Effect of surface hydrophobicity on the function of the immobilized biomineralization protein Mms6
Abstract
Magnetotactic bacteria produce magnetic nanocrystals with uniform shapes and sizes in nature, which has inspired in vitro synthesis of uniformly sized magnetite nanocrystals under mild conditions. Mms6, a biomineralization protein from magnetotactic bacteria with a hydrophobic N-terminal domain and a hydrophilic C-terminal domain, can promote formation of magnetite nanocrystals in vitro with well-defined shape and size in gels under mild conditions. Here we investigate the role of surface hydrophobicity on the ability of Mms6 to template magnetite nanoparticle formation on surfaces. Our results confirmed that Mms6 can form a protein network structure on a monolayer of hydrophobic octadecanethiol (ODT)-coated gold surfaces and facilitate magnetite nanocrystal formation with uniform sizes close to those seen in nature, in contrast to its behavior on more hydrophilic surfaces. We propose that this hydrophobicity effect might be due to the amphiphilic nature of the Mms6 protein and its tendency to incorporate the hydrophobic N-terminal domain into the hydrophobic lipid bilayer environment of the magnetosome membrane, exposing the hydrophilic C-terminal domain that promotes biomineralization. Supporting this hypothesis, the larger and well-formed magnetite nanoparticles were found to be preferentially located on ODT surfaces covered with Mms6 as compared to control samples, as characterized by scanning electron microscopy,more »
- Authors:
-
- Ames Lab. (AMES), Ames, IA (United States); Iowa State Univ., Ames, IA (United States)
- Iowa State Univ., Ames, IA (United States)
- Ames Lab., Ames, IA (United States)
- Publication Date:
- Research Org.:
- Ames Laboratory (AMES), Ames, IA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1234516
- Report Number(s):
- IS-J-8846
Journal ID: ISSN 0888-5885
- Grant/Contract Number:
- AC02-07CH11358.
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Industrial and Engineering Chemistry Research
- Additional Journal Information:
- Journal Volume: 54; Journal Issue: 42; Journal ID: ISSN 0888-5885
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Liu, Xunpei, Zhang, Honghu, Nayak, Srikanth, Parada, German, Anderegg, James, Feng, Shuren, Nilsen-Hamilton, Marit, Akinc, Mufit, and Mallapragada, Surya K. Effect of surface hydrophobicity on the function of the immobilized biomineralization protein Mms6. United States: N. p., 2015.
Web. doi:10.1021/acs.iecr.5b01413.
Liu, Xunpei, Zhang, Honghu, Nayak, Srikanth, Parada, German, Anderegg, James, Feng, Shuren, Nilsen-Hamilton, Marit, Akinc, Mufit, & Mallapragada, Surya K. Effect of surface hydrophobicity on the function of the immobilized biomineralization protein Mms6. United States. https://doi.org/10.1021/acs.iecr.5b01413
Liu, Xunpei, Zhang, Honghu, Nayak, Srikanth, Parada, German, Anderegg, James, Feng, Shuren, Nilsen-Hamilton, Marit, Akinc, Mufit, and Mallapragada, Surya K. Thu .
"Effect of surface hydrophobicity on the function of the immobilized biomineralization protein Mms6". United States. https://doi.org/10.1021/acs.iecr.5b01413. https://www.osti.gov/servlets/purl/1234516.
@article{osti_1234516,
title = {Effect of surface hydrophobicity on the function of the immobilized biomineralization protein Mms6},
author = {Liu, Xunpei and Zhang, Honghu and Nayak, Srikanth and Parada, German and Anderegg, James and Feng, Shuren and Nilsen-Hamilton, Marit and Akinc, Mufit and Mallapragada, Surya K.},
abstractNote = {Magnetotactic bacteria produce magnetic nanocrystals with uniform shapes and sizes in nature, which has inspired in vitro synthesis of uniformly sized magnetite nanocrystals under mild conditions. Mms6, a biomineralization protein from magnetotactic bacteria with a hydrophobic N-terminal domain and a hydrophilic C-terminal domain, can promote formation of magnetite nanocrystals in vitro with well-defined shape and size in gels under mild conditions. Here we investigate the role of surface hydrophobicity on the ability of Mms6 to template magnetite nanoparticle formation on surfaces. Our results confirmed that Mms6 can form a protein network structure on a monolayer of hydrophobic octadecanethiol (ODT)-coated gold surfaces and facilitate magnetite nanocrystal formation with uniform sizes close to those seen in nature, in contrast to its behavior on more hydrophilic surfaces. We propose that this hydrophobicity effect might be due to the amphiphilic nature of the Mms6 protein and its tendency to incorporate the hydrophobic N-terminal domain into the hydrophobic lipid bilayer environment of the magnetosome membrane, exposing the hydrophilic C-terminal domain that promotes biomineralization. Supporting this hypothesis, the larger and well-formed magnetite nanoparticles were found to be preferentially located on ODT surfaces covered with Mms6 as compared to control samples, as characterized by scanning electron microscopy, X-ray diffraction, X-ray photoelectron spectroscopy, and atomic force microscopy studies. A C-terminal domain mutant of this protein did not form the same network structure as wild-type Mms6, suggesting that the network structure is important for the magnetite nanocrystal formation. This article provides valuable insights into the role of surface hydrophilicity on the action of the biomineralization protein Mms6 to synthesize magnetic nanocrystals and provides a facile route to controlling bioinspired nanocrystal synthesis in vitro.},
doi = {10.1021/acs.iecr.5b01413},
journal = {Industrial and Engineering Chemistry Research},
number = 42,
volume = 54,
place = {United States},
year = {Thu Aug 13 00:00:00 EDT 2015},
month = {Thu Aug 13 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Magnetic Nanoparticles: Synthesis, Protection, Functionalization, and Application
journal, February 2007
- Lu, An-Hui; Salabas, E. L.; Schüth, Ferdi
- Angewandte Chemie International Edition, Vol. 46, Issue 8
Superparamagnetic Colloids: Controlled Synthesis and Niche Applications
journal, January 2007
- Jeong, U.; Teng, X.; Wang, Y.
- Advanced Materials, Vol. 19, Issue 1
Multifunctional Magnetic Nanoparticles: Design, Synthesis, and Biomedical Applications
journal, August 2009
- Gao, Jinhao; Gu, Hongwei; Xu, Bing
- Accounts of Chemical Research, Vol. 42, Issue 8
Synthesis, Functionalization, and Biomedical Applications of Multifunctional Magnetic Nanoparticles
journal, May 2010
- Hao, Rui; Xing, Ruijun; Xu, Zhichuan
- Advanced Materials, Vol. 22, Issue 25
The preparation of magnetic nanoparticles for applications in biomedicine
journal, June 2003
- Tartaj, Pedro; Morales, Mar a. del Puerto; Veintemillas-Verdaguer, Sabino
- Journal of Physics D: Applied Physics, Vol. 36, Issue 13
Ultra-large-scale syntheses of monodisperse nanocrystals
journal, November 2004
- Park, Jongnam; An, Kwangjin; Hwang, Yosun
- Nature Materials, Vol. 3, Issue 12
Size-Controlled Synthesis of Magnetite Nanoparticles
journal, July 2002
- Sun, Shouheng; Zeng, Hao
- Journal of the American Chemical Society, Vol. 124, Issue 28
Magnetic Iron Oxide Nanoparticles: Synthesis, Stabilization, Vectorization, Physicochemical Characterizations, and Biological Applications
journal, June 2008
- Laurent, Sophie; Forge, Delphine; Port, Marc
- Chemical Reviews, Vol. 108, Issue 6, p. 2064-2110
Magnetosome formation in prokaryotes
journal, March 2004
- Bazylinski, Dennis A.; Frankel, Richard B.
- Nature Reviews Microbiology, Vol. 2, Issue 3
Magnetite as a prokaryotic biomarker: A review: MAGNETITE AS A PROKARYOTIC BIOMARKER
journal, April 2010
- Jimenez-Lopez, Concepcion; Romanek, Christopher S.; Bazylinski, Dennis A.
- Journal of Geophysical Research: Biogeosciences, Vol. 115, Issue G2
Structural insight into magnetochrome-mediated magnetite biomineralization
journal, October 2013
- Siponen, Marina I.; Legrand, Pierre; Widdrat, Marc
- Nature, Vol. 502, Issue 7473
Biomineralization of ferrimagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magnetotactic bacterium
journal, January 1990
- Mann, Stephen; Sparks, Nicholas H. C.; Frankel, Richard B.
- Nature, Vol. 343, Issue 6255
Biogenic and biomimetic magnetic nanosized assemblies
journal, August 2012
- Lu, Yang; Dong, Liang; Zhang, Le-Cheng
- Nano Today, Vol. 7, Issue 4
Magnetite Biomineralization in Magnetospirillum gryphiswaldense : Time-Resolved Magnetic and Structural Studies
journal, April 2013
- Fdez-Gubieda, M. Luisa; Muela, Alicia; Alonso, Javier
- ACS Nano, Vol. 7, Issue 4
A Cultured Greigite-Producing Magnetotactic Bacterium in a Novel Group of Sulfate-Reducing Bacteria
journal, December 2011
- Lefevre, C. T.; Menguy, N.; Abreu, F.
- Science, Vol. 334, Issue 6063
Molecular Mechanisms of Magnetosome Formation
journal, June 2007
- Komeili, Arash
- Annual Review of Biochemistry, Vol. 76, Issue 1
Nature’s hierarchical materials
journal, November 2007
- Fratzl, Peter; Weinkamer, Richard
- Progress in Materials Science, Vol. 52, Issue 8
Higher-Order Organization by Mesoscale Self-Assembly and Transformation of Hybrid Nanostructures
journal, May 2003
- Cölfen, Helmut; Mann, Stephen
- Angewandte Chemie International Edition, Vol. 42, Issue 21
Novel magnetic nanomaterials inspired by magnetotactic bacteria: Topical review
journal, May 2013
- Prozorov, Tanya; Bazylinski, Dennis A.; Mallapragada, Surya K.
- Materials Science and Engineering: R: Reports, Vol. 74, Issue 5
Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters
journal, February 2014
- Kolinko, Isabel; Lohße, Anna; Borg, Sarah
- Nature Nanotechnology, Vol. 9, Issue 3
Protein-Mediated Synthesis of Uniform Superparamagnetic Magnetite Nanocrystals
journal, April 2007
- Prozorov, T.; Mallapragada, S. K.; Narasimhan, B.
- Advanced Functional Materials, Vol. 17, Issue 6, p. 951-957
Controlled formation of magnetite crystal by partial oxidation of ferrous hydroxide in the presence of recombinant magnetotactic bacterial protein Mms6
journal, December 2007
- Amemiya, Yosuke; Arakaki, Atsushi; Staniland, Sarah S.
- Biomaterials, Vol. 28, Issue 35
Control of the morphology and size of magnetite particles with peptides mimicking the Mms6 protein from magnetotactic bacteria
journal, March 2010
- Arakaki, Atsushi; Masuda, Fukashi; Amemiya, Yosuke
- Journal of Colloid and Interface Science, Vol. 343, Issue 1
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
journal, December 2011
- Wang, Lijun; Prozorov, Tanya; Palo, Pierre E.
- Biomacromolecules, Vol. 13, Issue 1
Morphological Transformations in the Magnetite Biomineralizing Protein Mms6 in Iron Solutions: A Small-Angle X-ray Scattering Study
journal, February 2015
- Zhang, Honghu; Liu, Xunpei; Feng, Shuren
- Langmuir, Vol. 31, Issue 9
Interfacial Properties and Iron Binding to Bacterial Proteins That Promote the Growth of Magnetite Nanocrystals: X-ray Reflectivity and Surface Spectroscopy Studies
journal, February 2012
- Wang, Wenjie; Bu, Wei; Wang, Lijun
- Langmuir, Vol. 28, Issue 9
Integrated Self-Assembly of the Mms6 Magnetosome Protein to Form an Iron-Responsive Structure
journal, July 2013
- Feng, Shuren; Wang, Lijun; Palo, Pierre
- International Journal of Molecular Sciences, Vol. 14, Issue 7
Iron oxide crystal formation on a substrate modified with the Mms6 protein from magnetotactic bacteria
journal, January 2009
- Arakaki, Atsushi; Masuda, Fukashi; Matsunaga, Tadashi
- MRS Proceedings, Vol. 1187
Biotemplated Magnetic Nanoparticle Arrays
journal, November 2011
- Galloway, Johanna M.; Bramble, Jonathan P.; Rawlings, Andrea E.
- Small, Vol. 8, Issue 2
Nanomagnetic Arrays Formed with the Biomineralization Protein Mms6
journal, February 2012
- Galloway, Johanna M.; Bramble, Jonathan P.; Rawlings, Andrea E.
- Journal of Nano Research, Vol. 17
Cobalt Ferrite Nanocrystals: Out-Performing Magnetotactic Bacteria
journal, October 2007
- Prozorov, Tanya; Palo, Pierre; Wang, Lijun
- ACS Nano, Vol. 1, Issue 3
Ultralarge atomically flat template-stripped Au surfaces for scanning probe microscopy
journal, July 1993
- Hegner, Martin; Wagner, Peter; Semenza, Giorgio
- Surface Science, Vol. 291, Issue 1-2
Formation of monolayer films by the spontaneous assembly of organic thiols from solution onto gold
journal, January 1989
- Bain, Colin D.; Troughton, E. Barry; Tao, Yu Tai
- Journal of the American Chemical Society, Vol. 111, Issue 1, p. 321-335
Poly(ethylene glycol) Monolayer Formation and Stability on Gold and Silicon Nitride Substrates
journal, October 2008
- Cerruti, Marta; Fissolo, Stefano; Carraro, Carlo
- Langmuir, Vol. 24, Issue 19
Molecular Conformation in Oligo(ethylene glycol)-Terminated Self-Assembled Monolayers on Gold and Silver Surfaces Determines Their Ability To Resist Protein Adsorption
journal, January 1998
- Harder, P.; Grunze, M.; Dahint, R.
- The Journal of Physical Chemistry B, Vol. 102, Issue 2
Mixed poly (ethylene glycol) and oligo (ethylene glycol) layers on gold as nonfouling surfaces created by backfilling
journal, December 2011
- Lokanathan, Arcot R.; Zhang, Shuai; Regina, Viduthalai R.
- Biointerphases, Vol. 6, Issue 4
Chemisorption of thiolated poly(ethylene oxide) to gold: surface chain densities measured by ellipsometry and neutron reflectometry
journal, January 2005
- Unsworth, Larry D.; Tun, Zin; Sheardown, Heather
- Journal of Colloid and Interface Science, Vol. 281, Issue 1
Interaction of colloidal nanoparticles with their local environment: the (ionic) nanoenvironment around nanoparticles is different from bulk and determines the physico-chemical properties of the nanoparticles
journal, July 2014
- Pfeiffer, Christian; Rehbock, Christoph; Hühn, Dominik
- Journal of The Royal Society Interface, Vol. 11, Issue 96
The effect of humic acid adsorption on pH-dependent surface charging and aggregation of magnetite nanoparticles
journal, March 2006
- Illés, E.; Tombácz, E.
- Journal of Colloid and Interface Science, Vol. 295, Issue 1
Characterization of the “native” surface thin film on pure polycrystalline iron: A high resolution XPS and TEM study
journal, February 2007
- Bhargava, G.; Gouzman, I.; Chun, C. M.
- Applied Surface Science, Vol. 253, Issue 9
Magnetite-polylactic acid core-shell nanoparticles by ring-opening polymerization under microwave irradiation
journal, January 2012
- Nan, Alexandrina; Turcu, Rodica; Liebscher, Jürgen
- Journal of Polymer Science Part A: Polymer Chemistry, Vol. 50, Issue 8
Atomic number and crystallographic contrast images with the SEM: a review of backscattered electron techniques
journal, March 1987
- Lloyd, Geoffrey E.
- Mineralogical Magazine, Vol. 51, Issue 359
Structure prediction of magnetosome-associated proteins
journal, January 2014
- Nudelman, Hila; Zarivach, Raz
- Frontiers in Microbiology, Vol. 5
The magnetosome model: insights into the mechanisms of bacterial biomineralization
journal, January 2013
- Rahn-Lee, Lilah; Komeili, Arash
- Frontiers in Microbiology, Vol. 4
Magnetic bacterial protein Mms6 controls morphology, crystallinity and magnetism of cobalt-doped magnetite nanoparticles in vitro
journal, January 2011
- Galloway, Johanna M.; Arakaki, Atsushi; Masuda, Fukashi
- Journal of Materials Chemistry, Vol. 21, Issue 39
Works referencing / citing this record:
Tuning properties of biomimetic magnetic nanoparticles by combining magnetosome associated proteins
journal, June 2019
- Peigneux, Ana; Jabalera, Ylenia; Vivas, Ma Antonia Fernández
- Scientific Reports, Vol. 9, Issue 1
Nano- and micro-patterning biotemplated magnetic CoPt arrays
journal, January 2016
- Galloway, J. M.; Bird, S. M.; Talbot, J. E.
- Nanoscale, Vol. 8, Issue 22
Tuning properties of biomimetic magnetic nanoparticles by combining magnetosome associated proteins
journal, June 2019
- Peigneux, Ana; Jabalera, Ylenia; Vivas, Ma Antonia Fernández
- Scientific Reports, Vol. 9, Issue 1