Comparative transcriptomic analysis of Stenotrophomonas sp. MNB17 revealed mechanisms of manganese tolerance at different concentrations and the role of histidine biosynthesis in manganese removal.

Bacteria possess protective mechanisms against excess Mn(Ⅱ) to reduce its toxicity. Stenotrophomonas sp. MNB17 showed high Mn(Ⅱ) removal capacity (92.24–99.16 %) by forming Mn-precipitates (MnCO 3 and Mn-oxides), whose Mn-oxides content increased with increasing Mn(Ⅱ) concentrations (10–50 mM). Compared with 0 mM Mn(Ⅱ)-stressed cells, transcriptomic analysis identified genes with the same transcriptional trends in 10 mM and 50 mM Mn(Ⅱ)-stressed cells, including genes involved in metal transport, cell envelope homeostasis, and histidine biosynthesis, as well as genes with different transcriptional trends, such as those involved in oxidative stress response, glyoxylate cycle, electron transport, and protein metabolism. The upregulation of histidine biosynthesis and oxidative stress responses were the most prominent features of these metabolisms under Mn(Ⅱ) stress. We confirmed that the increased level of reactive oxygen species was one of the reasons for the increased Mn-oxides formation at high Mn(Ⅱ) concentrations. Metabolite analysis indicated that the enhanced histidine biosynthesis rather than the tricarboxylic acid cycle resulted in an elevated level of α-ketoglutarate, which helped eliminate reactive oxygen species. Consistent with these results, the exogenous addition of histidine significantly reduced the production of reactive oxygen species and Mn-oxides and enhanced the removal of Mn(Ⅱ) as MnCO 3. This study is the first to correlate histidine biosynthesis, reactive oxygen species, and Mn-oxides formation at high Mn(Ⅱ) concentrations, providing novel insights into the molecular regulatory mechanisms associated with Mn(Ⅱ) removal in bacteria. • Strain MNB17 strain handles increased Mn(Ⅱ) stress by producing more Mn-oxides. • Reactive oxygen species contribute to the Mn-oxides generation. • Mn(Ⅱ) stress induces significant upregulation of histidine biosynthesis in MNB17. • Strain MNB17 diverts histidine towards α-ketoglutarate to combat oxidative stress. • Exogenous histidine reduces Mn-oxides formation and promotes Mn(Ⅱ) removal as MnCO 3. [ABSTRACT FROM AUTHOR]