Single-cell genomics reveals potential for magnetite and greigite biomineralization in an uncultivated multicellular magnetotactic prokaryote

Abstract

For magnetic orientation, magnetotactic bacteria biosynthesize magnetosomes, which consist of membrane-enveloped magnetic nanocrystals of either magnetite (Fe3O4) or greigite (Fe3S4). While magnetite formation is increasingly well understood, much less is known about the genetic control of greigite biomineralization. Recently, two related yet distinct sets of magnetosome genes were discovered in a cultivated magnetotactic deltaproteobacterium capable of synthesizing either magnetite or greigite, or both minerals. This led to the conclusion that greigite and magnetite magnetosomes are synthesized by separate biomineralization pathways. Although magnetosomes of both mineral types co-occurred in uncultured multicellular magnetotactic prokaryotes (MMPs), so far only one type of magnetosome genes could be identified in the available genome data. The MMP CandidatusMagnetomorum strain HK-1 from coastal tidal sand flats of the North Sea (Germany) was analysed by a targeted single-cell approach. The draft genome assembly resulted in a size of 14.3 Mb and an estimated completeness of 95%. In addition to genomic features consistent with a sulfate-reducing lifestyle, we identified numerous genes putatively involved in magnetosome biosynthesis. Remarkably, most mam orthologues were present in two paralogous copies with highest similarity to either magnetite or greigite type magnetosome genes, supporting the ability to synthesize magnetite and greigite magnetosomes.