The MagA Protein of Magnetospirilla Is Not Involved in Bacterial Magnetite Biomineralization

Abstract

Magnetotactic bacteria have the ability to orient along geomagnetic field lines based on the formation of magnetosomes, which are intracellular nanometer-sized, membrane-enclosed magnetic iron minerals. The formation of these unique bacterial organelles involves several processes, such as cytoplasmic membrane invagination and magnetosome vesicle formation, the accumulation of iron in the vesicles, and the crystallization of magnetite. Previous studies suggested that the magA gene encodes a magnetosome-directed ferrous iron transporter with a supposedly essential function for magnetosome formation in Magnetospirillum magneticum AMB-1 that may cause magnetite biomineralization if expressed in mammalian cells. However, more recent studies failed to detect the MagA protein among polypeptides associated with the magnetosome membrane and did not identify magA within the magnetosome island, a conserved genomic region that is essential for magnetosome formation in magnetotactic bacteria. This raised increasing doubts about the presumptive role of magA in bacterial magnetosome formation, which prompted us to reassess MagA function by targeted deletion in Magnetospirillum magneticum AMB-1 and Magnetospirillum gryphiswaldense MSR-1. Contrary to previous reports, magA mutants of both strains still were able to form wild-type-like magnetosomes and had no obvious growth defects. This unambiguously shows that magA is not involved in magnetosome formation in magnetotactic bacteria.

MS-1 magA

“…Although it is tempting to suggest that this could be related to magA ’s function as an iron transporter, leading to more iron uptake and consequently an increase in FTH1 translation, recent evidence suggests that magA is not only unnecessary for magnetosome formation in MTBs but also unlikely to work as an iron transporter. 30 It is now known that iron is not the only regulator of ferritin translation and that other signals, including oxidative stress, can lead to increases in ferritin protein. 32 Considering our observations with stem cells, which did not tolerate the expression of magA , it is reasonable to suggest that magA expression in HEK cells might also lead to changes in homeostasis with one of the consequences being an increase in FTH1 translation.…”

Biophysical features of MagA expression in mammalian cells: implications for MRI contrast

“…Although not an essential magnetosome gene (Uebe et al, 2012), we showed that overexpression of MagA from AMB-1 provides MR contrast comparable to the overexpression of modified, mammalian ferritin subunits ( HF + LF ) that are devoid of iron regulatory elements (Rohani et al, 2013). In a mouse model of tumor growth, transplanted cells were repetitively imaged over 5 weeks and compared to the parental cell xenograft.…”

CHAPTER 11. Magnetic Resonance‐Based Cell Imaging Using Contrast Media and Reporter Genes

“…142 However, magA as a putative MR reporter gene is rather controversial as its implication in magnetosome formation has recently been contested. 169 A second magnetosome gene, Mms6, is being explored as a reporter for MRI contrast. 170 The Mms6 protein has a high affinity for iron proteins 171 and plays a critical role in the crystallization of magnetite within magnetosomes, most probably in controlling the magnetite crystal morphology.…”