ohki K, Fujita Y (1979) In vivo transformation of phycobiliproteins during photobleaching of Tolypothrix tenuis to forms active in photoreversible absorption changes. Plant Cell Physiol 20:1341–1347

    Article  CAS  Google Scholar 

  • Rayan G, Guet J-E, Taulier N, Pincet F, Urbach W (2010) Recent applications of fluorescence recovery after photobleaching (FRAP) to membrane bio-macromolecules. Sensors (Basel) 10:5927–5948

    Article  Google Scholar 

  • Samsonoff WA, MacColl R (2001) Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat. Arch Microbiol 176:400–405

    Article  CAS  Google Scholar 

  • Sarcina M, Mullineaux CW (2000) Effects of tubulin assembly inhibitors on cell division in prokaryotes in vivo. FEMS Microbiol Lett 191:25–29

    Article  CAS  Google Scholar 

  • Sarcina M, Tobin MJ, Mullineaux CW (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942: effects of phycobilisome size, temperature, and membrane lipid composition. J Biol Chem 276:46830–46834

    Article  CAS  Google Scholar 

  • Siebzehnrubl S, Fischer R, Kufer W, Scheer H (1989) Photochemistry of phycobiliproteins: reciprocity of reversible photochemistry and aggregation in phycoerythrocyanin from Mastigocladus laminosus. Photochem Photobiol 49:753–761

    Article  CAS  Google Scholar 

  • Verkman AS (2002) Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem Sci 27:27–33

    Article  CAS  Google Scholar 

  • Watanabe M, Ikeuchi M (2013) Phycobilisome: architecture of a light-harvesting supercomplex. Photosynth Res 116:265–276

    Article  CAS  Google Scholar 

  • Yang S, Su Z, Li H, Feng J, Xie J, Xia A, Gong Y, Zhao J (2007) Demonstration of phycobilisome mobility by the time- and space-correlated fluorescence imaging of a cyanobacterial cell. Biochim Biophys Acta 1767:15–21

    Article  CAS  Google Scholar 

  • Zhao K-H, Scheer H (1995) Type I and type II reversible photochemistry of phycoerythrocyanin α-subunit from Mastigocladus laminosus both involve Z, E isomerization of phycoviolobilin chromophore and are controlled by sulfhydryls in apoprotein. Biochim Biophys Acta 1228:244–253

    Article  Google Scholar 

  • Zhao K-H, Haessner R, Cmiel E, Scheer H (1995) Type I reversible photochemistry of phycoerythrocyanin involves Z/E-isomerization of α-84 phycoviolobilin chromophore. Biochim Biophys Acta 1228:235–243

    Article  Google Scholar 

  • Zhao L-S, Su H-N, Li K, Xie B-B, Liu L-N, Zhang X-Y, Chen X-L, Huang F, Zhou B-C, Zhang Y-Z (2016) Supramolecular architecture of photosynthetic membrane in red algae in response to nitrogen starvation. Biochim Biophys Acta 1857:1751–1758

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Haiyan Yu and Xiaomin Zhao from Core Facilities for Life and Environmental Sciences of Shandong University for technical help. This work was supported by the National Natural Science Foundation of China (no. 31900023), National Key R&D Program of China (no. 2018YFC1406701), Program of Shandong Taishan Scholars (no. tspd20181203), Natural Science Foundation of Shandong (no. ZR2017LD013), AoShan Talents Cultivation Program (no. 2017ASTCP-OS14), State Key Laboratory of Microbial Technology Open Projects Fund (no. M2019-07), and Young Scholars Program of Shandong University (no. 2017WLJH22).

Author information

Authors and Affiliations

  1. State Key Laboratory of Microbial Technology, and Marine Biotechnology Research Center, Shandong University, Qingdao, 266237, China

    Nan Zhang, Kang Li, Bin-Bin Xie, Xiu-Lan Chen, Bai-Cheng Zhou, Hai-Nan Su & Yu-Zhong Zhang

  2. College of Marine Life Sciences, Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, 266003, China

    Yu-Zhong Zhang

  3. Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Kang Li & Yu-Zhong Zhang

  4. College of Bioengineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, 250353, China

    Nan Zhang

Authors
  1. Nan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin-Bin Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiu-Lan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bai-Cheng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hai-Nan Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yu-Zhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YZZ and HNS conceived this work; NZ, HNS, and KL performed experiments; HNS, BBX, XLC, and BCZ analyzed data; NZ and HNS prepared the figures and wrote the manuscript. All authors approved the final manuscript.

Corresponding authors

Correspondence to Hai-Nan Su or Yu-Zhong Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Animal and human rights statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Edited by Jiamei Li.

The original online version of this article was revised: A funding number was incorrect in the Acknowledgements section.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, N., Li, K., Xie, BB. et al. Fluorescence recovery after photobleaching: analyses of cyanobacterial phycobilisomes reveal intrinsic fluorescence recovery. Mar Life Sci Technol 3, 427–433 (2021). https://doi.org/10.1007/s42995-021-00104-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42995-021-00104-z

Keywords

Search

Navigation