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Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil


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.

Author information

C.P. and M.A.M. designed the project. M.A.M., C.P., S.J.W. and B.L.T. performed the soil sampling. Q.Y., T.C.H., S.G.T. and C.P. performed the metagenomics. Z.L. and X.G. performed the metaproteomics. Q.Y. and M.A.M. performed the enzyme assay. M.M.T., L.P.-T. and Y.S. performed the soil organic matter analysis. Q.Y. and C.P. analysed the meta-omics results. B.L.T., S.J.W. and M.A.M. assisted in interpretation of the results. The manuscript was drafted by Q.Y. and C.P. and revised by all authors.

Correspondence to Chongle Pan.

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Supplementary information

Supplementary Information

Supplementary Figures 1 and 2

Life Sciences Reporting Summary

Supplementary Data 1

Summary of the community proteogenomic results

Supplementary Data 2

Differential analysis of gene abundances by EC numbers and GO terms in the Gigante soil metagenomes

Supplementary Data 3

Assembly and pathway analysis of the near-complete genomes

Supplementary Data 4

Differential analysis of protein abundances by EC numbers and GO terms in the Gigante soil metaproteomes

Supplementary Data 5

Measurement of soil properties

Supplementary Data 6

Measurement of soil organic matter by Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FTICR-MS)

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Further reading

Fig. 1: Impact of phosphorus availability on the phosphorus, carbon, nitrogen and sulfur cycles of the Gigante soil communities.
Fig. 2: Taxonomic distribution of key phosphorus-acquisition enzymes.
Fig. 3: Classification and evolution of phytase genes.
Fig. 4: Proteogenomics comparison of phosphorus-deficient and phosphorus-rich soils.
Fig. 5: Comparison of enzyme activities.