Iron uptake and magnetite biomineralization in the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1: An iron isotope study

Amor, Matthieu; Busigny, Vincent; Louvat, Pascale; Tharaud, Mickaël; Gélabert, Alexandre; Cartigny, Pierre; Carlut, Julie; Isambert, Aude; Durand-Dubief, Mickaël; Ona-Nguéma, Georges; Alphandéry, Edouard; Chebbi, Imène; Guyot, François

doi:10.1016/j.gca.2018.04.020

Cited by 28 publications

(49 citation statements)

References 67 publications

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“…This fraction could correspond to iron associated with organic compounds that include proteins. Iron isotope work on MTB showed a specific enrichment in heavy isotopes of the iron fraction associated with these proteins (Amor et al ., , ), in good agreement with iron isotope data obtained from environments in which MTB populations were observed (Ilina et al ., ; Chen et al ., ). This suggests that MTB could control partly the dissolved iron isotope budget in the environment, and that iron isotopes could be used as a tool for probing iron released and/or precipitated by MTB.…”

Section: Resultssupporting

confidence: 89%

“…S1 and Table S1). This observation indicates that some bacterial iron could be lost during growth in culture, a finding in good agreement with previous studies that proposed Fe(II) diffusion between the bacterial internal medium and the external solution (Amor et al ., ). The maximum bacterial iron content was reached at 100 μM of iron in the initial external medium, with a mass of iron per cell of ~1 × 10 −6 ng per cell, and no increase in intracellular iron was observed for higher initial iron concentrations (Fig.…”

Section: Resultsmentioning

confidence: 97%

“…). The general picture of iron cycling in AMB‐1 suggests that iron is first transported to the additional iron pool, distinct from magnetite, before its precipitation in magnetosomes (Amor et al ., ). Our results are in good agreement with this model, as they indicate a delay in magnetite precipitation as iron incorporation in AMB‐1 increases.…”

Section: Resultsmentioning

confidence: 97%

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Single‐cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

Amor

Tharaud

Gélabert

et al. 2019

Environmental Microbiology

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Summary Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that mineralize dissolved iron into intracellular magnetic crystals. After cell death, these crystals are trapped into sediments that remove iron from the soluble pool. MTB may significantly impact the iron biogeochemical cycle, especially in the ocean where dissolved iron limits nitrogen fixation and primary productivity. A thorough assessment of their impact has been hampered by a lack of methodology to measure the amount of, and variability in, their intracellular iron content. We quantified the iron mass contained in single MTB cells of Magnetospirillum magneticum strain AMB‐1 using a time‐resolved inductively coupled plasma‐mass spectrometry methodology. Bacterial iron content depends on the external iron concentration, and reaches a maximum value of ~10−6 ng of iron per cell. From these results, we calculated the flux of dissolved iron incorporation into environmental MTB populations and conclude that MTB may mineralize a significant fraction of dissolved iron into crystals.

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Section: Resultssupporting

confidence: 89%

Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 97%

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Single‐cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

Amor

Tharaud

Gélabert

et al. 2019

Environmental Microbiology

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“…Interestingly, we also observed that only a minority of intracellular iron was in a crystallized form, suggesting that the majority of intra-cellular iron is not used for magnetosome synthesis. Over the whole growth, the maximum percentage of intracellular iron transformed in magnetosome chains (45%) is similar to that of 50% reported in one study (Amor et al, 2018) and lower than that of 99.5% reported in two other studies (Grünberg et al, 2004), suggesting that as in Amor et al, iron does not only serve for magnetosome formation but also for the overall metabolic activity of MTB (Naresh et al, 2012) or is stored in cells under other forms than magnetite (Amor et al, 2018). Furthermore, it is possible that the different results reported in Grünberg et al (2004) than in this study or Amor et al (2018) is due to the quantity of available iron in MTB growth medium, which is more important here and in Amor et al (2018) than in Grünberg et al (2004).…”

Section: Discussionsupporting

confidence: 87%

A Method for Producing Highly Pure Magnetosomes in Large Quantity for Medical Applications Using Magnetospirillum gryphiswaldense MSR-1 Magnetotactic Bacteria Amplified in Minimal Growth Media

Berny

Fèvre²,

Guyot

et al. 2020

Front. Bioeng. Biotechnol.

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We report the synthesis in large quantity of highly pure magnetosomes for medical applications. For that, magnetosomes are produced by MSR-1 Magnetospirillum gryphiswaldense magnetotactic bacteria using minimal growth media devoid of uncharacterized and toxic products prohibited by pharmaceutical regulation, i.e., yeast extract, heavy metals different from iron, and carcinogenic, mutagenic and reprotoxic agents. This method follows two steps, during which bacteria are first pre-amplified without producing magnetosomes and are then fed with an iron source to synthesize magnetosomes, yielding, after 50 h of growth, an equivalent OD 565 of ∼8 and 10 mg of magnetosomes in iron per liter of growth media. Compared with magnetosomes produced in non-minimal growth media, those particles have lower concentrations in metals other than iron. Very significant reduction or disappearance in magnetosome composition of zinc, manganese, barium, and aluminum are observed. This new synthesis method paves the way towards the production of magnetosomes for medical applications.

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“…6,13). Iron isotope studies of MTB suggested that a large fraction (~50%) of the total cellular iron could be located in a reservoir distinct from magnetite (14,15), such that the mass of magnetite in MTB cells is not an accurate estimate of the total mass of iron they contain. Estimation of total iron in MTB cells from measurement of total bacterial iron in a given population is also prone to biases.…”

Section: Significance Statementmentioning

confidence: 99%

Single-cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

Amor

Tharaud

Gélabert

et al. 2019

Preprint

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Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that biomineralize dissolved iron from the environment into intracellular nanoparticles of magnetite [Fe(II)Fe(III)2O4] or greigite [Fe(II)Fe(III)2S4] in a genetically controlled manner. After cell death, these magnetite and greigite crystals are trapped into sediments which effectively removes iron from the soluble pool. MTB may significantly impact the iron biogeochemical cycle, especially in the ocean where dissolved iron limits nitrogen fixation and primary productivity. Although MTB are ubiquitous in the environment, their impact on the biogeochemical cycling of metallic elements is still poorly constrained. A thorough assessment of the mass of iron incorporated by MTB has been hampered by a lack of methodology to accurately measure the amount of, and variability in, their intracellular iron content. Here, we quantify the mass of iron contained in single MTB cells of the model organism, Magnetospirillum magneticum sp. AMB-1, using a time-resolved mass spectrometry methodology. Bacterial iron content depends on the external iron concentration, and reaches a maximum value of 10-6 ng of iron per cell when bacteria are cultivated with initial iron concentrations of 100 μM or higher. From our experimental results, we calculated the flux of dissolved iron incorporation into natural MTB populations and conclude that MTB may mineralize a significant fraction of environmental dissolved iron into crystals.

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Iron uptake and magnetite biomineralization in the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1: An iron isotope study

Cited by 28 publications

References 67 publications

Single‐cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

Single‐cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

A Method for Producing Highly Pure Magnetosomes in Large Quantity for Medical Applications Using Magnetospirillum gryphiswaldense MSR-1 Magnetotactic Bacteria Amplified in Minimal Growth Media

Single-cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

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