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

Abstract

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.

Fig. 1.

Mass of iron per cell measured in AMB-1 populations cultivated at (A) 10, (B) 50, (C) 100, (D) 200, (E) 300 or (F) 500 μM of Fe(III).

Fig. 2.

Mass of iron per AMB-1 cell cultivated for two days versus initial Fe(III) concentration in the external medium. Each symbol represents the mean value of three replicates ± 1SD. The mass of iron per cell shows a logarithmic increase with higher iron concentration in AMB-1 growth medium (correlation coefficient of 0.92).

Fig. 3.

Magnetite length in AMB-1 versus (A) Initial Fe(III) concentration in the external medium and (B) mass of iron per cell. Each point corresponds to the mean value of two replicates ± 1SD. At least 300 magnetite nanoparticles corresponding to a given population were measured. Magnetite length shows logarithmic and exponential increase with Fe(III) concentration in the external medium (correlation coefficient of 0.97) and mass of iron per cell (correlation coefficient of 0.98), respectively.

Fig. 4.

Model indicating the main inputs of dissolved iron to the oceans (in red, data from ref. 29) and the fluxes of iron incorporation by magnetotactic bacteria (in blue, data from this study). All flux numbers are given in kg of iron pear year.