Summary The magnetotactic lifestyle represents one of the most complex traits found in many bacteria from aquatic environments and depends on magnetic organelles, the magnetosomes. Genetic transfer of magnetosome biosynthesis operons to a non‐magnetotactic bacterium has only been reported once so far, but it is unclear whether this may also occur in other recipients. Besides magnetotactic species from freshwater, the genus Magnetospirillum of the Alphaproteobacteria also comprises a number of strains lacking magnetosomes, which are abundant in diverse microbial communities. Their close phylogenetic interrelationships raise the question whether the non‐magnetotactic magnetospirilla may have the potential to (re)gain a magnetotactic lifestyle upon acquisition of magnetosome gene clusters. Here, we studied the transfer of magnetosome gene operons into several non‐magnetotactic environmental magnetospirilla. Single‐step transfer of a compact vector harbouring >30 major magnetosome genes from M. gryphiswaldense induced magnetosome biosynthesis in a Magnetospirillum strain from a constructed wetland. However, the resulting magnetic cellular alignment was insufficient for efficient magnetotaxis under conditions mimicking the weak geomagnetic field. Our work provides insights into possible evolutionary scenarios and potential limitations for the dissemination of magnetotaxis by horizontal gene transfer and expands the range of foreign recipients that can be genetically magnetized.

Magnetotactic bacteria are widely represented microorganisms that have the ability to synthesize magnetosomes. The magnetotactic cocci of the order Magnetococcales are the most frequently identified, but their classification remains unclear due to the low number of cultivated representatives. This paper reports the analysis of an uncultivated magnetotactic coccus UR-1 collected from the Uda River (in eastern Siberia). Genome analyses of this bacterium and comparison to the available Magnetococcales genomes identified a novel species called “Ca. Magnetaquicoccus inordinatus,” and a delineated candidate family “Ca. Magnetaquicoccaceae” within the order Magnetococcales is proposed. We used average amino acid identity values <55–56% and <64–65% as thresholds for the separation of families and genera, respectively, within the order Magnetococcales. Analyses of the genome sequence of UR-1 revealed a potential ability for a chemolithoautotrophic lifestyle, with the oxidation of a reduced sulfur compound and carbon assimilation by rTCA. A nearly complete magnetosome genome island, containing a set of mam and mms genes, was also identified. Further comparative analyses of the magnetosome genes showed vertical inheritance as well as horizontal gene transfer as the evolutionary drivers of magnetosome biomineralization genes in strains of the order Magnetococcales.