Decoding Collimonas pratensis PMB3(1) responses during biotite interaction and dissolution: a multi-omics and geochemical perspective.

Abstract

Mineral weathering bacteria are known to mobilize the nutrients entrapped in minerals using acidification- and chelation-driven mineral weathering (MWe) mechanisms. Through these mechanisms, bacteria are expected to play important roles in soil nutrient cycling and tree nutrition. Among the most effective MWe bacteria identified, Collimonas are particularly interesting due to their occurrence in the rhizosphere and their ability to acidify their environment using a glucose methanol choline oxidoreductase and to mobilize iron using malleobactin. Until now, the regulations of these functions according to nutrient availability and presence/absence of minerals remain uncharacterized, as does the potential involvement of other direct and indirect MWe mechanisms. In this context, we investigated how the solution chemistry and the functions expressed by strain PMB3(1) were regulated according to the concentrations of iron and magnesium and the presence/absence of biotite. Transcriptomics and proteomics dual approach highlighted that under nutrient-depleted conditions and in the absence of biotite, strain PMB3(1) increased the expression of genes and abundance of proteins related to osmoprotection, stress, and iron mobilization. On the contrary, in the presence of biotite, an upregulation of genes and proteins associated with surface sensing, motility, chemotaxis, transport, acidification, and iron storage was observed. These new findings represent a crucial first step in understanding the regulatory processes and mechanisms employed by Collimonas during its interaction with and weathering of biotite. They show that bacteria respond to nearby minerals in more complex ways than simply reacting to a lack of nutrients.IMPORTANCEMinerals and rocks represent reactive interfaces at the geochemical level and a particular habitat at the microbial level. They are, however, usually considered inert substrata, although they represent 80% of the soil composition. The works performed on interactions between minerals and bacteria have mainly considered anoxic processes and microorganisms and poorly soil heterotrophs. In this context, our understanding of the role of soil minerals and rocks in soil fertility and the relative contribution and the molecular mechanisms employed by effective mineral weathering bacterial communities remain poorly documented. The combined use in our study of transcriptomics, proteomics, and geochemical analyses permitted filling this gap. The new findings obtained here suggest that minerals impact the global metabolism and the effectiveness at weathering of the strain Collimonas pratensis PMB3(1). They also reveal that the behavior exhibited by this bacterial strain extends beyond a mere reaction to the lack of nutrients. The complex interactions occurring between the physicochemical properties of these minerals and the activities of the MWe bacteria we observed in vitro offer a new view of the relative importance of minerals and rocks in in situ processes (e.g., nutrient cycling, soil fertility, and tree nutrition) at both geochemical and biological levels.