Skip to main content
SpringerLink
Log in

Size control of in vitro synthesized magnetite crystals by the MamC protein of Magnetococcus marinus strain MC-1

  • Biotechnologically relevant enzymes and proteins
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Magnetotactic bacteria are a diverse group of prokaryotes that share the unique ability of biomineralizing magnetosomes, which are intracellular, membrane-bounded crystals of either magnetite (Fe3O4) or greigite (Fe3S4). Magnetosome biomineralization is mediated by a number of specific proteins, many of which are localized in the magnetosome membrane, and thus is under strict genetic control. Several studies have partially elucidated the effects of a number of these magnetosome-associated proteins in the control of the size of magnetosome magnetite crystals. However, the effect of MamC, one of the most abundant proteins in the magnetosome membrane, remains unclear. In this present study, magnetite nanoparticles were synthesized inorganically in free-drift experiments at 25 °C in the presence of different concentrations of the iron-binding recombinant proteins MamC and MamCnts (MamC without its first transmembrane segment) from the marine, magnetotactic bacterium Magnetococcus marinus strain MC-1 and three commercial proteins [α-lactalbumin (α-Lac), myoglobin (Myo), and lysozyme (Lyz)]. While no effect was observed on the size of magnetite crystals formed in the presence of the commercial proteins, biomimetic synthesis in the presence of MamC and MamCnts at concentrations of 10–60 μg/mL resulted in the production of larger and more well-developed magnetite crystals (~30–40 nm) compared to those of the control (~20–30 nm; magnetite crystals grown protein-free). Our results demonstrate that MamC plays an important role in the control of the size of magnetite crystals and could be utilized in biomimetic synthesis of magnetite nanocrystals.

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

Similar content being viewed by others

References

  • Addadi L, Weiner S (1992) Control and design principles in biological mineralization. Angew Chem Int Ed 31:153–169

    Article  Google Scholar 

  • Amemiya Y, Arakaki A, Staniland SS, Tanaka T, Matsunaga T (2007) Controlled formation of magnetite crystal by partial oxidation of ferrous hydroxide in the presence of recombinant magnetotactic bacterial protein Mms6. Biomaterials 28:5381–5389

    Article  CAS  PubMed  Google Scholar 

  • Arai T, Norde W (1990) The behavior of some model proteins at solid–liquid interfaces 2. Sequential and competitive adsorption. Colloids Surf 51:17–28

    Article  CAS  Google Scholar 

  • Arakaki A, Webb J, Matsunaga T (2003) A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1. J Biol Chem 278:8745–8750

    Article  CAS  PubMed  Google Scholar 

  • Arakaki A, Masuda F, Amemiya Y, Tanaka T, Matsunaga T (2010) Control of the morphology and size of magnetite particles with peptides mimicking the Mms6 protein from magnetotactic bacteria. J Colloid Interf Sci 343(1):65–70

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bruno J, Wersin P, Stumm W (1992) On the influence of carbonate in mineral dissolution: II. The solubility of FeCO3 (s) at 25 °C and 1 atm total pressure. Geochim Cosmochim Acta 56:1149–1155

    Article  CAS  Google Scholar 

  • Chen, Drysdale (1993) Detection of iron binding proteins by a blotting technique. Anal Biochem 212:47–49

    Article  CAS  PubMed  Google Scholar 

  • Flade K, Lau C, Mertig M, Pompe W (2001) Osteocalcin-controlled dissolution–reprecipitation of calcium phosphate under biomimetic conditions. Chem Mater 13:3596–3602

    Article  CAS  Google Scholar 

  • Garrels RM, Christ CL (1990) Solutions, minerals and equilibria. In: Jones and Bartlett, 2nd edn. Boston, MA, pp 450

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy Server. In: Walker JM (ed) The proteomics protocols handbook. Humana, Totowa, New Jersey, pp 571–607

    Chapter  Google Scholar 

  • Grünberg K, Wawer C, Tebo BM, Schüler D (2001) A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Appl Environ Microbiol 67:4573–4582

    Article  PubMed Central  PubMed  Google Scholar 

  • Grünberg K, Müller EC, Otto A, Reszka R, Linder D, Kube M, Reinhardt R, Schüler D (2004) Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl Environ Microbiol 70:1040–1050

    Article  PubMed Central  PubMed  Google Scholar 

  • Haynes AC, Norde WJ (1994) Interfacial behaviour of biomacromolecules. J Colloid Interf Sci 164:394–409

    Article  CAS  Google Scholar 

  • Hattan SJ, Laue TM, Chasteen ND (2001) Purification and characterization of a novel calcium-binding protein from the extrapallial fluid of the mollusc Mytilus edulis. J Biol Chem 276:4461–4468

    Article  CAS  PubMed  Google Scholar 

  • Kashyap S, Woehl TJ, Valverde-Tercedor C, Sanchez-Quesada MS, Jimenez-Lopez C, Prozorov T (2014) Iron-binding micelles in acidic recombinant biomineralization protein, MamC. J Nano Mat 320124

  • Kolinko I, Lohße A, Borg S, Raschdorf O, Jogler C, Tu Q, Posfai M, Tompa E, Plitzko JM, Brachmann A, Wanner G, Müller R, Zhang Y, Schüler D (2014) Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nat Nanotechnol 9:193–197

    Article  CAS  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lippard SJ, Berg JM (1994) Principles of bioinorganic chemistry. University Science Books, Mill Valley, CA, pp 43–46

    Google Scholar 

  • Mann S, Frankel RB, Blakemore RP (1984) Structure, morphology and crystal growth of bacterial magnetite. Nature 310:405–407

    Article  Google Scholar 

  • Mann S, Frankel RB (1989) Magnetite biomineralization in unicellular organisms. In: Mann S, Webb J, Williams RJP (eds) Biomineralization: chemical and biochemical perspectives. VCH, New York, pp 157–182

    Google Scholar 

  • Martín-Platero AM, Valdivia E, Maqueda M, Martínez-Bueno M (2007) Fast, convenient, and economical method for isolating genomic DNA from lactic acid bacteria using a modification of the protein “salting-out” procedure. Anal Biochem 366:102–104

    Article  PubMed  Google Scholar 

  • Martín Ramos JD (2004) XPowder, a software package for powder X-ray diffraction analysis. Legal Deposit GR 1001/04

  • Matsunaga T, Okamura Y, Fukuda Y, Wahyudi AT, Murase Y, Takeyama H (2005) Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Res 12:157–166

    Article  CAS  PubMed  Google Scholar 

  • Nudelman H, Zarivach R (2014) Structure prediction of magnetosome-associated proteins. Front Microbiol 5:9

    Article  PubMed Central  PubMed  Google Scholar 

  • Perez-Gonzalez T, Rodriguez-Navarro A, Jimenez-Lopez C (2011) Inorganic magnetite precipitation at 25 °C: a low-cost inorganic coprecipitation method. J Supercond Nov Magn 24(1–2):549–557

    Article  CAS  Google Scholar 

  • Prozorov T, Mallapragada SK, Narasimhan B, Wang L, Palo P, Nilsen-Hamilton M, Williams TJ, Bazylinski DA, Prozorov R, Canfield PC (2007) Protein-mediated synthesis of uniform superparamagnetic magnetite nanocrystals. Adv Funct Mater 17:951–957

    Article  CAS  Google Scholar 

  • Prozorov T, Bazylinski DA, Mallapragada SK, Prozorov R (2013) Novel magnetic nanomaterials inspired by magnetotactic bacteria: topical review. Mater Sci Eng R 74:133–172

    Article  Google Scholar 

  • Raj PA, Johnsson M, Levine MJ, Nancollas GH (1992) Salivary statherin. Dependence on sequence, charge, hydrogen bonding potency, and helical conformation for adsorption to hydroxyapatite and inhibition of mineralization. J Biol Chem 267:5968–5976

    CAS  PubMed  Google Scholar 

  • Reddy LH, Arias JL, Nicolas J, Couvreur P (2012) Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem Rev 112(11):5818–5878

    Article  CAS  PubMed  Google Scholar 

  • Scheffel A, Gärdes A, Grünberg K, Wanner G, Schüler D (2008) The major magnetosome proteins MamGFDC are not essential for magnetite biomineralization in Magnetospirillum gryphiswaldense but regulate the size of magnetosome crystals. J Bacteriol 190:377–386

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schübbe S, Williams TJ, Xie G, Kiss HE, Brettin TS, Martinez D, Ross CA, Schüler D, Cox BL, Nealson KH, Bazylinski DA (2009) Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 75:4835–4852

    Article  PubMed Central  PubMed  Google Scholar 

  • Sweeton FH, Baes JCF (1970) The solubility of magnetite and hydrolysis of ferrous ion in aqueous solutions at elevated temperatures. J Chem Thermodyn 2(4):479–500

    Article  CAS  Google Scholar 

  • Tanaka M, Okamura Y, Arakaki A, Tanaka T, Takeyama H, Matsunaga T (2006) Origin of magnetosome membrane: proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics 6:5234–5247

    Article  CAS  PubMed  Google Scholar 

  • Thomas LA, Dekker L, Kallumadil M, Southern P, Wilson M, Nair SP, Pankhurst QA, Parkin IP (2009) Carboxylic acid-stabilised iron oxide nanoparticles for use in magnetic hyperthermia. J Mater Chem 19:6529–6535

    Article  CAS  Google Scholar 

  • Thomas-Keprta KL, Bazylinski DA, Kirschvink JL, Clemett SJ, McKay DS, Wentworth SJ, Vali H, Gibson JEK, Romanek CS (2000) Elongated prismatic magnetite crystals in ALH84001 carbonate globules: potential Martian magnetofossils. Geochim Cosmochim Acta 64:4049–4081

    Article  CAS  PubMed  Google Scholar 

  • Valverde-Tercedor C, Abadía-Molina F, Martinez-Bueno M, Pineda-Molina E, Chen L, Oestreicher Z, Lower BH, Lower S, Bazylinski DA, Jimenez-Lopez C (2014) Subcellular localization of the magnetosome protein MamC in the marine magnetotactic bacterium Magnetococcus marinus strain MC-1 using immunoelectron microscopy. Arch Microbiol 196:481–488

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Prozorov T, Palo PE, Liu X, Vaknin D, Prozorov R (2012) Self-assembly and biphasic iron-binding characteristics of Mms6, a bacterial protein that promotes the formation of superparamagnetic magnetite nanoparticles of uniform size and shape. Biomacromol 13:98–105

    Article  Google Scholar 

  • Wolff A, Frese K, Wissbrock M, Eckstaedt K, Ennen I, Hetaba W, Loeffler S, Regtmeier A, Thomas P, Sewald N, Schattschneider P, Huetten A (2012) Influence of the synthetic polypeptide c25-mms6 on cobalt ferrite nanoparticle formation. J Nanopart Res 14:1161/1

    Article  CAS  Google Scholar 

  • Wolff A, Mill N, Eckstadt K, Ennen I, Hutten A, Hetaba W, Wissbrock M, Sewald N, Loffler S, Dreyer A, Schattschneider P (2014) Oriented attachment explains cobalt ferrite nanoparticle growth in bioinspired syntheses. Beilstein J Nanotechnol 5:210

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Financial funding for this work was provided by grants CGL2010-18274 and CGL2013-46612 from the Spanish Ministry of Culture (MEC). We thank Dr. Angel Delgado Mora (Universidad de Granada) for the Z-size analyses and Rafael López Moreno for the assistance in the experiments. We thank the Centro de Instrumentación Científica personnel from the University of Granada for the TEM analyses and technical assistance and to the personnel from La Factoría (Granada) and LAC (IACT, CSIC-UGR) for their help in protein expression and purification. T. Prozorov acknowledges support from the Department of Energy Office of Science Early Career Research Award. Magnetization measurements and part of the electron microscopy analysis were carried out at the Ames Laboratory (US DOE, Iowa State University), contract no. DE-AC02-07CH11358. D.A.B... is supported by US NSF Grant EAR-1423939 and by SC-12-384 (US DOE C02-07CH11358, Ames Laboratory at Iowa State University). Finally, we also thank C.S. Romanek and three anonymous reviewers for their comments and suggestions that have greatly improved this manuscript.

Author information

Author notes

  1. C. Valverde-Tercedor

    Present address: Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Science Park Golm, 14424, Potsdam, Germany

  2. M. Montalbán-López

    Present address: Department of Molecular Genetics, University of Groningen, Groningen, Netherlands

  3. D. Trubitsyn

    Present address: Department of Biological Sciences, Southwestern Oklahoma State University, Weatherford, OK, 73096, USA

Authors and Affiliations

  1. Departamento de Microbiologia, Universidad de Granada, Campus de Fuentenueva s/n, 18071, Granada, Spain

    C. Valverde-Tercedor, M. Montalbán-López, T. Perez-Gonzalez, M. S. Sanchez-Quesada, M. A. Fernandez-Vivas & C. Jimenez-Lopez

  2. US DOE Ames Laboratory, Ames, IA, 50011, USA

    T. Prozorov

  3. Laboratorio de Estudios Cristalográficos, IACT, CSIC, Granada, Spain

    E. Pineda-Molina

  4. Departamento de Mineralogía y Petrología, Universidad de Granada, Granada, Spain

    A. B. Rodriguez-Navarro

  5. School of Life Sciences, University of Nevada at Las Vegas, Las Vegas, NV, USA

    D. Trubitsyn & Dennis A. Bazylinski

Authors
  1. C. Valverde-Tercedor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Montalbán-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Perez-Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. S. Sanchez-Quesada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Prozorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. Pineda-Molina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. A. Fernandez-Vivas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. B. Rodriguez-Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. D. Trubitsyn
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dennis A. Bazylinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. C. Jimenez-Lopez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to C. Valverde-Tercedor or C. Jimenez-Lopez.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 733 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valverde-Tercedor, C., Montalbán-López, M., Perez-Gonzalez, T. et al. Size control of in vitro synthesized magnetite crystals by the MamC protein of Magnetococcus marinus strain MC-1. Appl Microbiol Biotechnol 99, 5109–5121 (2015). https://doi.org/10.1007/s00253-014-6326-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-6326-y

Keywords

Search

Navigation