Magnetosomes eliminate intracellular reactive oxygen species in Magnetospirillum gryphiswaldense MSR‐1

Abstract

Magnetotactic bacteria synthesize magnetic particles called magnetosomes that cause them to orient to their external magnetic fields. However, the physiological significance and other possible functions of these magnetosomes have not been explored in detail. In this study, we have investigated the biological functions of magnetosomes with respect to their ability to scavenge reactive oxygen species (ROS) in Magnetospirillum gryphiswaldense MSR-1. To assess the changes in ROS levels under different conditions, cells were cultured under aerobic or micro-aerobic conditions in medium containing high and low amounts of iron. To ensure that the observed results were not due to nonspecific interactions, reactions were carried out using a mutant deficient in synthesizing magnetite (mamO-deficient mutant), its complementary strain or the wild-type MSR-1. We observed that the levels of intercellular ROS under micro-aerobic conditions with high-iron medium were much higher when the non-synthetic Fe(3) O(4) crystals mutant Mu21-415 was employed for the assay, compared with the wild-type or complementary strain, or when conditions were aerobic with low-iron medium. These results indicated that magnetosomes function in the scavenging of intracellular ROS. Furthermore, we have demonstrated that the magnetosomes exhibit peroxidase-like properties, by using the earlier reported in vitro horseradish peroxidase assay for artificial magnetic nanoparticles. In addition to possessing peroxidase-like activity, the magnetosomes also exhibited a more enzymatic kinetic response, suggesting that proteins on the membranes of the magnetosomes likely contribute to the enzymatic activity. This is the first study to demonstrate that magnetosomes play an important role in decreasing or eliminating ROS.

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

“…Indeed, cells of Magnetovibrio blakemorei were shown to produce magnetosomes even when the major source of iron is omitted from the growth medium, thereby starving themselves of iron and limiting their growth yield. It was recently shown that magnetite magnetosomes scavenge reactive oxygen species in Magnetospirillum gryphiswaldense and exhibit peroxidase-like activities (77). In terms of evolution, cells likely took up a great deal of iron for some unknown reason before magnetosomes had developed, perhaps for energy conservation (e.g., formation of ATP) during iron reduction where Fe 3ϩ serves as the electron acceptor, for oxidation where Fe 2ϩ serves as the electron donor, or for both.…”

Magnetosomes extracted from Magnetospirillum magneticum strain AMB-1 showed enhanced peroxidase-like activity under visible-light irradiation

“…This response is independent of wavelength and magnetotaxis, but the mechanism of phototaxis in AMB-1 is still not well understood. Guo et al showed that magnetosomes can eliminate intracellular ROS depending on peroxidase activity exhibited by Fe 3 O 4 crystals [7]. Therefore, in this study, we investigated the peroxidase-like activity of magnetosomes extracted from M. magneticum strain AMB-1 with or without visible-light irradiation compared with that of HRP, ferric/ferrous ions, and naked magnetosomes to elucidate phototaxis mechanisms of MTB.…”

“…Moreover, magnetosomes reportedly play a role in iron storage [4] and/or in eliminating the toxicity of free iron in a cell, which leads to the production of toxic radicals because of the Fenton reaction [5,6]. Magnetosomes can also scavenge reactive oxygen species (ROS) [7].…”

The Bacterial Magnetosome: A Unique Prokaryotic Organelle

“…It seems logical that there are physiological reasons for magnetosome biomineralization (e.g. detoxification of free iron ions in the cell; decomposition of toxic oxygen radicals produced during respiration such as hydrogen peroxide [Blakemore, 1982;Guo et al, 2012]) but, to date, any convincing physiological link remains elusive.…”