Physiological characteristics of Magnetospirillum gryphiswaldense MSR-1 that control cell growth under high-iron and low-oxygen conditions

Wang, Qing; Wang, Xu; Zhang, Weijia; Li, Xianyu; Zhou, Yuan; Li, Dan; Wang, Yinjia; Tian, Jie; Jiang, Wei; Zhang, Ziding; Peng, You-Liang; Wang, Lei; Li, Ying; Li, Jilun

doi:10.1038/s41598-017-03012-4

Cited by 15 publications

(15 citation statements)

References 45 publications

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“…Moreover, recent work on MSR-1 also suggested that iron can be contained outside magnetite in this strain ( 32 ). Iron-starving conditions can impact the iron cycling and homeostasis in MTB, as low-iron conditions have been shown to induce overexpression of iron acquisition systems in AMB-1 and MSR-1 ( 33 , 34 ). They might optimize the transfer of incorporated iron to magnetosomes for magnetite precipitation.…”

Section: Discussionmentioning

confidence: 99%

Magnetotactic Bacteria Accumulate a Large Pool of Iron Distinct from Their Magnetite Crystals

Amor

Ceballos

Wan

et al. 2020

Appl Environ Microbiol

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Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that form intracellular nanoparticles of magnetite (Fe3O4) or greigite (Fe3S4) in a genetically controlled manner. Magnetite and greigite synthesis requires MTB to transport a large amount of iron from the environment. Most intracellular iron was proposed to be contained within the crystals. However, recent mass spectrometry studies suggest that MTB may contain a large amount of iron that is not precipitated in crystals. Here, we attempt to resolve these discrepancies by performing chemical and magnetic assays to quantify the different iron pools in the magnetite-forming strain Magnetospirillum magneticum AMB-1, as well as mutant strains showing defects in crystal precipitation, cultivated at varying iron concentrations. All results show that magnetite represents at most 30 % of the total intracellular iron under our experimental conditions, and even less in the mutant strains. We further examined the iron speciation and subcellular localization in AMB-1 using the fluorescent indicator FIP-1 that is designed for detection of labile Fe(II). Staining with this probe suggests that unmineralized reduced iron is found in the cytoplasm and associated with magnetosomes. Our results demonstrate that, under our experimental conditions, AMB-1 is able to accumulate a large pool of iron distinct from magnetite. Finally, we discuss the biochemical and geochemical implications of these results. Importance Magnetotactic bacteria (MTB) produce iron-based intracellular magnetic crystals. They represent a model system for studying iron homeostasis and biomineralization in microorganisms. MTB sequester an important iron mass in their crystals, and have thus been proposed to significantly impact the iron biogeochemical cycle. Several studies proposed that MTB could also accumulate iron in a reservoir distinct from their crystals. Here, we present a chemical and magnetic methodology for quantifying the iron pools of iron in the magnetotactic strain AMB-1. Results showed that most of iron is not contained in crystals. We then adapted protocols for the fluorescent Fe(II) detection in bacteria, and showed that iron could be detected outside of crystals using fluorescence assays. This work suggests a more complex picture for iron homeostasis in MTB than previously thought. Because iron speciation controls and its fate in the environment, our results also provide important insights into the geochemical impact of MTB.

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Section: Discussionmentioning

confidence: 99%

Magnetotactic Bacteria Accumulate a Large Pool of Iron Distinct from Their Magnetite Crystals

Amor

Ceballos

Wan

et al. 2020

Appl Environ Microbiol

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“…Indeed, time‐course experiments require to first grow bacteria under iron‐starving conditions ( i.e . no iron provided to the growth medium), which trigger overexpression of iron transporters (Suzuki et al ., 2006; Wang et al ., 2017). This could optimize the transfer of iron to magnetosomes for magnetite precipitation, and prevent accumulation of iron in a reservoir distinct from magnetite.…”

Section: Iron Biomineralization In Mtbmentioning

confidence: 99%

Iron‐biomineralizing organelle in magnetotactic bacteria: function, synthesis and preservation in ancient rock samples

Amor

Mathon

Monteil

et al. 2020

Environmental Microbiology

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Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that incorporate iron from their environment to synthesize intracellular nanoparticles of magnetite (Fe 3 O 4) or greigite (Fe 3 S 4) in a genetically controlled manner. Magnetite and greigite magnetic phases allow MTB to swim towards redox transition zones where they thrive. MTB may represent some of the oldest microorganisms capable of synthesizing minerals on Earth and have been proposed to significantly impact the iron biogeochemical cycle by immobilizing soluble iron into crystals that subsequently fossilize in sedimentary rocks. In the present article, we describe the distribution of MTB in the environment and discuss the possible function of the magnetite and greigite nanoparticles. We then provide an overview of the chemical mechanisms leading to iron mineralization in MTB. Finally, we update the methods used for the detection of MTB crystals in sedimentary rocks and present their occurrences in the geological record.

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“…Moreover, most of the magnetotactic bacteria strains have been found to consume oxygen, ferric quinate, and nitrate as electron acceptors and use succinate or lactate, acetate, and nitrate as electron donors [11] . Culture medium optimization was very effective for high-yield cultivation of magnetosome, as it has previously been reported that at higher dissolved oxygen (DO) level, cell growth would be greater, but for higher yield of magnetosome, low DO concentrations are the prerequisite [23,24] . Thus, to resolve this situation, it is necessary to enhance DO to an optimum level by stirring the medium to increase the magnetotactic bacteria growth and allow the microbe to lower DO by the respiration process to an optimum level.…”

Section: Introuductionmentioning

confidence: 99%

Effects of Environmental Conditions on High-Yield Magnetosome Production by Magnetospirillum gryphiswaldense MSR-1

Jajan

Hosseini

Ghorbani

et al. 2019

ibj

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Background: Magnetotactic bacteria are a heterogeneous group of Gram-negative prokaryote cells that produce linear chains of magnetic particles called magnetosomes, intracellular organelles composed of magnetic iron particles. Many important applications have been defined for magnetic nanoparticles in biotechnology, such as cell separation applications, as well as acting as carriers of enzymes, antibodies, or anti-cancer drugs. Since the bacterial growth is difficult and the yield of magnetosome production is low, the application of magnetosome has not been developed on a commercial scale. Methods: Magnetospirillum gryphiswaldense strain MSR-1 was used in a modified current culture medium supplemented by different concentrations of oxygen, iron, carbon, and nitrogen, to increase the yield of magnetosomes. Results: Our improved MSR-1 culture medium increased magnetosome yield, magnetosome number per bacterial cell, magnetic response, and bacterial cell growth yield significantly. The yield of magnetosome increased approximately four times. The optimized culture medium containing 25 mM of Na-pyruvate, 40 mM of NaNO3, 200 µM of ferrous sulfate, and 5-10 ppm of dissolved oxygen (DO) resulted in 186.67 mg of magnetosome per liter of culture medium. The iron uptake increased significantly, and the magnetic response of the bacteria to the magnetic field was higher than threefold as compared to the previously reported procedures. Conclusion: This technique not only decreases the cultivation time but also reduces the production cost. In this modified method, the iron and DO are the major factors affecting the production of magnetosome by M. gryphiswaldense strain MSR-1. However, refining this technique will enable a further yield of magnetosome and cell density.

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Physiological characteristics of Magnetospirillum gryphiswaldense MSR-1 that control cell growth under high-iron and low-oxygen conditions

Cited by 15 publications

References 45 publications

Magnetotactic Bacteria Accumulate a Large Pool of Iron Distinct from Their Magnetite Crystals

Magnetotactic Bacteria Accumulate a Large Pool of Iron Distinct from Their Magnetite Crystals

Iron‐biomineralizing organelle in magnetotactic bacteria: function, synthesis and preservation in ancient rock samples

Effects of Environmental Conditions on High-Yield Magnetosome Production by Magnetospirillum gryphiswaldense MSR-1

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