Acidification-based mineral weathering mechanism involves a glucose/methanol/choline oxidoreductase in Caballeronia mineralivorans PML1(12).

While mineral weathering (MWe) plays a key role in plant growth promotion and soil fertility, the molecular mechanisms and the genes used by bacteria to weather minerals remain poorly characterized. Acidification-based dissolution is considered the primary mechanism used by bacteria. This mechanism is historically associated with the conversion of glucose to protons and gluconic acid through the action of particular glucose dehydrogenases (GDH) dependent on the pyrroquinoline quinone (PQQ) cofactor. Recently, bacteria lacking the GDH-PQQ system have been shown to perform the same enzymatic conversion with a glucose/methanol/choline (GMC) FAD-dependent oxidoreductase. Determining whether this particular enzyme is specific or widespread is especially important in terms of ecology and evolution. Genome analysis of the effective MWe strain Caballeronia mineralivorans PML1(12) revealed the presence of both systems (i.e., GDH-PQQ and several GMC oxidoreductases). The combination of mutagenesis, functional assays, and geochemical analyses demonstrated the key role of one of these GMC oxidoreductases in the mineral weathering ability of strain PML1(12) and the importance of the carbon source metabolized. Mass spectrometry confirmed the conversion of glucose to gluconic acid. Phylogenetic analyses highlighted a good relatedness of this new GMC oxidoreductase with GMC oxidoreductases presenting a GDH activity in Burkholderia cepacia and Collimonas pratensis and conferring its mineral weathering ability to the last one. Together, our analyses expand the number of bacteria capable of weathering minerals using GMC oxidoreductases, showing that such enzymes are not restricted to Collimonas.

Importance: This work deciphers the molecular and genetic bases used by strain PML1(12) of Caballeronia mineralivorans to weather minerals. Through bioinformatics analyses, we identified a total of four GMC-FAD oxidoreductases in the genome of strain PML1(12) and a putative PQQ-dependent glucose dehydrogenase. Through a combination of physiological and geochemical analyses, we revealed that one of them (i.e., GMC3) was the enzyme responsible for the acidification-based mineral weathering mechanism used by strain PML1(12). To date, a single representative of this enzyme family has been identified in the effective mineral-weathering bacterial strain Collimonas pratensis PMB3(1). Phylogenetic analyses revealed that this new system appeared conserved in the Collimonas genus. The new findings presented in this work demonstrate that GMC oxidoreductases can have an active role in other effective MWe bacteria outside of collimonads and that Caballeronia are capable of weathering minerals using this type of enzyme. Our findings offer relevant information for different fields of research, such as environmental genomics, microbiology, chemistry, evolutionary biology, and soil sciences.