Metagenomic strategies uncover the soil bioavailable phosphorus improved by organic fertilization in Mollisols

Microorganisms play essential roles in soil phosphorus (P) cycling and the regulation of P bioavailability, however, genetic information on microbial P cycling in response to nutrient inputs is largely unclear. Here, metagenomic sequencing and genome binning were used to investigate microbial functional traits under chemical and organic fertilization in three long-term field experiments across black soil region of Northeast China. The results revealed that manure amendments strongly affected microbial P cycle-related functional gene patterns, which were significantly and positively correlated with the contents of soil total P (TP) and available P (AP). Manure addition directly increased soil AP concentrations, and indirectly acted through the alterations of microbial functional genes involved in soil P cycling. Specifically, manure amendments consistently decreased abundances of phnC gene and increased gene abundances of phnP, opd, and phoN across three locations, suggesting the potentially inhibition of soil microbial P-uptake and transport and the promotion of soil microbial organic P- mineralization. Manure addition promoted microbial inorganic P-solubilization by enriching the ppa, gcd, and pqqC genes at two out of three locations, while chemical fertilizer (CF) addition slightly stimulated the functional gene abundances involved in microbial P-uptake and transport and P-starvation response regulation. In addition, soil AP content was negatively correlated with the phnC gene abundance but positively correlated with the gene abundances of opd and phoN. Moreover, 23 metagenome-assembled genomes (MAGs) were reconstructed covering all soil samples, all of which contained the phnC gene with the copy numbers varying from 1 to 19. Nevertheless, only bin44 had a negative correlation with soil AP (r = −0.361, P = 0.030) and could be considered as a potential indicator regulating microbial P-uptake and transport. Taken together, manure inputs positively accelerated microbial P-transformations, which was beneficial for the establishment of efficient P management strategies in sustainable-intensive agriculture.