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Magnetic immobilization of Bacillus subtilis natto cells for menaquinone-7 fermentation

  • Biotechnological products and process engineering
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Abstract

Production of menaquinone-7 (MK-7) by Bacillus subtilis natto is associated with major drawbacks. To address the current challenges in MK-7 fermentation, studying the effect of magnetic nanoparticles on the bacterial cells can open up a new domain for intensified bioprocesses. This article introduces the new concept of application of iron oxide nanoparticles (IONs) as a pioneer tool for MK-7 process intensification. In this order, IONs with the average size of 11 nm were successfully fabricated and characterized for possible in situ removal of target substances from the fermentation media. The prepared particles were used for decoration and immobilization of B. subtilis natto cells. Presence of iron oxide nanoparticles significantly enhanced the MK-7 specific yield (15 %) as compared to the control samples. In addition, fabricated IONs showed a promising ability for in situ recovery of bacterial cells from the fermentation media with more than 95 % capture efficiency. Based on the results, IONs can be implemented successfully as a novel tool for MK-7 production. This study provides a considerable interest for industrial application of magnetic nanoparticles and their future role in designing an intensified biological process.

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References

  • Ansari F, Grigoriev P, Libor S, Tothill IE, Ramsden JJ (2009) DBT degradation enhancement by decorating Rhodococcus erythropolis IGST8 with magnetic Fe3O4 nanoparticles. Biotechnol Bioeng 102:1505–1512

    Article  PubMed  CAS  Google Scholar 

  • Berenjian A, Mahanama R, Talbot A, Biffin R, Regtop H, Valtchev P, Kavanagh J, Dehghani F (2011) Efficient media for high menaquinone-7 production: response surface methodology approach. N Biotechnol 28:665--672

  • Berenjian A, Mahanama R, Talbot A, Regtop H, Kavanagh J, Dehghani F (2014) Designing of an intensification process for biosynthesis and recovery of menaquinone-7. Appl Biochem Biotechnol 172:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Berenjian A, Mahanama R, Kavanagh J, Dehghani F (2015) Vitamin K series: current status and future prospects. Crit Rev Biotechnol 35:199–208

    Article  PubMed  CAS  Google Scholar 

  • Berry CC, Wells S, Charles S, Aitchison G, Curtis ASG (2004) Cell response to dextran-derivatised iron oxide nanoparticles post internalisation. Biomaterials 25:5405–5413

    Article  PubMed  CAS  Google Scholar 

  • Bromberg L, Chang EP, Hatton TA, Concheiro A, Magariños B, Alvarez-Lorenzo C (2011) Bactericidal core-shell paramagnetic nanoparticles functionalized with poly(hexamethylene biguanide). Langmuir 27:420–429

    Article  PubMed  CAS  Google Scholar 

  • Brunner TJ, Wick P, Manser P, Spohn P, Grass RN, Limbach LK, Bruinink A, Stark WJ (2006) In vitro cytotoxicity of oxide nanoparticles: comparison to asbestos, silica, and the effect of particle solubility. Environ Sci Technol 40:4374–4381

    Article  PubMed  CAS  Google Scholar 

  • Can K, Ozmen M, Ersoz M (2009) Immobilization of albumin on aminosilane modified superparamagnetic magnetite nanoparticles and its characterization. Colloids Surf B Biointerfaces 71:154–159

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S, Bandyopadhyay A, Sarkar K (2011) Effect of iron oxide and gold nanoparticles on bacterial growth leading towards biological application. J Nanobiotechnology 9:34

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chwalibog A, Sawosz E, Hotowy A, Szeliga J, Mitura S, Mitura K, Grodzik M, Orlowski P, Sokolowska A (2010) Visualization of interaction between inorganic nanoparticles and bacteria or fungi. Int J Nanomedicine 5:1085–1094

    Article  PubMed  PubMed Central  Google Scholar 

  • Dickson JS, Koohmaraie M (1989) Cell surface charge characteristics and their relationship to bacterial attachment to meat surfaces. Appl Environ Microbiol 55:832–836

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ebrahiminezhad A, Davaran S, Rasoul-Amini S, Barar J, Moghadam M, Ghasemi Y (2012) Synthesis, characterization and anti-listeria monocytogenes effect of amino acid coated magnetite nanoparticles. Curr Nanosci 8:868–874

    Article  CAS  Google Scholar 

  • Ebrahiminezhad A, Ghasemi Y, Rasoul-Amini S, Barar J, Davaran S (2013) Preparation of novel magnetic fluorescent nanoparticles using amino acids. Colloids Surf B Biointerfaces 102:534–539

    Article  PubMed  CAS  Google Scholar 

  • Ebrahiminezhad A, Rasoul-Amini S, Davaran S, Barar J, Ghasemi Y (2014) Impacts of iron oxide nanoparticles on the invasion power of Listeria monocytogenes. Curr Nanosci 10:382–388

    Article  CAS  Google Scholar 

  • Ebrahiminezhad A, Rasoul-Amini S, Kouhpayeh A, Davaran S, Barar J, Ghasemi Y (2015) Impacts of amine functionalized iron oxide nanoparticles on HepG2 cell line. Curr Nanosci 11:113–119

    Article  CAS  Google Scholar 

  • Epand RM, Epand RF, Savage PB (2008) Ceragenins (cationic steroid compounds), a novel class of antimicrobial agents. Drug News Perspect 21:307–311

    Article  PubMed  CAS  Google Scholar 

  • Ficai D, Andronescu E, Ficai A, Voicu G, Vasile B, Ionita V, Guran C (2012) Synthesis and characterization of mesoporous magnetite based nanoparticles. Curr Nanosci 8:875–879

    Article  CAS  Google Scholar 

  • Gholami A, Rasoul-Amini S, Ebrahiminezhad A, Seradj SH, Ghasemi Y (2015) Lipoamino acid coated superparamagnetic iron oxide nanoparticles concentration and time dependently enhanced growth of human hepatocarcinoma cell line (Hep-G2). J Nanomater 45:1–9

    Article  Google Scholar 

  • Grumezescu AM, Mihaiescu DE, Mogosanu DE, Chifiriuc MC, Lazar V, Calugarescu I, Traistaru V (2010) In vitro assay of the antimicrobial activity of Fe3O4 and CoFe2O4/oleic acid—core/shell on clinical isolates of bacterial and fungal strains. Optoelectron Adv Mat 4:1798–1801

    CAS  Google Scholar 

  • Huang YF, Wang YF, Yan XP (2010) Amine-functionalized magnetic nanoparticles for rapid capture and removal of bacterial pathogens. Environ Sci Technol 44:7908–7913

    Article  PubMed  CAS  Google Scholar 

  • Islam S, Kusumoto Y, Abdulla-Al-Mamun M, Manaka H, Horie Y (2012) Synthesis, characterization and application of Dumbbell-shaped magnetic (Fe3O4 and-Fe2O3) nanoparticles against HeLa (cancer) cells. Curr Nanosci 8:811–818

    Article  CAS  Google Scholar 

  • Jucker BA, Harms H, Zehnder A (1996) Adhesion of the positively charged bacterium Stenotrophomonas (Xanthomonas) maltophilia 70401 to glass and Teflon. J Bacteriology 178:5472–5479

    CAS  Google Scholar 

  • Karlsson HL, Gustafsson J, Cronholm P, Möller L (2009) Size-dependent toxicity of metal oxide particles—a comparison between nano- and micrometer size. Toxicol Lett 188:112–118

    Article  PubMed  CAS  Google Scholar 

  • Larsen MU, Seward M, Tripathi A, Shapley NC (2009) Biocompatible nanoparticles trigger rapid bacteria clustering. Biotechnol Prog 25:1094–1102

    Article  PubMed  CAS  Google Scholar 

  • Li YG, Gao HS, Li WL, Xing JM, Liu HZ (2009) In situ magnetic separation and immobilization of dibenzothiophene-desulfurizing bacteria. Bioresour Technol 100:5092–5096

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Guan Y, Yang Y, Ma Z, Wu X, Liu H (2004) Preparation of superparamagnetic immunomicrospheres and application for antibody purification. J Appl Polym Sci 94:2205–2211

    Article  CAS  Google Scholar 

  • Mahanama R, Berenjian A, Valtchev P, Talbot A, Biffin R, Regtop H, Dehghani F, Kavanagh JM (2011) Enhanced production of menaquinone 7 via solid substrate fermentation from Bacillus subtilis. Int J Food Eng 7:5

    Article  Google Scholar 

  • Mahanama R, Berenjian A, Regtop H, Talbot A, Dehghani F, Kavanagh JM (2012) Modeling menaquinone 7 production in tray type solid state fermenter. ANZIAM J 53:354–372

    Google Scholar 

  • Marques MPC, Fernandes P (2011) Microfluidic devices: useful tools for bioprocess intensification. Molecules 16:8368–8401

    Article  PubMed  CAS  Google Scholar 

  • Martin ST, Morrison CL, Hoffmann MR (1994) Photochemical mechanism of size-quantized vanadium-doped TiO2 particles. J Phys Chem 98:13695–13704

    Article  CAS  Google Scholar 

  • Muller K, Skepper JN, Posfai M, Trivedi R, Howarth S, Corot C, Lancelot E, Thompson PW, Brown AP, Gillard JH (2007) Effect of ultrasmall superparamagnetic iron oxide nanoparticles (ferumoxtran-10) on human monocyte-macrophages in vitro. Biomaterials 28:1629–1642

    Article  PubMed  Google Scholar 

  • Ramteke C, Sarangi BK, Chakrabarti T, Mudliar S, Satpute D, Pandey RA (2010) Synthesis and broad spectrum antibacterial activity of magnetite ferrofluid. Curr Nanosci 6:587–591

    Article  CAS  Google Scholar 

  • Singh N, Jenkins GJ, Asadi R, Doak SH (2010) Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev 1:5358

    Article  Google Scholar 

  • Soneshein AL, Hoch JA, Losick R (2002) Bacillus subtilis and its closest relatives. ASM Press, Washington DC

    Google Scholar 

  • Vaghari H, Eskandari M, Sobhani V, Berenjian A, Song Y, Jafarizadeh-Malmiri H (2015) Process intensification for production and recovery of biological products. Am J Biochem Biotech 11:37–43

    Article  Google Scholar 

  • Wei Wang X, Cheng ZH, Li JS, Yuan ZH (2012) Controllable synthesis and magnetic properties of ferromagnetic nanowires and nanotubes. Curr Nanosci 8:801–809

    Article  Google Scholar 

  • Wohlgemuth R (2009) The locks and keys to industrial biotechnology. N Biotechnol 25(4):204–213

    Article  PubMed  CAS  Google Scholar 

  • Zhao SY, Don KL, Chang WK, Hyun GC, Young HK, Young SK (2006) Synthesis of magnetic nanoparticles of Fe3O4 and CoFe2O4 and their surface modification by surfactant adsorption. Bull Korean Chem Soc 27:237–242

    Article  Google Scholar 

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Acknowledgments

This investigation was financially supported by Iran National Science Foundation and The University of Waikato, New Zealand.

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The authors declare that they have no competing interests.

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The article is original and has not been formally published in any other peer-reviewed journal and does not infringe any existing copyright and any other third party rights.

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Authors and Affiliations

  1. Department of Medical Biotechnology, School of Medicine and Noncommunicable Diseases Research Center, Fasa University of Medical Sciences, Fasa, Iran

    Alireza Ebrahiminezhad

  2. School of Engineering, Faculty of Science and Engineering, The University of Waikato, Hamilton, New Zealand

    Alireza Ebrahiminezhad, Vikas Varma, Shuyi Yang & Aydin Berenjian

Authors
  1. Alireza Ebrahiminezhad
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  2. Vikas Varma
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  3. Shuyi Yang
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  4. Aydin Berenjian
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Correspondence to Aydin Berenjian.

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Ebrahiminezhad, A., Varma, V., Yang, S. et al. Magnetic immobilization of Bacillus subtilis natto cells for menaquinone-7 fermentation. Appl Microbiol Biotechnol 100, 173–180 (2016). https://doi.org/10.1007/s00253-015-6977-3

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  • DOI: https://doi.org/10.1007/s00253-015-6977-3

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