Population-level control of two manganese oxidases expands the niche for bacterial manganese biomineralization

The enzymatic oxidation of aqueous divalent manganese (Mn) is a widespread
microbial trait that produces reactive Mn(III, IV) oxide minerals. These
biominerals drive carbon, nutrient, and trace metal cycles, thus playing
important environmental and ecological roles. However, the regulatory
mechanisms and physiological functions of Mn biomineralization are
unknown. This challenge arises from the common occurrence of multiple Mn
oxidases within the same organism and the use of Mn oxides as indicators
of combined gene activity. Through detection of gene activation in
individual cells, we discover that expression of
mnxG and mcoA, two Mn oxidase-encoding genes in
Pseudomonas putida GB-1, is confined to subsets of cells within the
population, with each gene showing distinct spatiotemporal patterns that
reflect local microenvironments. These coordinated intra-population
dynamics control Mn biomineralization and illuminate the strategies used
by microbial communities to dictate the extent, location and timing of
biogeochemical transformations.