Manganese-Oxidizing Antarctic Bacteria (Mn-Oxb) Release Reactive Oxygen Species (ROS) as Secondary Mn(II) Oxidation Mechanisms to Avoid Toxicity

SIMPLE SUMMARY: Manganese (Mn)-oxidizing bacteria (MnOxb) are an essential group of microorganisms that oxidize soluble Mn(II) to form precipitate Mn(III) minerals, playing a crucial role in soil formation. The Fildes Peninsula is one of the fastest-warming areas globally and, therefore, the maritime Antarctic soils from this pivotal location allow for the examination of the effect of temperature on bacterial communities. The temperature causes an increase in the microbial respiratory rate, producing reactive oxygen species (ROS), which are harmful to bacteria. We evaluate an evasive secondary non-enzymatic mechanism for ROS production under increasing temperature in MnOxb isolated from Antarctic soils. Bacteria produce ROS capable of oxidizing Mn(II) as temperature increases, contributing to the enzymatic pathway protecting microbial cells from Mn(II) toxicity. In addition, we determine that certain strains, such as Arthobacter oxydans, can use these ROS as mechanisms to protect themselves from Mn toxicity at high concentrations. In conclusion, we describe a secondary mechanism of Mn(II) oxidation in bacterial strains of Antarctic soils. ABSTRACT: Manganese (Mn) oxidation is performed through oxidative Mn-oxidizing bacteria (MnOxb) as the main bio-weathering mechanism for Mn(III/IV) deposits during soil formation. However, with an increase in temperature, the respiration rate also increases, producing Reactive Oxygen Species (ROS) as by-products, which are harmful to microbial cells. We hypothesize that bacterial ROS oxidize Mn(II) to Mn(III/IV) as a secondary non-enzymatic temperature-dependent mechanism for cell protection. Fourteen MnOxb were isolated from Antarctic soils under the global warming effect, and peroxidase (PO) activity, ROS, and Mn(III/IV) production were evaluated for 120 h of incubation at 4 °C, 15 °C, and 30 °C. ROS contributions to Mn oxidation were evaluated in Arthrobacter oxydans under antioxidant (Trolox) and ROS-stimulated (menadione) conditions. The Mn(III/IV) concentration increased with temperature and positively correlated with ROS production. ROS scavenging with Trolox depleted the Mn oxidation, and ROS-stimulant increased the Mn precipitation in A. oxydans. Increasing the Mn(II) concentration caused a reduction in the membrane potential and bacterial viability, which resulted in Mn precipitation on the bacteria surface. In conclusion, bacterial ROS production serves as a complementary non-enzymatic temperature-dependent mechanism for Mn(II) oxidation as a response in warming environments.