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

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

doi:10.1038/s41559-017-0463-5

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

Journal Article · Mon Jan 22 00:00:00 EST 2018 · Nature Ecology and Evolution

DOI:https://doi.org/10.1038/s41559-017-0463-5· OSTI ID:1474724

Yao, Qiuming ^[1]; Li, Zhou ^[1];

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^[5]; Paša-Tolić, Ljiljana ^[5];

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^[2]; Mayes, Melanie A. ^[1];

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Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Smithsonian Tropical Research Inst., Balboa, Ancon (Panama)
Univ. of Tennessee, Knoxville, TN (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)

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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Research Organization:: Oak Ridge National Laboratory (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 Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1474724

Alternate ID(s):: OSTI ID: 1561882

Journal Information:: Nature Ecology and Evolution, Vol. 2, Issue 3; ISSN 2397-334X

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 95 works

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References (68)

Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms Tveit, Alexander; Schwacke, Rainer; Svenning, Mette M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.99	journal	September 2012
Integrated proteomics and metabolomics suggests symbiotic metabolism and multimodal regulation in a fungal-endobacterial system: Symbiotic metabolism and multimodal regulation Li, Zhou; Yao, Qiuming; Dearth, Stephen P. Environmental Microbiology, Vol. 19, Issue 3 https://doi.org/10.1111/1462-2920.13605	journal	January 2017
Sipros Ensemble improves database searching and filtering for complex metaproteomics Guo, Xuan; Li, Zhou; Yao, Qiuming Bioinformatics, Vol. 34, Issue 5 https://doi.org/10.1093/bioinformatics/btx601	journal	September 2017
Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming Xue, Kai; M. Yuan, Mengting; J. Shi, Zhou Nature Climate Change, Vol. 6, Issue 6 https://doi.org/10.1038/nclimate2940	journal	February 2016
Responses of extracellular enzymes to simple and complex nutrient inputs Allison, Steven D.; Vitousek, Peter M. Soil Biology and Biochemistry, Vol. 37, Issue 5 https://doi.org/10.1016/j.soilbio.2004.09.014	journal	May 2005
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2687	journal	January 2016
Carbon-Degrading Enzyme Activities Stimulated by Increased Nutrient Availability in Arctic Tundra Soils Koyama, Akihiro; Wallenstein, Matthew D.; Simpson, Rodney T. PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0077212	journal	October 2013
Sipros/ProRata: a versatile informatics system for quantitative community proteomics Wang, Yingfeng; Ahn, Tae-Hyuk; Li, Zhou Bioinformatics, Vol. 29, Issue 16 https://doi.org/10.1093/bioinformatics/btt329	journal	June 2013
Gene and translation initiation site prediction in metagenomic sequences Hyatt, Doug; LoCascio, Philip F.; Hauser, Loren J. Bioinformatics, Vol. 28, Issue 17 https://doi.org/10.1093/bioinformatics/bts429	journal	July 2012
Statistical evaluation of methods for identification of differentially abundant genes in comparative metagenomics Jonsson, Viktor; Österlund, Tobias; Nerman, Olle BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2386-y	journal	January 2016
Metatranscriptomic insights on gene expression and regulatory controls in Candidatus Accumulibacter phosphatis Oyserman, Ben O.; Noguera, Daniel R.; del Rio, Tijana Glavina The ISME Journal, Vol. 10, Issue 4 https://doi.org/10.1038/ismej.2015.155	journal	November 2015
Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data Rapaport, Franck; Khanin, Raya; Liang, Yupu Genome Biology, Vol. 14, Issue 9 https://doi.org/10.1186/gb-2013-14-9-r95	journal	January 2013
Resource partitioning for soil phosphorus: a hypothesis Turner, Benjamin L. Journal of Ecology, Vol. 96, Issue 4 https://doi.org/10.1111/j.1365-2745.2008.01384.x	journal	July 2008
Microbial Community Structure Affects Marine Dissolved Organic Matter Composition Kujawinski, Elizabeth B.; Longnecker, Krista; Barott, Katie L. Frontiers in Marine Science, Vol. 3 https://doi.org/10.3389/fmars.2016.00045	journal	April 2016
Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization Mack, Michelle C.; Schuur, Edward A. G.; Bret-Harte, M. Syndonia Nature, Vol. 431, Issue 7007 https://doi.org/10.1038/nature02887	journal	September 2004
Responses in Microbes and Plants to Changed Temperature, Nutrient, and Light Regimes in the Arctic Jonasson, Sven; Michelsen, Anders; Schmidt, Inger K. Ecology, Vol. 80, Issue 6 https://doi.org/10.1890/0012-9658(1999)080[1828:RIMAPT]2.0.CO;2	journal	September 1999
Accounting for the Multiple Natures of Missing Values in Label-Free Quantitative Proteomics Data Sets to Compare Imputation Strategies Lazar, Cosmin; Gatto, Laurent; Ferro, Myriam Journal of Proteome Research, Vol. 15, Issue 4 https://doi.org/10.1021/acs.jproteome.5b00981	journal	March 2016
Resource-use efficiency and plant invasion in low-resource systems Funk, Jennifer L.; Vitousek, Peter M. Nature, Vol. 446, Issue 7139 https://doi.org/10.1038/nature05719	journal	April 2007
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
Elevated temperature alters proteomic responses of individual organisms within a biofilm community Mosier, Annika C.; Li, Zhou; Thomas, Brian C. The ISME Journal, Vol. 9, Issue 1 https://doi.org/10.1038/ismej.2014.113	journal	July 2014
MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets Wu, Yu-Wei; Simmons, Blake A.; Singer, Steven W. Bioinformatics, Vol. 32, Issue 4 https://doi.org/10.1093/bioinformatics/btv638	journal	October 2015
Microbial species delineation using whole genome sequences Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia Nucleic Acids Research, Vol. 43, Issue 14 https://doi.org/10.1093/nar/gkv657	journal	July 2015
Kraken: A set of tools for quality control and analysis of high-throughput sequence data Davis, Matthew P. A.; van Dongen, Stijn; Abreu-Goodger, Cei Methods, Vol. 63, Issue 1 https://doi.org/10.1016/j.ymeth.2013.06.027	journal	September 2013
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes Segata, Nicola; Börnigen, Daniela; Morgan, Xochitl C. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3304	journal	August 2013
Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils Sharma, Seema B.; Sayyed, Riyaz Z.; Trivedi, Mrugesh H. SpringerPlus, Vol. 2, Issue 1 https://doi.org/10.1186/2193-1801-2-587	journal	October 2013
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest Wurzburger, Nina; Wright, S. Joseph Ecology, Vol. 96, Issue 8 https://doi.org/10.1890/14-1362.1	journal	August 2015
Soils of Amazonia with particular reference to the RAINFOR sites Quesada, C. A.; Lloyd, J.; Anderson, L. O. Biogeosciences, Vol. 8, Issue 6 https://doi.org/10.5194/bg-8-1415-2011	journal	January 2011
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest Turner, Benjamin L.; Joseph Wright, S. Biogeochemistry, Vol. 117, Issue 1 https://doi.org/10.1007/s10533-013-9848-y	journal	April 2013
Improved Yield of High Molecular Weight DNA Coincides with Increased Microbial Diversity Access from Iron Oxide Cemented Sub-Surface Clay Environments Hurt, Richard A.; Robeson, Michael S.; Shakya, Migun PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0102826	journal	July 2014
Distribution and diversity of phytate-mineralizing bacteria Lim, Boon Leong; Yeung, Pok; Cheng, Chiwai The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.40	journal	June 2007
Omega: an Overlap-graph de novo Assembler for Metagenomics Haider, Bahlul; Ahn, Tae-Hyuk; Bushnell, Brian Bioinformatics, Vol. 30, Issue 19 https://doi.org/10.1093/bioinformatics/btu395	journal	June 2014
Ecological Stoichiometry Sterner, Robert W.; Elser, James J. Princeton University Press https://doi.org/10.1515/9781400885695	book	December 2003
Advanced Solvent Based Methods for Molecular Characterization of Soil Organic Matter by High-Resolution Mass Spectrometry Tfaily, Malak M.; Chu, Rosalie K.; Tolić, Nikola Analytical Chemistry, Vol. 87, Issue 10 https://doi.org/10.1021/acs.analchem.5b00116	journal	April 2015
Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14238	journal	March 2015
Functional phylogenomics analysis of bacteria and archaea using consistent genome annotation with UniFam Chai, Juanjuan; Kora, Guruprasad; Ahn, Tae-Hyuk BMC Evolutionary Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12862-014-0207-y	journal	October 2014
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
Soil organic phosphorus transformations along a coastal dune chronosequence under New Zealand temperate rain forest Turner, Benjamin L.; Wells, Andrew; Condron, Leo M. Biogeochemistry, Vol. 121, Issue 3 https://doi.org/10.1007/s10533-014-0025-8	journal	August 2014
The application of ecological stoichiometry to plant–microbial–soil organic matter transformations Zechmeister-Boltenstern, Sophie; Keiblinger, Katharina Maria; Mooshammer, Maria Ecological Monographs, Vol. 85, Issue 2 https://doi.org/10.1890/14-0777.1	journal	May 2015
Plant Allocation and the Multiple Limitation Hypothesis Gleeson, Scott K.; Tilman, David The American Naturalist, Vol. 139, Issue 6 https://doi.org/10.1086/285389	journal	June 1992
Seasonal Changes and Treatment Effects on Soil Inorganic Nutrients Following a Decade of Fertilizer Addition in a Lowland Tropical Forest Turner, Benjamin L.; Yavitt, Joseph B.; Harms, Kyle E. Soil Science Society of America Journal, Vol. 77, Issue 4 https://doi.org/10.2136/sssaj2012.0128	journal	January 2013
Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil Brookes, P. C.; Landman, Andrea; Pruden, G. Soil Biology and Biochemistry, Vol. 17, Issue 6 https://doi.org/10.1016/0038-0717(85)90144-0	journal	January 1985
Sequential extraction protocol for organic matter from soils and sediments using high resolution mass spectrometry Tfaily, Malak M.; Chu, Rosalie K.; Toyoda, Jason Analytica Chimica Acta, Vol. 972 https://doi.org/10.1016/j.aca.2017.03.031	journal	June 2017
Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem Rinnan, Riikka; Michelsen, Anders; BÅÅTh, Erland Global Change Biology, Vol. 13, Issue 1 https://doi.org/10.1111/j.1365-2486.2006.01263.x	journal	January 2007
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
A Comparative Study of Techniques for Differential Expression Analysis on RNA-Seq Data Zhang, Zong Hong; Jhaveri, Dhanisha J.; Marshall, Vikki M. PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0103207	journal	August 2014
C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Cleveland, Cory C.; Liptzin, Daniel Biogeochemistry, Vol. 85, Issue 3 https://doi.org/10.1007/s10533-007-9132-0	journal	July 2007
Plant and soil fungal but not soil bacterial communities are linked in long-term fertilized grassland Cassman, Noriko A.; Leite, Marcio F. A.; Pan, Yao Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23680	journal	March 2016
An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C Beck, T.; Joergensen, R. G.; Kandeler, E. Soil Biology and Biochemistry, Vol. 29, Issue 7 https://doi.org/10.1016/S0038-0717(97)00030-8	journal	July 1997
The Perseus computational platform for comprehensive analysis of (prote)omics data Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel Nature Methods, Vol. 13, Issue 9 https://doi.org/10.1038/nmeth.3901	journal	June 2016
The term phytase comprises several different classes of enzymes Mullaney, Edward J.; Ullah, Abul H. J. Biochemical and Biophysical Research Communications, Vol. 312, Issue 1 https://doi.org/10.1016/j.bbrc.2003.09.176	journal	December 2003
Identification of β-propeller phytase-encoding genes in culturable Paenibacillus and Bacillus spp. from the rhizosphere of pasture plants on volcanic soils: Phytase genes in volcanic soils Jorquera, Milko A.; Crowley, David E.; Marschner, Petra FEMS Microbiology Ecology, Vol. 75, Issue 1 https://doi.org/10.1111/j.1574-6941.2010.00995.x	journal	November 2010
Resource Limitation in Plants-An Economic Analogy Bloom, A. J.; Chapin, F. S.; Mooney, H. A. Annual Review of Ecology and Systematics, Vol. 16, Issue 1 https://doi.org/10.1146/annurev.es.16.110185.002051	journal	November 1985
Soil organic phosphorus in lowland tropical rain forests Turner, Benjamin L.; Engelbrecht, Bettina M. J. Biogeochemistry, Vol. 103, Issue 1-3 https://doi.org/10.1007/s10533-010-9466-x	journal	June 2010
Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy Letunic, I.; Bork, P. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr201	journal	April 2011
Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest Wright, S. Joseph; Yavitt, Joseph B.; Wurzburger, Nina Ecology, Vol. 92, Issue 8 https://doi.org/10.1890/10-1558.1	journal	August 2011
Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition: Tropical tree seedling N-P-K responses Santiago, Louis S.; Wright, S. Joseph; Harms, Kyle E. Journal of Ecology, Vol. 100, Issue 2 https://doi.org/10.1111/j.1365-2745.2011.01904.x	journal	October 2011
Seasonal changes in soil organic matter after a decade of nutrient addition in a lowland tropical forest Turner, Benjamin L.; Yavitt, Joseph B.; Harms, Kyle E. Biogeochemistry, Vol. 123, Issue 1-2 https://doi.org/10.1007/s10533-014-0064-1	journal	January 2015
Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest Mayor, Jordan R.; Wright, S. Joseph; Turner, Benjamin L. Journal of Ecology, Vol. 102, Issue 1 https://doi.org/10.1111/1365-2745.12190	journal	December 2013
Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China Liu, Lei; Gundersen, Per; Zhang, Tao Soil Biology and Biochemistry, Vol. 44, Issue 1 https://doi.org/10.1016/j.soilbio.2011.08.017	journal	January 2012
Resource Competition and Community Structure. (MPB-17) Tilman, David https://doi.org/10.1515/9780691209654	book	December 1982
Soils of amazonia with particular reference to the rainfor sites Quesada, C. A.; Lloyd, J.; Anderson, L. O. Biogeosciences Discussions, Vol. 6, Issue 2 https://doi.org/10.5194/bgd-6-3851-2009	journal	January 2009
Accounting For The Multiple Natures Of Missing Values In Label-Free Quantitative Proteomics Data Sets To Compare Imputation Strategies Lazar, Cosmin; Gatto, Laurent; Ferro, Myriam Zenodo https://doi.org/10.5281/zenodo.802973	text	January 2016
Diversity and composition of the North Sikkim hot spring mycobiome using a culture-independent method Das, Sayak; Roy, Goshaidas; Najar, Ishfaq Nabi Folia Microbiologica, Vol. 66, Issue 3 https://doi.org/10.1007/s12223-021-00859-z	journal	March 2021
Polinton-like viruses are abundant in aquatic ecosystems Bellas, Christopher M.; Sommaruga, Ruben Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00956-0	journal	January 2021
Accounting For The Multiple Natures Of Missing Values In Label-Free Quantitative Proteomics Data Sets To Compare Imputation Strategies Lazar, Cosmin; Gatto, Laurent; Ferro, Myriam Zenodo https://doi.org/10.5281/zenodo.802972	text	January 2016

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