Distribution of phosphorus cycling genes across land uses and microbial taxonomic groups based on metagenome and genome mining

Abstract

Phosphorus (P) is an essential and limiting nutrient in soil and is tightly linked to soil fertility and productivity. Microorganisms have developed different mechanisms to respond to P scarcity and increase its availability in soil, which are susceptible to change under contrasting land uses. Here, we calculated and compared metagenomic redundancy, as a measurement of ecosystem potential capacity, of 23 key functional genes related to organic P mineralization, inorganic P solubilization and P-starvation response regulation in forest, grassland and cropland soils through mining in public sequence repository. The redundancy of those genes in all currently published genomes (genome redundancy) from archaea, bacteria and fungi was also studied. Microbes in croplands and grasslands showed a higher potential (i.e., redundancy) to mineralize organic P through the action of alkaline phosphatases (phoA, phoD and phoX genes) and to solubilize inorganic P (gcd and pqqC) by producing gluconic acid than those in forests. Instead, the capacity of microbes to mineralize phosphonates through the action of C–P lyases (phnG, phnH, …, phnM) was found to be higher in forests. The impact of land use on the metagenomic redundancy of genes encoding phytases (appA and 3-phytase) was dependent on the type of phytase. Intermetagenome redundancy (potentiality per metagenome unit) reached maximum values for phosphatase production, P solubilization and regulation of P starvation, denoting the crucial role that these functions have in P cycling. Proteobacteria, within Bacteria, and Euryarchaeota, within Archaea, showed the greatest genomic potential to respond to P scarcity. However, the role of fungi seems to be more restricted. The present study provides an overview on how the microbial mechanisms that regulate P availability in soil potentially change with land use and taxonomy of microbes.