Abstract
Bacterial non-enzymatic Mn(II) oxidation involving reactive oxygen species (ROS) (i.e., indirect oxidation), initially discovered from a marine alpha-proteobacterium, is believed to be of importance in controlling biogeochemical cycles. For soil-borne bacteria, however, evidence of indirect Mn(II) oxidation remains unclear. In this study, the indirect Mn(II) oxidation was evidenced in a soil-borne bacterium, Providencia sp. LLDRA6. First, with and without 50mM of Mn(II) exposure for LLDRA6, 300 differentially expressed genes were found to be linked to Mn(II) exposure via transcriptome sequencing. Among them, an operon, responsible for phenylacetic acid catabolism, was sharply upregulated in transcription, drawing us a special attention, since its transcriptional upregulation has recently shown to be important for withstanding ROS. Next, a fluorometric probe, 2',7'-Dichlorofluorescin diacetate (DCFDA), was used to qualitatively detect ROS from cells, showing a distinct increase in fluorescence intensities of ROS during Mn(II) exposure. Furthermore, concentrations of superoxide and hydrogen peroxide from cells were detected, respectively, with and without Mn(II) exposure, exhibiting that when Mn(II) oxidation occurred, superoxide concentration significantly increased but hydrogen peroxide concentration significantly decreased. Particularly, superoxide produced by LLDRA6 was proven to be the oxidant for Mn(II) in the formation of Mn oxides. Finally, we predicted links between phenylacetic acid metabolism pathway and ROS during Mn(II) exposure, proposing that the excessive ROS, generated in response to Mn(II) exposure, transcriptionally activate phenylacetic acid catabolism presumably by increasing concentrations of highly reactive oxepins.
Highlights
The oxidation of soluble Mn(II) to insoluble Mn(III/IV) minerals plays a critical role in global biogeochemical cycles, greatly affecting the fate and transport of trace elements, the cycling of carbon-based nutrients, and the activity of microbial metabolisms (Learman et al 2011a)
LLDRA6 exploited the indirect Mn(II) oxidation strategy of production coupled to H2O2 consumption to form Mn oxides
According to the detailed information from catabolic pathway of phenylacetic acid (PAA) in aerobic bacteria as reported by Teufel et al (2010), we find that the crucial process for degrading the inert aromatic ring of PAA, is the introduction of an oxygen atom into the aromatic ring catalyzed by the multicomponent enzyme PaaABCDE, and the subsequent formation of a highly reactive oxygen-containing, seven-member heterocycle catalyzed by PaaG (Fig. 6)
Summary
The oxidation of soluble Mn(II) to insoluble Mn(III/IV) minerals plays a critical role in global biogeochemical cycles, greatly affecting the fate and transport of trace elements, the cycling of carbon-based nutrients, and the activity of microbial metabolisms (Learman et al 2011a). Over 30 different types of Mn (oxyhydr) oxides (hereon Mn oxides), with layered or tunnel structures, occur in a wide variety of environmental settings from oceans to soils (Hens et al 2018). These ubiquitous minerals exhibit high binding affinity to metal ions because of their large surface-to-volume porous structure, and are often used as one of the strongest metal scavengers in the environment (Butterfield et al 2016). In the absence of oxygen, Mn oxides (e.g., MnO2) can be terminal electron acceptors, supporting the respiration and growth of certain anaerobic Mn-reductive bacteria (Henkel et al 2019)
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