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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]
  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.
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. doi:10.1038/s41559-017-0463-5.
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. doi:10.1038/s41559-017-0463-5. https://www.osti.gov/servlets/purl/1474724.
@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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Cited by: 26 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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Works referenced in this record:

Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms
journal, September 2012

  • Tveit, Alexander; Schwacke, Rainer; Svenning, Mette M.
  • The ISME Journal, Vol. 7, Issue 2
  • DOI: 10.1038/ismej.2012.99

Sipros Ensemble improves database searching and filtering for complex metaproteomics
journal, September 2017


Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming
journal, February 2016

  • Xue, Kai; M. Yuan, Mengting; J. Shi, Zhou
  • Nature Climate Change, Vol. 6, Issue 6
  • DOI: 10.1038/nclimate2940

Responses of extracellular enzymes to simple and complex nutrient inputs
journal, May 2005


Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone
journal, January 2016

  • Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F.
  • PeerJ, Vol. 4
  • DOI: 10.7717/peerj.2687

Carbon-Degrading Enzyme Activities Stimulated by Increased Nutrient Availability in Arctic Tundra Soils
journal, October 2013


Soils of amazonia with particular reference to the rainfor sites
journal, January 2009

  • Quesada, C. A.; Lloyd, J.; Anderson, L. O.
  • Biogeosciences Discussions, Vol. 6, Issue 2
  • DOI: 10.5194/bgd-6-3851-2009

Sipros/ProRata: a versatile informatics system for quantitative community proteomics
journal, June 2013


Gene and translation initiation site prediction in metagenomic sequences
journal, July 2012


Statistical evaluation of methods for identification of differentially abundant genes in comparative metagenomics
journal, January 2016


Metatranscriptomic insights on gene expression and regulatory controls in Candidatus Accumulibacter phosphatis
journal, November 2015

  • Oyserman, Ben O.; Noguera, Daniel R.; del Rio, Tijana Glavina
  • The ISME Journal, Vol. 10, Issue 4
  • DOI: 10.1038/ismej.2015.155

Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data
journal, January 2013


Resource partitioning for soil phosphorus: a hypothesis
journal, July 2008


Microbial Community Structure Affects Marine Dissolved Organic Matter Composition
journal, April 2016

  • Kujawinski, Elizabeth B.; Longnecker, Krista; Barott, Katie L.
  • Frontiers in Marine Science, Vol. 3
  • DOI: 10.3389/fmars.2016.00045

Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization
journal, September 2004

  • Mack, Michelle C.; Schuur, Edward A. G.; Bret-Harte, M. Syndonia
  • Nature, Vol. 431, Issue 7007
  • DOI: 10.1038/nature02887

Responses in Microbes and Plants to Changed Temperature, Nutrient, and Light Regimes in the Arctic
journal, September 1999


Accounting for the Multiple Natures of Missing Values in Label-Free Quantitative Proteomics Data Sets to Compare Imputation Strategies
journal, March 2016


Resource-use efficiency and plant invasion in low-resource systems
journal, April 2007


MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015


Elevated temperature alters proteomic responses of individual organisms within a biofilm community
journal, July 2014


MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets
journal, October 2015


Microbial species delineation using whole genome sequences
journal, July 2015

  • Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
  • Nucleic Acids Research, Vol. 43, Issue 14
  • DOI: 10.1093/nar/gkv657

Kraken: A set of tools for quality control and analysis of high-throughput sequence data
journal, September 2013


CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes
journal, August 2013

  • Segata, Nicola; Börnigen, Daniela; Morgan, Xochitl C.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3304

Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils
journal, October 2013

  • Sharma, Seema B.; Sayyed, Riyaz Z.; Trivedi, Mrugesh H.
  • SpringerPlus, Vol. 2, Issue 1
  • DOI: 10.1186/2193-1801-2-587

Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest
journal, August 2015

  • Wurzburger, Nina; Wright, S. Joseph
  • Ecology, Vol. 96, Issue 8
  • DOI: 10.1890/14-1362.1

Soils of Amazonia with particular reference to the RAINFOR sites
journal, January 2011


Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
journal, December 2008

  • Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
  • Nature Protocols, Vol. 4, Issue 1
  • DOI: 10.1038/nprot.2008.211

Distribution and diversity of phytate-mineralizing bacteria
journal, June 2007

  • Lim, Boon Leong; Yeung, Pok; Cheng, Chiwai
  • The ISME Journal, Vol. 1, Issue 4
  • DOI: 10.1038/ismej.2007.40

Omega: an Overlap-graph de novo Assembler for Metagenomics
journal, June 2014


Advanced Solvent Based Methods for Molecular Characterization of Soil Organic Matter by High-Resolution Mass Spectrometry
journal, April 2015


Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes
journal, March 2015

  • Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel
  • Nature, Vol. 521, Issue 7551
  • DOI: 10.1038/nature14238

Functional phylogenomics analysis of bacteria and archaea using consistent genome annotation with UniFam
journal, October 2014


edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


Soil organic phosphorus transformations along a coastal dune chronosequence under New Zealand temperate rain forest
journal, August 2014


The application of ecological stoichiometry to plant–microbial–soil organic matter transformations
journal, May 2015

  • Zechmeister-Boltenstern, Sophie; Keiblinger, Katharina Maria; Mooshammer, Maria
  • Ecological Monographs, Vol. 85, Issue 2
  • DOI: 10.1890/14-0777.1

Plant Allocation and the Multiple Limitation Hypothesis
journal, June 1992

  • Gleeson, Scott K.; Tilman, David
  • The American Naturalist, Vol. 139, Issue 6
  • DOI: 10.1086/285389

Seasonal Changes and Treatment Effects on Soil Inorganic Nutrients Following a Decade of Fertilizer Addition in a Lowland Tropical Forest
journal, January 2013

  • Turner, Benjamin L.; Yavitt, Joseph B.; Harms, Kyle E.
  • Soil Science Society of America Journal, Vol. 77, Issue 4
  • DOI: 10.2136/sssaj2012.0128

Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil
journal, January 1985


Sequential extraction protocol for organic matter from soils and sediments using high resolution mass spectrometry
journal, June 2017


Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem
journal, January 2007


Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

A Comparative Study of Techniques for Differential Expression Analysis on RNA-Seq Data
journal, August 2014


C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass?
journal, July 2007


Plant and soil fungal but not soil bacterial communities are linked in long-term fertilized grassland
journal, March 2016

  • Cassman, Noriko A.; Leite, Marcio F. A.; Pan, Yao
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep23680

An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C
journal, July 1997


The Perseus computational platform for comprehensive analysis of (prote)omics data
journal, June 2016

  • Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel
  • Nature Methods, Vol. 13, Issue 9
  • DOI: 10.1038/nmeth.3901

The term phytase comprises several different classes of enzymes
journal, December 2003

  • Mullaney, Edward J.; Ullah, Abul H. J.
  • Biochemical and Biophysical Research Communications, Vol. 312, Issue 1
  • DOI: 10.1016/j.bbrc.2003.09.176

Resource Limitation in Plants-An Economic Analogy
journal, November 1985


Soil organic phosphorus in lowland tropical rain forests
journal, June 2010


Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
journal, April 2011

  • Letunic, I.; Bork, P.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr201

Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest
journal, August 2011

  • Wright, S. Joseph; Yavitt, Joseph B.; Wurzburger, Nina
  • Ecology, Vol. 92, Issue 8
  • DOI: 10.1890/10-1558.1

Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition: Tropical tree seedling N-P-K responses
journal, October 2011


Seasonal changes in soil organic matter after a decade of nutrient addition in a lowland tropical forest
journal, January 2015


Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest
journal, December 2013

  • Mayor, Jordan R.; Wright, S. Joseph; Turner, Benjamin L.
  • Journal of Ecology, Vol. 102, Issue 1
  • DOI: 10.1111/1365-2745.12190

Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China
journal, January 2012


    Works referencing / citing this record:

    Contrasting patterns of plant and microbial diversity during long-term ecosystem development
    journal, January 2019

    • Turner, Benjamin L.; Zemunik, Graham; Laliberté, Etienne
    • Journal of Ecology, Vol. 107, Issue 2
    • DOI: 10.1111/1365-2745.13127

    Potentialities and soil impact analysis of rock phosphorus fertilization of perennial and annual legume crops
    journal, August 2019


    Soil metaproteomics as a tool for monitoring functional microbial communities: promises and challenges
    journal, December 2019

    • Abiraami, T. V.; Singh, Surender; Nain, Lata
    • Reviews in Environmental Science and Bio/Technology, Vol. 19, Issue 1
    • DOI: 10.1007/s11157-019-09519-8

    Online supercritical fluid extraction mass spectrometry (SFE-LC-FTMS) for sensitive characterization of soil organic matter
    journal, January 2019

    • Shen, Yufeng; Zhao, Rui; Tolić, Nikola
    • Faraday Discussions, Vol. 218
    • DOI: 10.1039/c9fd00011a

    Seasonal changes in soil respiration linked to soil moisture and phosphorus availability along a tropical rainfall gradient
    journal, September 2019


    Phylogenetic conservation of soil bacterial responses to simulated global changes
    journal, March 2020

    • Isobe, Kazuo; Bouskill, Nicholas J.; Brodie, Eoin L.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798
    • DOI: 10.1098/rstb.2019.0242

    Genome-Resolved Proteomic Stable Isotope Probing of Soil Microbial Communities Using 13CO2 and 13C-Methanol
    journal, December 2019


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