Metagenomic evidence for adaptive P-acquisition strategies to sustain elevated soil microbial biomass P under swine manure fertilization

Abstract

The application of livestock manure increases soil microbial biomass phosphorus (MBP), a highly bioavailable P pool, thereby enhancing soil P fertility and helping address global P challenges. However, it remains unclear how microbial communities adapt their P-acquisition strategies to sustain the elevated MBP, limiting a comprehensive understanding of the microbial mechanisms underlying this sustainable P management practice. This study investigated the relationship between soil MBP and microbial functional profiles of P transformation through metagenomic analysis at a long-term experimental site with repeated applications of swine manure. Manure fertilization significantly increased soil MBP by 153% and reshaped the composition of microbial P-transformation genes, with a significant increase in the normalized abundances of 85 out of the 135 detected genes. MBP was signifi-cantly and positively correlated with the metabolic potential for P-acquisition processes including orthophosphate uptake, phosphoglycerol uptake, phytate hydrolysis, 2-aminoethylphosphonic acid degradation, and phosphite oxidation. Distinct dominant genera were significantly enriched under manure fertilization among the bacterial communities involved in these critical P-acquisition processes. Solirubrobacter and Nocardioides were the shared enriched taxa and crucial for the stability of their corresponding communities. The considerable variation in copy numbers of the corresponding genes among the 56 reconstructed bacterial metagenome-assembled genomes was indicative of potential shifts in the functional capacity for the critical P-acquisition processes of the enriched taxa. Collectively, the findings of this study suggest the detailed adaptive P-acquisition strategies employed by soil microbial communities to maintain the elevated MBP under swine manure fertilization and the microbial taxa contributing to this adaptation.

Graphical abstract

Keywords

upland Ultisol / soil P management / soil P availability / microbial adaptation / microbial functional profiles

Highlight

	● Swine manure fertilization increased soil MBP and altered microbial functional profiles of P transformation.
	● Microbial metabolic potential for P acquisition and synthesis were upregulated under swine manure fertilization.
	● MBP increased with the increasing metabolic potential for P acquisition from Ortho-P, Glycerol-P, phytate, 2-AEP, and phosphite.
	● Distinct taxa were associated with the enhanced metabolic potential for these P-acquisition processes.

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