Skip to main content
SpringerLink
Log in

Comparative proteomic analysis of Nostoc flagelliforme reveals the difference in adaptive mechanism in response to different ultraviolet-B radiation treatments

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Nostoc flagelliforme is a pioneer organism in the desert and highly resistant to ultraviolet B (UV-B) radiation, while the involved adaptive mechanism has not been fully explored yet. To elucidate the responsive mechanism, two doses of UV-B radiation (low: 1 W/m2 and high: 5 W/m2) were irradiated for 6 h and 48 h, respectively, and their effects on global metabolism in N. flagelliforme were comprehensively investigated. In this study, we used iTRAQ-based proteomic approach to explore the proteomes of N. flagelliforme, and 151, 172, 124 and 148 differentially expressed proteins were identified under low and high UV-B doses for 6 h and 48 h, respectively. Functional classification analysis showed these proteins were mainly involved in photosynthesis, amino acid metabolism, antioxidant activity and carbohydrate metabolism. Further analysis revealed that UV-B imposed restrictions on primary metabolism including photosynthesis, Calvin cycle, and amino acid metabolism, and cells started defense mechanism through repair of DNA and protein damage, increasing antioxidant activity, and accumulating extracellular polysaccharides to minimize the damage. Moreover, high UV-B dose imposed more severe restrictions and activated stronger defense mechanism compared with low dose. The results would improve the understanding of molecular mechanisms of UV-B-stress adaption in N. flagelliforme.

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

References

  1. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T (2006) The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci USA 103(14):5442–5447

    Article  CAS  Google Scholar 

  2. Rastogi RP, Sinha RP, Moh SH, Lee TH, Kottuparambil S, Kim YJ, Rhee JS, Choi EM, Brown MT, Häder DP, Han T (2014) Ultraviolet radiation and cyanobacteria. J Photochem Photobiol B 141:154–169

    Article  CAS  Google Scholar 

  3. Gao K, Yu H, Brown MT (2007) Solar PAR and UV radiation affects the physiology and morphology of the cyanobacterium Anabaena sp. PCC 7120. J Photochem Photobiol B 89:117–124

    Article  CAS  Google Scholar 

  4. Zhang XX, Tang XX, Zhou B, Hu SX, Wang Y (2015) Effect of enhanced UV-B radiation on photosynthetic characteristics of marine microalgae Dunaliella salina (Chlorophyta, Chlorophyceae). J Exp Mar Biol Ecol 469:27–35

    Article  CAS  Google Scholar 

  5. Li ZK, Dai GZ, Juneau P, Qiu BS, Posewitz M (2017) Different physiological responses of cyanobacteria to ultraviolet-B radiation under iron-replete and iron-deficient conditions: implications for underestimating the negative effects of UV-B radiation. J Phycol 53:425–536

    Article  CAS  Google Scholar 

  6. Gao KS, Zou DG (2001) Photosynthetic bicarbonate utilization by a terrestrial cyanobacterium, Nostoc flagelliforme (Cyanophyceae). J Appl Phycol 37:768–771

    Article  CAS  Google Scholar 

  7. Gao KS (1998) Chinese studies on the edible blue-green alga, Nostoc flagelliforme: a review. J Appl Phycol 10:37–49

    Article  Google Scholar 

  8. Ferroni L, Klisch M, Pancaldi S, Häder DP (2010) Complementary UV-absorption of mycosporine-like amino acids and scytonemin is responsible for the UV-insensitivity of photosynthesis in Nostoc flagelliforme. Mar Drugs 8:106–121

    Article  CAS  Google Scholar 

  9. Yu HF, Liu R (2013) Effect of UV-B radiation on the synthesis of UV-absorbing compounds in a terrestrial cyanobacterium Nostoc flagelliforme. J Appl Phycol 25:1441–1446

    Article  CAS  Google Scholar 

  10. Cheng X, Deng G, Su Y, Liu JJ, Yang Y, Du GH, Chen ZY, Liu FH (2016) Protein mechanisms in response to NaCl-stress of salt-tolerant and salt-sensitive industrial hemp based on iTRAQ technology. Ind Crop Prod 83:444–452

    Article  CAS  Google Scholar 

  11. Xia CG, Zhang DJ, Ma CN, Zhou J, He S, Su XR (2016) Characterization and comparison of proteomes of albino sea cucumber Apostichopus japonicus (Selenka) by iTRAQ analysis. Fish Shellfish Immunol 51:229–239

    Article  CAS  Google Scholar 

  12. Gao ZQ, Miao XX, Zhang XW, Wu GW, Guo YY, Wang MM, Li B, Li XB, Gao YH, Hu S, Sun JT, Cui JL, Meng CX, Li Y (2016) Comparative fatty acid transcriptomic test and iTRAQ-based proteomic analysis in Haematococcus pluvialis upon salicylic acid (SA) and jasmonic acid (JA) inductions. Algal Res 17:277–284

    Article  Google Scholar 

  13. Liu XJ, Jiang Y, Chen F (2005) Fatty acid profile of the edible filamentous cyanobacterium Nostoc flagelliforme at different temperatures and developmental stages in liquid suspension culture. Process Biochem 40:371–377

    Article  CAS  Google Scholar 

  14. Wang FX, Song QR (2007) Monitoring on the intensity of UVB radiation on different underlying ground in Yinchuan. Modern Prev Med 34:4207–4208

    Google Scholar 

  15. Han PP, Jia SR, Sun Y, Tan ZL, Zhong C, Dai YJ, Tan N, Shen SG (2014) Metabolomic approach to optimizing and evaluating antibiotic treatment in the axenic culture of cyanobacterium Nostoc flagelliforme. World J Microbiol Biotechnol 30:2407–2418

    Article  CAS  Google Scholar 

  16. Han PP, Guo RJ, Shen SG, Yan RR, Wu YK, Yao SY, Wang HY, Jia SR (2018) Proteomic profiling of Nostoc flagelliforme reveals the common mechanism in promoting polysaccharide production by different light qualities. Biochem Eng J 132:68–78

    Article  CAS  Google Scholar 

  17. Fisher T, Minnaard J, Dubinsky Z (1996) Photoacclimation in the marine alga Nannochloropsis sp. (Eustigmatophyte): a kinetic study. J Plankton Res 18(10):1797–1818

    Article  Google Scholar 

  18. Ahmad IZ, Sundaram S, Tripathi A, Soumya KK (2009) Isolation Of PS II nanoparticles and oxygen evolution studies in Synechococcus spp. PCC 7942 under heavy metal stress. AIP Conf Proc 1147(1):309–315

    Article  CAS  Google Scholar 

  19. Shen SG, Jia SR, Yan RR, Wu YK, Wang HY, Lin YH, Zhao DX, Tan ZL, Lv HX, Han PP (2018) The physiological responses of terrestrial cyanobacterium Nostoc flagelliforme to different intensities of ultraviolet-B radiation. RSC Adv 8:21065–21074

    Article  CAS  Google Scholar 

  20. Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252:361–376

    Article  Google Scholar 

  21. Turcsányi E, Vass I (2000) Inhibition of photosynthetic electron transport by UV-A radiation targets the photosystem II complex. Photochem Photobiol 72:513–520

    Article  Google Scholar 

  22. Shinopoulos KE, Brudvig GW (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. BBA 1817(1):66–75

    CAS  PubMed  Google Scholar 

  23. Frago S, Lans I, Navarro JA, Hervás M, Edmondson DE, De la Rosa MA, Gómez-Moreno C, Mayhew SG, Medina M (2010) Dual role of FMN in flavodoxin function: electron transfer cofactor and modulation of the protein-protein interaction surface. BBA 1797:262–271

    CAS  PubMed  Google Scholar 

  24. Hope AB (2000) Electron transfers amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms. BBA 1456:5–26

    CAS  PubMed  Google Scholar 

  25. Shrivastava AK, Chatterjee A, Yadav S, Singh PK, Singh S, Rai LC (2015) UV-B stress induced metabolic rearrangements explored with comparative proteomics in three Anabaena species. J Proteomics 127:122–133

    Article  CAS  Google Scholar 

  26. Kilian O, Steunou AS, Grossman AR, Bhaya DA (2008) A novel two domain-fusion protein in cyanobacteria with similarity to the CAB/ELIP/HLIP superfamily: evolutionary implications and regulation. Mol Plant 1:155–166

    Article  CAS  Google Scholar 

  27. Saradhi PP, Aliaarora S, Prasad KVSK (1995) Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochem Biophys Res Commun 209:1–5

    Article  CAS  Google Scholar 

  28. O‘Brien PA, Houghton JA (1982) UV-induced DNA degradation in the cyanobacterium Synechocystis PCC 6308. Photochem Photobiol 36:417–422

    Article  Google Scholar 

  29. Torok Z, Goloubinoff P, Horváth I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH, VÍgh L (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 98:3098–3103

    Article  CAS  Google Scholar 

  30. Verschooten L, Claerhout S, Laethemii AV, Agostinis P, Garmyn M (2006) New strategies of photoprotection. Photochem Photobiol 82:1016–1023

    Article  CAS  Google Scholar 

  31. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem-Biol Interact 160:1–40

    Article  CAS  Google Scholar 

  32. Vaara T (1982) The outermost surface structures in chroococcacean cyanobacteria. Can J Microbiol 28:929–941

    Article  Google Scholar 

  33. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Sinha RP, Singh N, Kumar A, Kumar HD, Häder M, Häder DP (1996) Effects of UV irradiation on certain physiological and biochemical processes in cyanobacteria. J Photochem Photobiol B 32:107–113

    Article  CAS  Google Scholar 

  35. Ehling-Schulz M, Schulz S, Wait R, Görg A, Scherer S (2002) The UV-B stimulon of the terrestrial cyanobacterium Nostoc commune comprises early shock proteins and late acclimation proteins. Mol Microbiol 46(3):827–843

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are very grateful for the financial support from the National Natural Science Foundation of China (Grant No. 31671842) and Changjiang Scholars and Innovative Research Team in University (Grant No. IRT1166).

Author information

Authors and Affiliations

  1. Key Laboratory of Industrial Fermentation Microbiology, Ministry of Education, State Key Laboratory of Food Nutrition and Safety, College of Biotechnology, Tianjin University of Science and Technology, Tianjin, 300457, People’s Republic of China

    Shi-gang Shen, Rong-jun Guo, Rong-rong Yan, Yi-kai Wu, Dong-xue Zhao, Ya-hui Lin, He-xin Lv, Shi-ru Jia & Pei-pei Han

Authors
  1. Shi-gang Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rong-jun Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rong-rong Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yi-kai Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dong-xue Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ya-hui Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. He-xin Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shi-ru Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pei-pei Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shi-ru Jia or Pei-pei Han.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1 (DOCX 42 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shen, Sg., Guo, Rj., Yan, Rr. et al. Comparative proteomic analysis of Nostoc flagelliforme reveals the difference in adaptive mechanism in response to different ultraviolet-B radiation treatments. Mol Biol Rep 45, 1995–2006 (2018). https://doi.org/10.1007/s11033-018-4355-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-018-4355-9

Keywords

Search

Navigation