Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

High-yield growth and magnetosome formation by Magnetospirillum gryphiswaldense MSR-1 in an oxygen-controlled fermentor supplied solely with air

  • 815 Accesses

  • 50 Citations

Abstract

Magnetotactic bacteria are difficult to grow under defined conditions in culture, which has presented a major obstacle to commercial application of magnetosomes. We studied the relationships among the cell growth, magnetosome formation, dissolved oxygen concentration (DO), and the ability to supply oxygen to the cells. Mass culture of Magnetospirillum gryphiswaldense MSR-1 for the production of magnetosomes was established in a 42-L fermentor under the following conditions: (1) sterile air was the sole gas supplied in the fermentor, and DO could be regulated at any level below 10% saturation by cascading the stir rate to DO, (2) to resolve the paradoxical situation that the cell growth requires higher DO whereas magnetosome formation requires low DO below the detectable range of regular oxygen electrode, DO was controlled to optimal level using the change of cell growth rate, rather than reading from the highly sensitive oxygen electrode, as the signal for determining appropriate DO, and (3) timing and rate of supplying the substrates were determined by measuring cell density and Na-lactate concentration. Under these conditions, cell density (OD565) of strain MSR-1 reached 7.24 after 60-h culture in a 42-L fermentor, and cell yield (dry weight) was 2.17 g/L, the highest yield so far being reported. The yield of magnetosomes (dry weight) was 41.7 mg/L and 16.7 mg/L/day, which were 2.8 and 2.7 times higher than the previously reported yields.

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

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

References

  1. Balkwill DL, Maratea D, Blakemore RP (1980) Ultrastructure of a magnetic spirillum. J Bacteriol 141(3):1399–1408

  2. Bazylinski D (1995) Structure and function of the bacterial magnetosome. ASM News 61:337–343

  3. Bazylinski DA, Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2:217–230

  4. Bazylinski DA, Garratt-Reed A, Frankel RB (1994) Electron-microscopic studies of magnetosomes in magnetotactic bacteria. Microsc Res Tech 27:389–401

  5. Blakemore RP (1975) Magnetotactic bacteria. Science 190:377–379

  6. Blakemore RP, Maratea D, Wolfe RS (1979) Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 140:720–729

  7. Blakemore RP, Short KA, Basilisk DA, Rosenblatt C, Frankel RB (1985) Microaerobic conditions are required for magnetite formation within Aquaspirillum magnetotacticum. Geomicrobiol J 4:53–71

  8. Gorby YA, Beveridge TJ, Blakemore RP (1988) Characterization of the bacterial magnetosome membrane. J Bacteriol 170:834–841

  9. Heyen U, Schüler D (2003) Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl Microbiol Biotechnol 61:536–544

  10. Hoell A, Wiedenmann A, Heyen U, Schüler D (2004) Nanostructure and field-induced arrangement of magnetosomes studied by SANSPOL. Physica B 350:e309–e3013

  11. Hopkin M (2004) Magnet-making bacteria could target tumours. Nature DOI https://doi.org/10.1038/news040906-11

  12. Jiang W, Zhao DH, Li Y, Tian JS, Wang ZF, Li JL (2002) Submerged culture of Magnetospirillum gryphiswaldense under N2-fixing condition and regulation of activity of nitrogen fixation. Chin Sci Bull 47(24):2095–2099

  13. Lang C, Schüler D, Faivre D (2007) Synthesis of magnetite nanoparticles for bio- and nanotechnology: genetic engineering and biomimetics of bacterial magnetosomes. Macromol Biosci 7:144–151

  14. Matsunaga T, Kamiya S (1987) Use of magnetic particles isolated from magnetotactic bacteria for enzyme immobilization. Appl Microbiol Biotechnol 26:328–332

  15. Matsunaga T, Tsujimura N, Kamiya S (1996) Enhancement of magnetic particle-production by nitrate and succinate fed-batch culture of Magnetospirillum sp. AMB-1. Biotechnol Tech 10:495–500

  16. Matsunaga T, Ueki F, Obata K, Tajima H, Tanaka T, Takeyama H, Goda Y, Fujimoto S (2003) Fully automated immunoassay system of endocrine disrupting chemicals using monoclonal antibodies chemically conjugated to bacterial magnetic particles. Anal Chim Acta 475:75–83

  17. Matsunaga T, Suzuki T, Tanaka M, Arakaki A (2007) Molecular analysis of magnetotactic bacteria and development of functional bacterial magnetic particles for nano-biotechnology. Trends Biotechnol 25(4):182–188

  18. Nakamura N, Matsunaga T (1993) Highly sensitive detection of allergen using bacterial magnetic particles. Anal Chim Acta 281:585–589

  19. Noguchi Y, Fujiwara T, Yoshimatsu K, Fukumori Y (1999) Iron reductase for magnetite synthesis in the magnetotactic bacterium Magnetospirillum magnetotacticum. J Bacteriol 181:2142–2147

  20. Ota H, Takeyama H, Nakayama H, Katoh T, Matsunaga T (2003) SNP detection in transforming growth factor-1 gene using bacterial magnetic particles. Biosens Bioelectron 18:683–687

  21. Schüler D, Baeuerlein E (1998) Dynamics of iron uptake and Fe3O4 mineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J Bacteriol 180:159–162

  22. Schüler D, Frankel RB (1999) Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications. Appl Microbiol Biotechnol 52:464–473

  23. Spring S, Schleifer K-H (1995) Diversity of magnetotactic bacteria. Syst Appl Microbiol 18:147–153

  24. Staniland S, Ward B, Harrison A, Gerrit van der L, Telling N (2007) Rapid magnetosome formation shown by real-time X-ray magnetic circular dichroism. Proc Natl Acad Sci 104(49):19524–19528

  25. Sun JB, Duan JH, Dai SL, Ren J, Zhang YD, Tian JS, Li Y (2007a) In vitro and in vivo antitumor effects of doxorubicin loaded with bacterial magnetosomes (DBMs) on H22 cells: the magnetic bio-nanoparticles as drug carriers. Cancer Lett 258:109–117

  26. Sun JB, Jiang W, Li Y, Zhang YD, Li JL (2007b) The magnetosomes of magnetotactic bacteria may be used as drug-carriers for targeted therapy. Microbiology 34(1):165–168

  27. Takeyama H, Yamazawa A, Nakamura C, Matsunaga T (1995) Application of bacterial magnetic particles as novel DNA carriers for ballistic transformation of a marine cyanobacterium. Biotechnol Tech 9(5):355–360

  28. Wacker R, Ceyhan B, Alhorn P, Schüler D, Lang C, Niemeyer CM (2007) Magneto immuno-PCR: A novel immunoassay based on biogenic magnetosome nanoparticles. Biochem Biophys Res Commun 357:391–396

  29. Yang CD, Takeyama H, Tanaka T, Matsunaga T (2001) Effects of growth medium composition, iron sources and atmospheric oxygen concentrations on production of luciferase–bacterial magnetic particle complex by a recombinant Magnetospirillum magneticum AMB-1. Enzyme Microbiol Tech 29:13–19

  30. Yoza B, Matsumoto M, Matsunaga T (2002) DNA extraction using bacterial magnetic particles in the presence of amino silane compound. J Biotechnol 94:217–224

Download references

Acknowledgements

This work was supported by the Chinese High Technology Research and Development Program (Grants No.2006AA02Z233 and 2007AA021804), and the Chinese National Science Foundation (Grant No. 30570023).

Author information

Correspondence to Ying Li.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sun, J., Zhao, F., Tang, T. et al. High-yield growth and magnetosome formation by Magnetospirillum gryphiswaldense MSR-1 in an oxygen-controlled fermentor supplied solely with air. Appl Microbiol Biotechnol 79, 389 (2008). https://doi.org/10.1007/s00253-008-1453-y

Download citation

Keywords

  • Magnetospirillum gryphiswaldense
  • Magnetosome
  • Oxygen-controlled
  • Fermentor
  • Submerged culture