OxyR controls magnetosome formation by regulating magnetosome island (MAI) genes, iron metabolism, and redox state

Abstract

Magnetospirillum gryphiswaldense MSR-1 uses chains of magnetosomes, membrane-enveloped magnetite (Fe(II)Fe(III)2O4) nanocrystals, to align along magnetic field. The process of magnetosome biomineralization requires a precise biological control of redox conditions to maintain a balanced amounts of ferric and ferrous iron. Here, we identified functions of the global regulator OxyR (MGMSRv2_4250, OxyR-4250) in MSR-1 during magnetosome formation. OxyR deletion mutant ΔoxyR-4250 displayed reduced magnetic response, and increased levels of intracellular ROS (reactive oxygen species). OxyR-4250 protein upregulated expression of six antioxidant genes (ahpC1, ahpC2, katE, katG, sodB, trxA), four iron metabolism-related regulator genes (fur, irrA, irrB, irrC), a bacterioferritin gene (bfr), and a DNA protection gene (dps). OxyR-4250 was shown, for the first time, to directly regulate magnetosome island (MAI) genes mamGFDC, mamXY, and feoAB1 operons. Taken together, our findings indicate that OxyR-4250 helps maintain a proper redox environment for magnetosome formation by eliminating excess ROS, regulating iron homeostasis and participating in regulation of Fe2+/Fe3+ ratio within the magnetosome vesicle through regulating MAI genes.