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

Abstract

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.

Authors:
 [1];  [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5];  [5]; ORCiD logo [6]; ORCiD logo [2];  [1]; ORCiD logo [6]
+ Show Author Affiliations
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Smithsonian Tropical Research Inst., Balboa, Ancon (Panama)
  3. Univ. of Tennessee, Knoxville, TN (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1474724
Alternate Identifier(s):
OSTI ID: 1561882
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Ecology and Evolution
Additional Journal Information:
Journal Volume: 2; Journal Issue: 3; Journal ID: ISSN 2397-334X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; element cycles; environmental microbiology; metagenomics; tropical ecology

Citation Formats

Yao, Qiuming, Li, Zhou, Song, Yang, Wright, S. Joseph, Guo, Xuan, Tringe, Susannah G., Tfaily, Malak M., Paša-Tolić, Ljiljana, Hazen, Terry C., Turner, Benjamin L., Mayes, Melanie A., and Pan, Chongle. Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. United States: N. p., 2018. Web. doi:10.1038/s41559-017-0463-5.
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Yao, Qiuming, Li, Zhou, Song, Yang, Wright, S. Joseph, Guo, Xuan, Tringe, Susannah G., Tfaily, Malak M., Paša-Tolić, Ljiljana, Hazen, Terry C., Turner, Benjamin L., Mayes, Melanie A., & Pan, Chongle. Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. United States. https://doi.org/10.1038/s41559-017-0463-5
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Yao, Qiuming, Li, Zhou, Song, Yang, Wright, S. Joseph, Guo, Xuan, Tringe, Susannah G., Tfaily, Malak M., Paša-Tolić, Ljiljana, Hazen, Terry C., Turner, Benjamin L., Mayes, Melanie A., and Pan, Chongle. Mon . "Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil". United States. https://doi.org/10.1038/s41559-017-0463-5. https://www.osti.gov/servlets/purl/1474724.
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@article{osti_1474724,
title = {Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil},
author = {Yao, Qiuming and Li, Zhou and Song, Yang and Wright, S. Joseph and Guo, Xuan and Tringe, Susannah G. and Tfaily, Malak M. and Paša-Tolić, Ljiljana and Hazen, Terry C. and Turner, Benjamin L. and Mayes, Melanie A. and Pan, Chongle},
abstractNote = {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.},
doi = {10.1038/s41559-017-0463-5},
journal = {Nature Ecology and Evolution},
number = 3,
volume = 2,
place = {United States},
year = {2018},
month = {1}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1038/s41559-017-0463-5
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Cited by: 74 works
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Figures / Tables:

Fig. 1 Fig. 1: Impact of phosphorus availability on the phosphorus, carbon, nitrogen and sulfur cycles of the Gigante soil communities. a, Phosphorus acquisition from organic phosphorus substrates ordered by recalcitrance. b, Degradation of carbon substrates ordered by recalcitrance. c, Transformation of nitrogenous compounds ordered by nitrogen reduction states. d, Transformation ofmore » sulfur substrates ordered by sulfur reduction states. EC numbers associated with each transformation process are shown with red arrows when more abundant in phosphorus-deficient soils, blue arrows when more abundant in phosphorus-rich soils and black arrows when present in both soils with no significant abundance change. Microbial communities in the phosphorus-deficient soils had higher gene abundances for enzymes (Table 1) to acquire phosphorus from phytate, nucleic acids and phospholipids, decompose hemicellulose and pectin, and degrade proteins. Microbial communities in the phosphorus-rich soils had higher gene abundances for enzymes (Table 1) to catabolize aromatic compounds, obtain ammonium from nitrophenol and ethanolamine, and uptake sulfur from taurine« less
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