Phylogenetic and genomic insights into magnetosome biomineralization in magnetotactic Alphaproteobacteria

Magnetotactic bacteria (MTB) biomineralize intracellular, membrane-enclosed magnetite or greigite nanocrystals (magnetosomes). How magnetosome gene clusters (MGCs) control magnetosome morphology and evolve across lineages remains central to reconstructing the history of magnetotaxis. Here, we report five uncultured MTB strains from Yuyuantan Lake (Beijing, China), all within Rhodospirillales order (Alphaproteobacteria class). Using phylogenetics, fluorescence in situ hybridization-scanning electron microscopy, and transmission electron microscopy, we show that magnetosome morphology is more strongly constrained by phylogeny than by cell morphology. Whole-genome comparisons and MGC phylogenies indicate that vertical inheritance predominates at the genus level, whereas topological incongruences reveal additional processes, notably horizontal transfer and gene duplication. In particular, the presence of a canonical mamAB operon together with a duplicated mamAB-2 cluster supports inter-genus horizontal gene transfer between Magnetospirillum and Paramagnetospirillum. These findings refine evolutionary models by showing that conserved MGC architectures provide a stable scaffold for magnetosome biomineralization while permitting diversification within the Alphaproteobacteria class.IMPORTANCEMagnetotactic bacteria (MTB) build intracellular magnetic nanoparticles (magnetosomes) that guide navigation and influence biogeochemical cycling. Yet how the underlying genes map onto ancestry and crystal shape remains unclear. Pairing quantitative crystal-morphology statistics with phylogenomic analysis for MTB from the Rhodospirillales order, we show that magnetosome traits carry a stronger phylogenetic signal than cell shape. Newly recovered uncultured strains broaden Paramagnetospirillum diversity, and a high-quality genome (YYTV-2) represents a novel species within the rarely studied Candidatus Magneticavibrio. Analyses of both the canonical mamAB operon and a duplicated mamAB-2 cluster indicate predominantly vertical inheritance, with horizontal transfer and gene duplication introducing modular variation. These results tighten genotype-mineral phenotype links, improving the interpretation of magnetofossils and MTB as indicators of environmental change.