Algae promotes the biogenic oxidation of Mn(II) by accelerated extracellular superoxide production.

ABSTRACT

Microbial manganese (Mn) oxidation, predominantly occurs within the anaerobic-aerobic interfaces, plays an important role in environmental pollution remediation. The anaerobic-aerobic transition zones, notably riparian and lakeside zones, are hotspots for algae-bacteria interactions. Here, we adopted a Mn(II)-oxidizing bacterium Pseudomonas sp. QJX-1 to investigate the impact of algae on microbial Mn(II) oxidation and verify the underlying mechanisms. Interestingly, we achieved a remarkable enhancement in bacterial Mn(II)-oxidizing activity within the algae-bacteria co-culture, despite the inability to oxidize Mn(II) for the algae used in this study. In addition, the bacterial density almost remains constant in the presence of algal cells. Therefore, the increased Mn(II) oxidation by QJX-1 in the presence of algae cannot be due to the increased biomass. Within this co-culture system, the Mn(II) oxidation rate surged to an impressive 0.23 mg/L/h, in stark contrast to 0.02 mg/L/h recorded within pure QJX-1 system. The presence of algae could inhibit the Fe-S cluster activity of QJX-1 by the produced active substance in co-culture, and result in the acceleration of extracellular superoxide production due to the impairment of electron transfer functions located in QJX-1 cell membranes. Moreover, elevated peroxidase gene expression and heightened extracellular catalase activity not only expedited Mn(II) ions oxidation but also facilitated conversion of intermediate Mn(III) ions into microbial Mn oxides, achieved through the degradation of hydrogen peroxide. Therefore, the acceleration of extracellular superoxide production and the decomposition of hydrogen peroxide are identified as the principal mechanisms behind the observed enhancement in Mn(II) oxidation within algae-bacteria co-cultures. Our findings highlight the need to consider the effect of algae on microbial Mn(II) oxidation, which plays an important role in the environmental pollution remediation.