Phosphorus is a scarce nutrient in many tropical ecosystems, yet how soil microbial communities cope with growth-limiting phosphorus deficiency at the gene and protein levels remains unknown. Here, we report a metagenomic and metaproteomic comparison of microbial communities in phosphorus-deficient and phosphorus-rich soils in a 17-year fertilization experiment in a tropical forest. The large-scale proteogenomics analyses provided extensive coverage of many microbial functions and taxa in the complex soil communities. A greater than fourfold increase in the gene abundance of 3-phytase was the strongest response of soil communities to phosphorus deficiency. Phytase catalyses the release of phosphate from phytate, the most recalcitrant phosphorus-containing compound in soil organic matter. Genes and proteins for the degradation of phosphorus-containing nucleic acids and phospholipids, as well as the decomposition of labile carbon and nitrogen, were also enhanced in the phosphorus-deficient soils. In contrast, microbial communities in the phosphorus-rich soils showed increased gene abundances for the degradation of recalcitrant aromatic compounds, transformation of nitrogenous compounds and assimilation of sulfur. Overall, these results demonstrate the adaptive allocation of genes and proteins in soil microbial communities in response to shifting nutrient constraints.
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This work was supported by Laboratory Directed Research and Development funding from Oak Ridge National Laboratory (ORNL). The authors acknowledge R. Hurt of ORNL’s Biosciences Division for assistance with DNA extractions from tropical soils and J. Phillips of ORNL’s Environmental Sciences Division for soil characterization. The metagenomic sequencing was conducted by the US Department of Energy (DOE) Joint Genome Institute (JGI). The Fourier transform ion cyclotron resonance MS analyses were performed by the Environmental Molecular Sciences Laboratory (EMSL). The JGI and EMSL are DOE Office of Science User Facilities sponsored by the Office of Biological and Environmental Research. This research used resources of the Oak Ridge Leadership Computing Facility. The ORNL and JGI are supported by the Office of Science of the US DOE under contract numbers DE-AC05-00OR22725 and DE-AC02-05CH11231, respectively.
The authors declare no competing financial interests.
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Supplementary Figures 1 and 2
Summary of the community proteogenomic results
Differential analysis of gene abundances by EC numbers and GO terms in the Gigante soil metagenomes
Assembly and pathway analysis of the near-complete genomes
Differential analysis of protein abundances by EC numbers and GO terms in the Gigante soil metaproteomes
Measurement of soil properties
Measurement of soil organic matter by Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FTICR-MS)
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Yao, Q., Li, Z., Song, Y. et al. Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. Nat Ecol Evol 2, 499–509 (2018). https://doi.org/10.1038/s41559-017-0463-5