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Cited by 180Geomagnetism and Paleomagnetism StudiesMagnetic Properties and Synthesis of FerritesCharacterization and Applications of Magnetic Nanoparticles

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Applications of Magnetotactic Bacteria, Magnetosomes and Magnetosome Crystals in Biotechnology and Nanotechnology: Mini-Review

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Vargas, Gabriele, Cypriano, Jefferson, Correa, Tarcisio, Leão, Pedro, Bazylinski, Dennis A., Abreu, Fernanda·2018·Molecules
DOI 10.3390/molecules23102438PMC PMC6222368
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Abstract

Magnetotactic bacteria (MTB) biomineralize magnetosomes, which are defined as intracellular nanocrystals of the magnetic minerals magnetite (Fe₃O₄) or greigite (Fe₃S₄) enveloped by a phospholipid bilayer membrane. The synthesis of magnetosomes is controlled by a specific set of genes that encode proteins, some of which are exclusively found in the magnetosome membrane in the cell. Over the past several decades, interest in nanoscale technology (nanotechnology) and biotechnology has increased significantly due to the development and establishment of new commercial, medical and scientific processes and applications that utilize nanomaterials, some of which are biologically derived. One excellent example of a biological nanomaterial that is showing great promise for use in a large number of commercial and medical applications are bacterial magnetite magnetosomes. Unlike chemically-synthesized magnetite nanoparticles, magnetosome magnetite crystals are stable single-magnetic domains and are thus permanently magnetic at ambient temperature, are of high chemical purity, and display a narrow size range and consistent crystal morphology. These physical/chemical features are important in their use in biotechnological and other applications. Applications utilizing magnetite-producing MTB, magnetite magnetosomes and/or magnetosome magnetite crystals include and/or involve bioremediation, cell separation, DNA/antigen recovery or detection, drug delivery, enzyme immobilization, magnetic hyperthermia and contrast enhancement of magnetic resonance imaging. Metric analysis using Scopus and Web of Science databases from 2003 to 2018 showed that applied research involving magnetite from MTB in some form has been focused mainly in biomedical applications, particularly in magnetic hyperthermia and drug delivery.

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Figure 1 Classification of scientific publications reporting on applications of magnetosomes by area [7,8] from 1987 until 2018. Scientific articles containing the keyword “magnetosome (s)” in the title were classified in different subareas of Biotechnology (bioremediation, cell separation, DNA analysis, drug delivery, enzyme immobilization, food, hyperthermia, image contrast). For analysis of raw data, see Table S1. The criteria used for selection of these data are detailed in “Database generation & analysis section”.
Figure 1 Classification of scientific publications reporting on applications of magnetosomes by area [7,8] from 1987 until 2018. Scientific articles containing the keyword “magnetosome (s)” in the title were classified in different subareas of Biotechnology (bioremediation, cell separation, DNA analysis, drug delivery, enzyme immobilization, food, hyperthermia, image contrast). For analysis of raw data, see Table S1. The criteria used for selection of these data are detailed in “Database generation & analysis section”.CC BY · PubMed Central
Figure 2 Global publication records (1st January 1975–25th February 2018) containing the keywords “magnetotactic bacteria or magnetosome(s)” in article titles [7,8]. For analysis of the raw data, see Table S2. The criteria used for selection of data are detailed in the “Database generation & analysis section”.
Figure 2 Global publication records (1st January 1975–25th February 2018) containing the keywords “magnetotactic bacteria or magnetosome(s)” in article titles [7,8]. For analysis of the raw data, see Table S2. The criteria used for selection of data are detailed in the “Database generation & analysis section”.CC BY · PubMed Central
Figure 3 Total number of publications by application area. All scientific articles on databases [7,8] containing the keyword “magnetosome (s)” in article title were classified according to application area in Biotechnology (bioremediation, cell separation, DNA analysis, drug delivery, enzyme immobilization, food, hyperthermia, image contrast). For analysis of raw data, see Table S1. The criteria used for selection of these data are detailed in “Database generation & analysis section”.
Figure 3 Total number of publications by application area. All scientific articles on databases [7,8] containing the keyword “magnetosome (s)” in article title were classified according to application area in Biotechnology (bioremediation, cell separation, DNA analysis, drug delivery, enzyme immobilization, food, hyperthermia, image contrast). For analysis of raw data, see Table S1. The criteria used for selection of these data are detailed in “Database generation & analysis section”.CC BY · PubMed Central
Figure 4 Transmission electron microscopy images of magnetosomes organized in chain(s) within magnetotactic bacteria, showing cuboctahedral (A), prismatic (B) and bullet-shaped (C) magnetite magnetosomes.
Figure 4 Transmission electron microscopy images of magnetosomes organized in chain(s) within magnetotactic bacteria, showing cuboctahedral (A), prismatic (B) and bullet-shaped (C) magnetite magnetosomes.CC BY · PubMed Central
Figure 5 Illustrative scheme of magnetosome purification. Cells of Magnetospirillum gryphiswaldense strain MRS-1 are grown in a fermenter and then lysed using different methods and magnetosomes purified from lysed cells using magnetic concentration and separation. This scheme is based on numerous studies [12,56,60,61,62,63,64].
Figure 5 Illustrative scheme of magnetosome purification. Cells of Magnetospirillum gryphiswaldense strain MRS-1 are grown in a fermenter and then lysed using different methods and magnetosomes purified from lysed cells using magnetic concentration and separation. This scheme is based on numerous studies [12,56,60,61,62,63,64].CC BY · PubMed Central
Figure 6 Illustrative scheme showing the magnetic recovery of Se-containing cells of Ms. magneticum strain AMB-1 grown in culture medium containing SeO32−. Cells reduced SeO32− to Se which accumulated in cells as intracytoplasmic granules (green). After seven days of incubation followed by magnetic separation of the cells, 68.1% of the Se was removed from the medium [85].
Figure 6 Illustrative scheme showing the magnetic recovery of Se-containing cells of Ms. magneticum strain AMB-1 grown in culture medium containing SeO32−. Cells reduced SeO32− to Se which accumulated in cells as intracytoplasmic granules (green). After seven days of incubation followed by magnetic separation of the cells, 68.1% of the Se was removed from the medium [85].CC BY · PubMed Central
Figure 7 Illustrative scheme of the functionalization of magnetosome from Ms. gryphyswaldense strain MSR-1 with doxorubicin (DOX) binding to the amino groups of magnetosome proteins (red rectangles) inserted into the membrane of magnetosomes, forming DBM (DOX loaded magnetosomes). After treatment with DBM, cancer cells were inhibited from growing and the use of DBM resulted in a slow release of DOX. This indicates that the DBM complex is not degraded during systemic circulation and possesses potent antitumor activity [63].
Figure 7 Illustrative scheme of the functionalization of magnetosome from Ms. gryphyswaldense strain MSR-1 with doxorubicin (DOX) binding to the amino groups of magnetosome proteins (red rectangles) inserted into the membrane of magnetosomes, forming DBM (DOX loaded magnetosomes). After treatment with DBM, cancer cells were inhibited from growing and the use of DBM resulted in a slow release of DOX. This indicates that the DBM complex is not degraded during systemic circulation and possesses potent antitumor activity [63].CC BY · PubMed Central
Figure 8 Illustrative scheme of cancer hyperthermia therapy research protocols using magnetosome magnetite crystals [104]. Magnetosomes coated with poly-l-lysine (PLL) without membrane (M-PLL) presented an antitumor effect in intracranial U87-Luc tumors in mice. This effect was observed after treatment of mice with 500 μg of M-PLL followed by 28 magnetic sessions (MS) 30 min/day with 202 kHz and 27 mT. In this case, hyperthermia induced a temperature increase, reaching 42 °C. After 350 days of the first exposure, tumors were eliminated in 100% of the treated mice. In contrast, the same treatment using superparamagnetic iron oxide nanoparticles (SION) resulted in a less effective increase of temperature and only 20% mice had tumors eliminated after 350 days [100].
Figure 8 Illustrative scheme of cancer hyperthermia therapy research protocols using magnetosome magnetite crystals [104]. Magnetosomes coated with poly-l-lysine (PLL) without membrane (M-PLL) presented an antitumor effect in intracranial U87-Luc tumors in mice. This effect was observed after treatment of mice with 500 μg of M-PLL followed by 28 magnetic sessions (MS) 30 min/day with 202 kHz and 27 mT. In this case, hyperthermia induced a temperature increase, reaching 42 °C. After 350 days of the first exposure, tumors were eliminated in 100% of the treated mice. In contrast, the same treatment using superparamagnetic iron oxide nanoparticles (SION) resulted in a less effective increase of temperature and only 20% mice had tumors eliminated after 350 days [100].CC BY · PubMed Central
Figure 9 Schematic representation of a functionalized magnetosome according to each application described in the Biotechnology section of this review (cell separation; hyperthermia, drug delivery, image contrast, food analysis, enzyme immobilization and bioremediation and DNA and antigen recovery/detection). Drug delivery: the association between the surface proteins of the magnetosome and doxorubicin (DOX), an anti-breast cancer drug [63]. Cell separation: the modified magnetosomes were bound to anti-murinic G Ig anti-CD19 and used for separating B-lymphocytes from peripheral blood cells [90]. Food sciences: a capture system with the magnetosome proteins fused using a cross-linking reagent bis(sulfosuccinimidyl) suberate (BS3) for attachment of antibodies to Salmonella and Vibrio species from food samples (e.g., milk, egg and pork) [76]. DNA/Antigen analysis: antibody-functionalized magnetosomes were used for immobilization of HBsAg (hepatitis B antigen) in human serum and enhancement of sensitivity of immunoassay [72]. Image contrast: magnetosomes with specific proteins bound to the surface with high affinity to target cells were used as superparamagnetic contrast agents for magnetic resonance imaging [117]. Hyperthermia: magnetosomes coated with poly-l-lysine (PLL) were used in hyperthermia [100]. Enzyme immobilization and bioremediation: magnetosome expressing MamC fused with organophosphohydrolase (OPD) from of Flavobacterium sp., were used for the degradation of paraoxon [103].
Figure 9 Schematic representation of a functionalized magnetosome according to each application described in the Biotechnology section of this review (cell separation; hyperthermia, drug delivery, image contrast, food analysis, enzyme immobilization and bioremediation and DNA and antigen recovery/detection). Drug delivery: the association between the surface proteins of the magnetosome and doxorubicin (DOX), an anti-breast cancer drug [63]. Cell separation: the modified magnetosomes were bound to anti-murinic G Ig anti-CD19 and used for separating B-lymphocytes from peripheral blood cells [90]. Food sciences: a capture system with the magnetosome proteins fused using a cross-linking reagent bis(sulfosuccinimidyl) suberate (BS3) for attachment of antibodies to Salmonella and Vibrio species from food samples (e.g., milk, egg and pork) [76]. DNA/Antigen analysis: antibody-functionalized magnetosomes were used for immobilization of HBsAg (hepatitis B antigen) in human serum and enhancement of sensitivity of immunoassay [72]. Image contrast: magnetosomes with specific proteins bound to the surface with high affinity to target cells were used as superparamagnetic contrast agents for magnetic resonance imaging [117]. Hyperthermia: magnetosomes coated with poly-l-lysine (PLL) were used in hyperthermia [100]. Enzyme immobilization and bioremediation: magnetosome expressing MamC fused with organophosphohydrolase (OPD) from of Flavobacterium sp., were used for the degradation of paraoxon [103].CC BY · PubMed Central

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Metadata

Authors
Vargas, G., Cypriano, J., Correa, T., Leão, P., Bazylinski, D. A., & Abreu, F.
Affiliations
  • Universidade Federal do Rio de Janeiro (BR)
  • Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Avenida Carlos Chagas Filho, 373, CCS, UFRJ, Rio de Janeiro, RJ 21941-902, Brazil
  • University of Nevada, Las Vegas (US)
Corresponding author
Abreu, Fernanda
ORCID
Venue
Molecules
Publisher
MDPI AG
Published
2018-09-24
Volume
23
Issue
10
Pages
2438
ISSN
1420-3049 (ISSN-L)
DOI
10.3390/molecules23102438
PMC
PMC6222368
OpenAlex
W2890606087
Cited by
180
References
0
Citations by year
2026: 16 · 2025: 21 · 2024: 15 · 2023: 26 · 2022: 29 · 2021: 35 · 2020: 32 · 2019: 5 · 2018: 1
FWCI
1.79
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecules (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Digital Scholarship - UNLV (University of Nevada Reno) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation (EAR-1423939)
  • Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (233179, E_26/200.019/2017)
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (E_26/200.019/2017)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Geophysics › Geomagnetism and Paleomagnetism Studies
  • Physical Sciences › Materials Science › Materials Chemistry › Magnetic Properties and Synthesis of Ferrites
  • Physical Sciences › Engineering › Biomedical Engineering › Characterization and Applications of Magnetic Nanoparticles
Keywords
magnetotactic bacteria, magnetosomes, magnetite, greigite, biomineralization, magnetic nanoparticles, magnetic hyperthermia, drug delivery, bioremediation, cell isolation, DNA recovery, enzyme immobilization, MRI contrast enhancement
MeSH terms
Bacteria, Bacterial Proteins, Biotechnology, Iron, Sulfides, Ferrosoferric Oxide, Nanoparticles, Magnetosomes

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