Isolation and cultivation of a novel sulfate-reducing magnetotactic bacterium belonging to the genus Desulfovibrio

Hirokazu Shimoshige,Akira Inoue,Toru Mizuki,Shigeru Shimamura,Toru Maekawa,Hideki Kobayashi,Inês A Cardoso Pereira

doi:10.1371/journal.pone.0248313

Hirokazu Shimoshige, Akira Inoue + Show 5 more

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https://doi.org/10.1371/journal.pone.0248313

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Abstract

Magnetotactic bacteria (MTB) synthesize magnetosomes composed of membrane-enveloped magnetite (Fe3O4) and/or greigite (Fe3S4) nanoparticles in the cells. It is known that the magnetotactic Deltaproteobacteria are ubiquitous and inhabit worldwide in the sediments of freshwater and marine environments. Mostly known MTB belonging to the Deltaproteobacteria are dissimilatory sulfate-reducing bacteria that biomineralize bullet-shaped magnetite nanoparticles, but only a few axenic cultures have been obtained so far. Here, we report the isolation, cultivation and characterization of a dissimilatory sulfate-reducing magnetotactic bacterium, which we designate “strain FSS-1”. We found that the strain FSS-1 is a strict anaerobe and uses casamino acids as electron donors and sulfate as an electron acceptor to reduce sulfate to hydrogen sulfide. The strain FSS-1 produced bullet-shaped magnetite nanoparticles in the cells and responded to external magnetic fields. On the basis of 16S rRNA gene sequence analysis, the strain FSS-1 is a member of the genus Desulfovibrio, showing a 96.7% sequence similarity to Desulfovibrio putealis strain B7-43T. Futhermore, the magnetosome gene cluster of strain FSS-1 was different from that of Desulfovibrio magneticus strain RS-1. Thus, the strain FSS-1 is considered to be a novel sulfate-reducing magnetotactic bacterium belonging to the genus Desulfovibrio.

Highlights

Magnetotactic bacteria (MTB) are Gram-negative prokaryotes that synthesize intracellular magnetic nanoparticles named magnetosomes
Strain WYHR-1 is a magnetotactic deltaproteobacterium that produces bullet-shaped magnetite nanoparticles, the crystal morphology of which is quite different from that of the magnetite nanoparticles produced by Deltaproteobacteria and magnetotactic Nitrospirae [20]
The MTB enriched by the MTB trap device were inoculated in screw-capped glass culture tubes as follows; (i) The screw-capped glass culture tubes were filled up to approximately 66% of their volume with the MD medium, which was bubbled with 100% O2 free-N2 gas for 5 min and autoclaved; (ii) After having autoclaved the medium, 0.5 ml/liter of a sterile anaerobic stock of vitamin solution [46], 5.6 ml/liter of a sterile anaerobic stock of 0.25 mM KHPO4 buffer, 5.0 ml/liter of a sterile anaerobic stock of 10 mM ferric quinate, and 0.4 g/liter of freshly made neutralized and filter sterilized cysteineHClH2O were added to the medium; (iii) Strain FSS-1 was incubated in the MD medium at 28 ̊C in dim light

Summary

Introduction

Magnetotactic bacteria (MTB) are Gram-negative prokaryotes that synthesize intracellular magnetic nanoparticles named magnetosomes. Known MTB are affiliated with the Alphaproteobacteria, Gammaproteobacteria, Deltaproteobacteria and Etaproteobacteria classes of the Proteobacteria phylum, and with the Nitrospirae and “Candidatus Omnitrophica” phyla [1, 9–. MTB belonging to the Deltaproteobacteria class are known to synthesize bullet-shaped magnetite and/or pleomorphic greigite within the same cells [3, 5, 13]. Magnetotactic Deltaproteobacteria are located close to the root of the phylogenetic tree of the Proteobacteria, which synthesize only bullet-shaped magnetite [5]. The bullet-shaped magnetite nanoparticles have attracted a lot of attention from microbiological and geological researchers since the magnetotactic Deltaproteobacteria generally synthesize a large number of magnetite nanoparticles in each cell, which contributes to sedimentary magnetization [27, 28]

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