Magnetotactic Bacteria (MTB) are a diverse, ubiquitous group of bacteria that navigate along the Earth's geomagnetic field in search of optimal environments with low or no oxygen. They achieve this by producing magnetosomes, organelles made up of magnetite or greigite typically enclosed in a lipid membrane. The process of magnetosome formation is extensively studied in two alpha-Proteobacterial species, known for their cubooctahedral magnetite crystals encased in lipid membranes. Alternatively, the synthesis mechanisms for tooth-shaped magnetosomes, believed to be the ancestral form of magnetosomes, remain largely unexplored. We used Desulfovibrio magneticus RS-1, a delta-Proteobacterium, as a model organism to understand the mechanisms of synthesizing magnetosomes in deeper branching MTB. This study has revealed that when RS-1 is cultivated in hydrogen-rich environments, magnetosomes fail to form, though iron uptake is not impacted. When hydrogen is substituted with nitrogen, the process of magnetite biomineralization begins and can be monitored with different techniques. We observe that early in the biomineralization cycle, cells predominantly contain equidimensional crystals, which later elongate and take on the distinctive tooth shape as the cycle progresses. Additionally, we discovered that chain formation occurs concurrently with biomineralization. Early in the cycle, cells possess one or a few crystals, while in later stages, they develop the typical long chains composed of several smaller sub-chains. Next, we pinpointed various genes and proteins that play roles in different stages of magnetosome synthesis through proteomic and genetic analyses. The findings show that magnetosomes extracted from cells at various stages of biomineralization contain different proportions of magnetosome proteins. MamA, MamB, MamEO, FmpA, FmpB, Mad4, and Mad10 are more abundant in the initial stages of biomineralization, while Mad20, Mad23, Mad28, and MamK are more abundant in the later stages of the process. Subsequently, we employed genetic techniques to investigate if these different cohorts of proteins have specific functions in magnetosome chain formation. Mutants of fmpA and fmpB exhibit significant disruptions in the early phases of magnetosome production and fail to develop into longer chains. Conversely, deletion mutants of mad10, mad20, mad23, mad25, mad26, mad28, and mamK exhibited a range of defects in the organization of the chains. Based on these results, we propose a model that RS-1 produces magnetosomes consecutively using the early biomineralization genes and actively transports these crystals to the positive curvature of the cell to construct a mature magnetosome chain. Notably, this method of chain organization is significantly different from that seen in alpha-Proteobacterial MTB. Our study highlights the shared as well as distinct evolutionary paths for magnetosome formation in deep-branching MTB. It also emphasizes the critical need for direct molecular genetic studies of magnetosome formation in diverse MTB model systems.