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Magnetic Fields as Inducers of Phycobiliprotein Production by Synechococcus elongatus PCC 7942

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Abstract

This study aimed to analyze the effect of magnetic field (MF) application on the metabolism of Synechococcus elongatus PCC 7942. Concentrations of biomass, carbohydrate, protein, lipid, and photosynthetic pigments (chlorophyll-a, C-phycocyanin, allophycocyanin and phycoerythrin) were determined. In cultures with MF application (30 mT for 24 h d−1), there were increases of 47.5% in total protein content, 87.4% in C-phycocyanin, and 332.8% in allophycocyanin contents, by comparison with the control. Allophycocyanin is the most affected pigment by MF application. Therefore, its biosynthetic route was investigated, and four genes related to its synthesis were found. However, the analysis of the gene expression showed no statistical differences from the control culture, which suggests that induction of such genes may occur soon after MF application with consequent stabilization over time. MF application may be a cost-effective alternative to increase production of compounds of commercial interest by cyanobacteria.

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References

  1. Bezerra PQM, Moraes L, Cardoso LG, Druzian JI, Morais MG, Nunes IL, Costa JAV (2020) Spirulina sp. LEB 18 cultivation in seawater and reduced nutrients: bioprocess strategy for increasing carbohydrates in biomass. Bioresour Technol 316:123883

    CAS  PubMed  Google Scholar 

  2. Satyanarayana KG, Mariano AB, Vargas JVC (2011) A review on microalgae, a versatile source for sustainable energy and materials. Int J Energy Res 35:291–311

    Google Scholar 

  3. Ducat DC, Sachdeva G, Silver PA (2011) Rewiring hydrogenase-dependent redox circuits in cyanobacteria. Proc Natl Acad Sci USA 108(10):3941–3946

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Ludwig M, Bryant DA (2011) Transcription profiling of the model cyanobacterium Synechococcus sp. strain PCC 7002 by next-gen (SOLiDTM) sequencing of cDNA. Front. Microbiol 2(41):1–23

    Google Scholar 

  5. Deamici KM, Santos LO, Costa JAV (2021) Magnetic field as promoter of growth in outdoor and indoor assays of Chlorella fusca. Bioprocess Biosyst Eng 44:1453–1460

    CAS  PubMed  Google Scholar 

  6. Costa SS, Peres BP, Machado BR, Costa JAV, Santos LO (2020) Increased lipid synthesis in the culture of Chlorella homosphaera with magnetic fields application. Bioresour Technol 315:123880

    CAS  PubMed  Google Scholar 

  7. Silva PGP, Prescendo Júnior D, Sala L, Burkert JFM, Santos LO (2020) Magnetic field as a trigger of carotenoid production by Phaffia rhodozyma. Process Biochem 98:131–138

    Google Scholar 

  8. Repacholi MH, Greenebaum B (1999) Interaction of static and extremely low frequency electric and magnetic fields with living systems: health effects and research needs. Bioelectromagnetics 20:133–160

    CAS  PubMed  Google Scholar 

  9. Ruiz-Dominguez MC, Jáuregui M, MedinaJaime EC, Cerezal Mezquita P (2019) Rapid green extractions of C-Phycocyanin from Arthrospira maxima for functional applications. Appl Sci 9:1–13

    Google Scholar 

  10. Ilter I, Akyıl S, Demirel Z, Koç M, Conk-Dalay M, Kaymak-Ertekin F (2018) Optimization of phycocyanin extraction from Spirulina platensis using different techniques. J Food Compos Anal 70:78–88

    CAS  Google Scholar 

  11. Khatoon H, Kok Leong L, Abdu Rahman N, Mian S, Begum H, Banerjee S, Endut A (2018) Effects of different light source and media on growth and production of phycobiliprotein from freshwater cyanobacteria. Bioresour Technol 249:652–658

    CAS  PubMed  Google Scholar 

  12. Rippka R, Deruelles J, Waterbury JW, Herdman M, Stanier RG (1979) Genetic assignments, strain histories and properties of pure cultures of Cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  13. Hendry JI, Prasannan CB, Joshi A, Dasgupta S, Wangikar PP (2016) Metabolic model of Synechococcus sp. PCC 7002: prediction of flux distribution and network modification for enhanced biofuel production. Bioresour Technol 213:190–197

    CAS  PubMed  Google Scholar 

  14. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    CAS  Google Scholar 

  15. Lowry OH, Rosebrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  16. Marsh JB, Weinstein DB (1966) Simple charring method for determination of lipids. J Lipid Res 7:574–576

    CAS  PubMed  Google Scholar 

  17. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    CAS  Google Scholar 

  18. Ores JC, Amarante MCA, Kalil SJ (2016) Co-production of carbonic anhydrase and phycobiliproteins by Spirulina sp. and Synechococcus nidulans. Bioresour Technol 219:219–227

    CAS  PubMed  Google Scholar 

  19. Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green-alga. J Cell Biol 58:419–435

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Bailey JE, Ollis DF (1986) Biochemical Engineering Fundamentals. 2ª ed. McGrawHill, Singapore, pp 397–398.

  21. Pinto F, Pacheco CC, Ferreira D, Moradas-Ferreira P, Tamagnini P (2012) Selection of suitable reference genes for RT-qPCR analyses in cyanobacteria. PLoS ONE 7:e34983

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  23. Bauer LM, Costa JAV, Da Rosa APC, Santos LO (2017) Growth stimulation and synthesis of lipids, pigments and antioxidants with magnetic fields in Chlorella kessleri cultivations. Bioresour Technol 244:1425–1432

    CAS  PubMed  Google Scholar 

  24. Deamici KM, Cardias BB, Costa JAV, Santos LO (2016) Static magnetic fields in culture of Chlorella fusca: Bioeffects on growth and biomass composition. Process Biochem 51:912–916

    CAS  Google Scholar 

  25. Ducret A, Müller SA, Goldie KN, Hefti A, Sidler WA, Zuber H, Engel A (1998) Reconstitution, characterization and mass analysis of the pentacylindrical allophycocyanin core complex from the cyanobacterium Anabaena sp. PCC 7120. J Mol Biol 278:369–388

    CAS  PubMed  Google Scholar 

  26. Sun L, Wang S (2003) Allophycocyanin complexes from the phycobilisome of a thermophilic blue-green alga Myxosarcina concinna Printz. J Photochem Photobiol B 72:45–53

    CAS  PubMed  Google Scholar 

  27. Deamici KM, Santos LO, Costa JAV (2019) Use of static magnetic fields to increase CO2 biofixation by the microalga Chlorella fusca. Bioresour Technol 276:103–109

    CAS  PubMed  Google Scholar 

  28. Wang HY, Zeng XB, Gui SY, Li ZT (2008) Effects of magnetic field on the antioxidant defense system of recirculation-cultured Chlorella vulgaris. Bioelectromagnetics 29:39–46

    PubMed  Google Scholar 

  29. Gao W, Liu Y, Zhou J, Pan H (2005) Effects of a strong static magnetic field on bacterium Shewanella oneidensis: an assessment by using whole genome microarray. Bioelectromagnetics 26:558–563

    PubMed  Google Scholar 

  30. Veiga MC, Fontoura MM, Oliveira MG, Costa JAV, Santos LO (2020) Magnetic felds: biomass potential of Spirulina sp. for food supplement. Bioprocess Biosyst Eng 43:1231–1240

    CAS  PubMed  Google Scholar 

  31. Li Z, Guo S, Li L, Cai M (2007) Effects of electromagnetic field on the batch cultivation and nutritional composition of Spirulina platensis in an air-lift photobioreactor. Bioresour Technol 98:700–705

    CAS  PubMed  Google Scholar 

  32. Deamici KM, Costa JAV, Santos LO (2016) Magnetic fields as triggers of microalga growth: evaluation of its effect on Spirulina sp. Bioresour Technol 220:62–67

    CAS  PubMed  Google Scholar 

  33. Duarte JH, Costa JAV (2017) Synechococcus nidulans from a thermoelectric coal power plant as a potential CO2 mitigation in culture medium containing flue gas wastes. Bioresour Technol 241:21–24

    CAS  PubMed  Google Scholar 

  34. Barsanti L, Gualtieri P (2006) Algae: Anatomy, Biochemistry, and Biotechnology. CRC Press - Taylor and Francis Group, Boca Raton

    Google Scholar 

  35. Noaman NH, Fattah A, Khaleafa M, Zaky SH (2004) Factors affecting antimicrobial activity of Synechococcus leopoliensis. Microbiol Res 159:395–402

    CAS  PubMed  Google Scholar 

  36. Miller AG, Colman G (1980) Evidence for HCO3- transport by the blue green alga (cyanobacterium) Coccochloris penuicystis. Plant Physiol 65:397–402

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Shiraiwa Y, Goyal A, Tolbert NE (1993) Alkalization of the medium by unicellular green algae during uptake of dissolved inorganic carbon. Plant Cell Physiol 34:649–657

    CAS  Google Scholar 

  38. Deamici KM, Cuellar-Bermudez SP, Muylaert K, Costa JAV, Santos LO (2019) Quantum yield alterations due to the static magnetic fields action on Arthrospira platensis SAG 21.99: evaluation of photosystem activity. Bioresour Technol 292:1–6

    Google Scholar 

  39. Snoussi S, El May AE, Coquet L, Chan P, Jouenne T, Landoulsi A, Dé E (2012) Adaptation of Salmonella enterica Hadar under static magnetic field: effects on outer membrane protein pattern. Proteome Sci 10:1–9

    Google Scholar 

  40. Menestrino BC, Pintos THC, Sala L, Costa JAV, Santos LO (2020) Application of static magnetic fields on the Mixotrophic culture of Chlorella minutissima for carbohydrate production. Appl Biochem Biotechnol 19:822–830

    Google Scholar 

  41. Deamici KM, Santos LO, Costa JAV (2018) Magnetic field action on outdoor and indoor cultures of Spirulina: evaluation of growth, medium consumption and protein profile. Bioresour Technol 249:168–174

    CAS  PubMed  Google Scholar 

  42. Cherdkiatikul T, Suwanwong Y (2014) Production of the α and β Subunits of Spirulina Allophycocyanin and C-Phycocyanin in Escherichia coli: a comparative study of their antioxidant activities. J Biomol Screen 19:959–965

    PubMed  Google Scholar 

  43. Aarholt E, Flinn EA, Smith CW (1982) Magnetic fields affect the lac operon system. Phys Med Biol 27:606–610

    CAS  PubMed  Google Scholar 

  44. Santos LO, Silva PGP, Machado BR, Sala L, Deamici KM (2022) Update on the application of magnetic fields to microalgal cultures. World J Microbiol Biotechnol 38:211

    CAS  PubMed  Google Scholar 

  45. MacColl R, Eisele LE, Menikh A (2003) Allophycocyanin: trimers, monomers, subunits, and homodimers. Biopolymers 72:352–365

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  47. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome reconstructing a giant. Photosynth Res 85:15–32

    CAS  PubMed  Google Scholar 

  48. Adir N, Dines M, Klartag M, McGregor A, Melamed-Frank M (2006) Assembly and disassembly of phycobilisomes. In: Shively JM (ed) Microbiology Monographs: Inclusions in Prokaryotes 2. Springer, Berlin Heidelberg, pp 47–77

    Google Scholar 

  49. Anderson LK, Toole CM (1998) A model for early events in the assembly pathway of cyanobacterial phycobilisomes. Mol Microbiol 30:467–474

    CAS  PubMed  Google Scholar 

  50. McGregor A, Klartag M, David L, Adir N (2008) Allophycocyanin trimer stability and functionality are primarily due to polar enhanced hydrophobicity of the phycocyanobilin binding pocket. J Mol Biol 384:406–421

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are thankful for the financial support provided by the National Counsel for Technological and Scientific Development – Brazil (CNPq). L. F. Marins is a research fellow from Brazilian CNPq (Proc. 309634/2018-0). L. O. Santos is a research fellow from CNPq (Proc. 312486/2022-7).

Funding

The authors received support from National Counsel for Technological and Scientific Development–Brazil (CNPq) for the submitted work.

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Authors and Affiliations

  1. Laboratory of Biotechnology, School of Chemistry and Food, Federal University of Rio Grande, Rio Grande, RS, 96203-900, Brazil

    Raphael R. C. Nascimento, Matheus R. Moreno & Lucielen O. Santos

  2. Laboratory of Molecular Biology, Institute of Biological Sciences, Federal University of Rio Grande, Rio Grande, RS, 96203-900, Brazil

    Raíza S. Azevedo & Luis F. Marins

  3. Laboratory of Biochemical Engineering, School of Chemistry and Food, Federal University of Rio Grande, Rio Grande, RS, 96203-900, Brazil

    Jorge A. V. Costa

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  1. Raphael R. C. Nascimento
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Contributions

RRCdN, MdRM, RdSA, JAVC, LFM, and LOdS: contributed to the study conception and design. Material preparation, data collection and analysis were performed by RRCdN, MdRM, and RdSA. The first draft of the manuscript was written by RRCdN and MdRM, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Lucielen O. Santos.

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Nascimento, R.R.C., Moreno, M.R., Azevedo, R.S. et al. Magnetic Fields as Inducers of Phycobiliprotein Production by Synechococcus elongatus PCC 7942. Curr Microbiol 80, 242 (2023). https://doi.org/10.1007/s00284-023-03348-3

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