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Magnetotactic Bacteria Accumulate a Large Pool of Iron Distinct bioRxiv preprint doi: https://doi.org/10.1101/2020.03.10.986679; this version posted March 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Magnetotactic bacteria accumulate a large pool of iron distinct 2 from their magnetite crystals 3 4 Matthieu Amor1*, Alejandro Ceballos2, Juan Wan1, Christian P. Simon3, Allegra T. Aron4,5,6, 5 Christopher J. Chang4,7, Frances Hellman2,3,8, Arash Komeili1,7 6 7 1 Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720-3102 8 2 Department of Materials Science and Engineering, University of California, Berkeley, California 9 94720 10 3 Department of Physics, University of California, Berkeley, California 94720 11 4 Department of Chemistry, University of California, Berkeley, CA 94720 12 5 Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, La 13 Jolla, CA 92093, USA 14 6 Collaborative Mass Spectrometry Innovation Center, University of California, San Diego, La Jolla, 15 CA 92093, USA 16 7 Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3200 17 8 Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 18 19 20 * Present address: CNRS, CEA, Aix-Marseille Université, UMR7265 Biosciences and 21 Biotechnologies Institute of Aix-Marseille, Saint Paul lez Durance, France. 22 Corresponding authors: [email protected] (MA); [email protected] (AK) 23 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.10.986679; this version posted March 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 24 Abstract 25 Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that form intracellular 26 nanoparticles of magnetite (Fe3O4) or greigite (Fe3S4) in a genetically controlled manner. 27 Magnetite and greigite synthesis requires MTB to transport a large amount of iron from the 28 environment which is subsequently concentrated in organelles called magnetosomes for 29 crystal precipitation and maturation. X-ray absorption analysis of MTB suggests that the 30 intracellular iron is mainly contained within the crystals, thus preventing potential toxic 31 effects of free iron. In contrast, recent mass spectrometry studies suggest that MTB may 32 contain a large amount of iron that is not precipitated in crystals. Here, we attempt to resolve 33 these descrepancies by performing chemical and magnetic assays to quantify the different iron 34 pools in the magnetite-forming strain Magnetospirillum magneticum AMB-1 cultivated at 35 varying iron concentrations. AMB-1 mutants showing defects in crystal precipitation were 36 also characterized following the same approach. All results show that magnetite represents at 37 most 30 % of the total intracellular iron under our experimental conditions. We further 38 examined the iron speciation and subcellular localization in AMB-1 using the fluorescent 39 indicator FIP-1 that is designed for detection of labile Fe(II). Staining with this probe suggests 40 that unmineralized reduced iron is found in the cytoplasm and associated with magnetosomes. 41 Our results demonstrate that, under our experimental conditions, AMB-1 is able to 42 accumulate a large pool of iron distinct from magnetite. Finally, we discuss the biochemical 43 and geochemical implications of these results. 44 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.10.986679; this version posted March 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 45 Importance 46 Magnetotactic bacteria (MTB) are a group of microorganisms producing iron-based 47 intracellular magnetic crystals. They represent a model system for studying iron homeostasis 48 and biomineralization in bacteria. MTB contain an important mass of iron, about 10 to 100 49 higher than other bacterial model such as Escherichia coli, suggesting efficient iron uptake 50 and storage systems. Accordingly, MTB have been proposed to significantly impact the iron 51 biogeochemical cycle in sequestering a large amount of soluble iron into crystals. Recently, 52 several studies proposed that MTB could also accumulate iron in a reservoir distinct from 53 their crystals. Here, we present a chemical and magnetic methodology for quantifying the 54 fraction of the total cellular iron contained in the magnetic crystals of the magnetotactic strain 55 Magnetospirillum magneticum AMB-1. Comparison of the mass of iron contained in the 56 different cellular pools showed that most of the bacterial iron is not contained in AMB-1 57 crystals. We then adapted protocols for the fluorescent detection of Fe(II) in bacteria, and 58 showed that iron could be detected outside of crystals using fluorescence assays. This work 59 suggests a more complex picture for iron homeostasis in MTB than previously thought. 60 Because iron speciation controls its solubility, our results also provide important insights into 61 the geochemical impact of MTB. A large pool of unmineralized iron in MTB could be more 62 easily released in the environment than magnetite, thus limiting iron sequestration into MTB 63 crystals. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.10.986679; this version posted March 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 64 Introduction 65 Many living organisms transform inorganic molecules into crystalline structures in a process 66 called biomineralization. Magnetotactic bacteria (MTB) represent an elegant example of such 67 organisms. They incorporate dissolved iron from their environment and precipitate it as 68 magnetite [Fe(II)Fe(III)2O4] or greigite [Fe(II)Fe(III)2S4] nanoparticles in organelles called 69 magnetosomes (Uebe and Schüler, 2016). MTB are ubiquitous gram-negative 70 microorganisms in aquatic environments. They inhabit the oxic/anoxic transition zones in the 71 water column or sediments where they thrive (Kopp and Kirschvink, 2008). In MTB, 72 magnetosomes are aligned as chains inside the cell, and provide the bacteria with a permanent 73 magnetic dipole presumably for navigation purposes (Uebe and Schüler, 2016). 74 Tremendous work has been carried out to determine the biological and chemical reactions 75 leading to magnetite synthesis in MTB (McCausland and Komeili, 2020). In the two best- 76 studied, magnetite-forming strains Magnetospirillum magneticum AMB-1 and 77 Magnetospirillum gryphiswaldense MSR-1, magnetosome formation is a genetically- 78 controlled process where: (i) magnetosome vesicles are formed from invagination of the inner 79 cell membrane, (ii) empty magnetosome vesicles are aligned as a chain inside the cell, (iii) 80 iron is transported and concentrated into magnetosome for initiation of biomineralization, and 81 (iv) crystal size and shape are precisely controlled in a species-specific manner. A set of ~30 82 genes, located in a distinct portion of the genome called the magnetosome island (MAI), is 83 required and sufficient for the step-wise formation of magnetosomes (Murat et al, 2010). 84 Recently, iron isotope studies have provided an integrative model for iron uptake and 85 precipitation as magnetite in the magnetotactic strain AMB-1 (Amor et al, 2016, 2018). This 86 model assumes that dissolved Fe(II) or Fe(III) species are incorporated into AMB-1 and 87 stored in the cytoplasm and/or periplasm as Fe(III). This Fe(III) pool is then partially reduced 88 into Fe(II) for trafficking to magnetosomes, and oxidized for precipitation as magnetite 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.10.986679; this version posted March 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 89 (Amor et al, 2018). Direct mass spectrometry measurements of iron content and iron isotope 90 composition in AMB-1 cells devoid of magnetosomes suggests that a large pool of iron, 91 which could represent at least 50% of the total cellular iron, accumulate in reservoir(s) 92 distinct from magnetite (Amor et al, 2016, 2018). The above-mentioned high-resolution mass 93 spectrometry measurements of iron showed discrepancy with previous X-ray absorption 94 analyses performed on both AMB-1 and MSR-1 strains, in which magnetite was the sole iron 95 species detected at the end of the biomineralization process (Baumgartner et al, 2013; Fdez- 96 Gubieda et al, 2013). 97 In the present work, we address the discrepancy between the mass spectrometry and X-ray 98 absorption experiments by determining the distribution of iron in AMB-1 cells. We grew 99 AMB-1 with different iron concentrations, and measured the mass of iron taken up by the 100 bacteria using chemical assays. Cells were then recovered and the mass of iron contained in 101 magnetite was quantified from magnetic characterizations. From these experimental results, 102 we found that magnetite represents ~25 to ~30% of the bulk cellular iron. Additional cultures 103 of AMB-1 were grown to determine the total mass of iron contained in magnetite at the scale 104 of a bacterial population. Simultaneous cell counting allowed us to estimate the mean mass of 105 magnetite per cell. Comparison of these results with published single-cell quantification of 106 bulk iron in AMB-1 supported mass balance estimations.
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