A genomic perspective on stoichiometric regulation of soil carbon cycling

Hartman, Wyatt H.; Ye, Rongzhong; Horwath, William R.; Tringe, Susannah G.

doi:10.1038/ismej.2017.115

Title: A genomic perspective on stoichiometric regulation of soil carbon cycling

Journal Article · Fri Jul 21 00:00:00 EDT 2017 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2017.115· OSTI ID:1482526

Hartman, Wyatt H. ^[1]; Ye, Rongzhong ^[2]; Horwath, William R. ^[3];

^[4]

USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. of California, Davis, CA (United States); Clemson Univ., Clemson, SC (United States)
Univ. of California, Davis, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Merced, CA (United States)

Similar to plant growth, soil carbon (C) cycling is constrained by the availability of nitrogen (N) and phosphorus (P). We hypothesized that stoichiometric control over soil microbial C cycling may be shaped by functional guilds with distinct nutrient substrate preferences. Across a series of rice fields spanning 5-25% soil C (N:P from 1:12 to 1:70), C turnover was best correlated with P availability and increased with experimental N addition only in lower C (mineral) soils with N:P-1/216. Microbial community membership also varied with soil stoichiometry but not with N addition. Shotgun metagenome data revealed changes in community functions with increasing C turnover, including a shift from aromatic C to carbohydrate utilization accompanied by lower N uptake and P scavenging. Similar patterns of C, N and P acquisition, along with higher ribosomal RNA operon copy numbers, distinguished that microbial taxa positively correlated with C turnover. Considering such tradeoffs in genomic resource allocation patterns among taxa strengthened correlations between microbial community composition and C cycling, suggesting simplified guilds amenable to ecosystem modeling. Our results suggest that patterns of soil C turnover may reflect community-dependent metabolic shifts driven by resource allocation strategies, analogous to growth rate-stoichiometry coupling in animal and plant communities.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1482526

Journal Information:: The ISME Journal, Vol. 11, Issue 12; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 78 works

Citation information provided by
Web of Science

References (101)

Microorganisms and climate change: terrestrial feedbacks and mitigation options Singh, Brajesh K.; Bardgett, Richard D.; Smith, Pete Nature Reviews Microbiology, Vol. 8, Issue 11 https://doi.org/10.1038/nrmicro2439	journal	October 2010
IMG/M 4 version of the integrated metagenome comparative analysis system Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573 https://doi.org/10.1093/nar/gkt919	journal	October 2013
Indigenous Nitrogen Supply of Rice Is Predicted by Soil Organic Carbon Espe, Matthew B.; Kirk, Emilie; van Kessel, Chris Soil Science Society of America Journal, Vol. 79, Issue 2 https://doi.org/10.2136/sssaj2014.08.0328	journal	January 2015
Rates of in situ carbon mineralization in relation to land-use, microbial community and edaphic characteristics Strickland, Michael S.; Callaham, Mac A.; Davies, Christian A. Soil Biology and Biochemistry, Vol. 42, Issue 2 https://doi.org/10.1016/j.soilbio.2009.10.026	journal	February 2010
Differential Nutrient Limitation of Soil Microbial Biomass and Metabolic Quotients (qCO2): Is There a Biological Stoichiometry of Soil Microbes? Hartman, Wyatt H.; Richardson, Curtis J. PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0057127	journal	March 2013
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4) Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0077-y	journal	October 2015
Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils Spohn, Marie; Chodak, Marcin Soil Biology and Biochemistry, Vol. 81 https://doi.org/10.1016/j.soilbio.2014.11.008	journal	February 2015
Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies Treseder, Kathleen K. Ecology Letters, Vol. 11, Issue 10 https://doi.org/10.1111/j.1461-0248.2008.01230.x	journal	October 2008
Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity Li, Jianwei; Wang, Gangsheng; Allison, Steven D. Biogeochemistry, Vol. 119, Issue 1-3 https://doi.org/10.1007/s10533-013-9948-8	journal	January 2014
Global biogeochemical impacts of phytoplankton: a trait-based perspective Litchman, Elena; de Tezanos Pinto, Paula; Edwards, Kyle F. Journal of Ecology, Vol. 103, Issue 6 https://doi.org/10.1111/1365-2745.12438	journal	October 2015
Elemental stoichiometry of Fungi and Bacteria strains from grassland leaf litter Mouginot, Céline; Kawamura, Rika; Matulich, Kristin L. Soil Biology and Biochemistry, Vol. 76 https://doi.org/10.1016/j.soilbio.2014.05.011	journal	September 2014
Optimization of Biomass Composition Explains Microbial Growth-Stoichiometry Relationships Franklin, Oskar; Hall, Edward K.; Kaiser, Christina The American Naturalist, Vol. 177, Issue 2 https://doi.org/10.1086/657684	journal	February 2011
Opposing effects of nitrogen and phosphorus on soil microbial metabolism and the implications for soil carbon storage Poeplau, Christopher; Herrmann, Anke M.; Kätterer, Thomas Soil Biology and Biochemistry, Vol. 100 https://doi.org/10.1016/j.soilbio.2016.05.021	journal	September 2016
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory Nature Biotechnology, Vol. 31, Issue 9 https://doi.org/10.1038/nbt.2676	journal	August 2013
Phylogenetic Distribution of Potential Cellulases in Bacteria Berlemont, Renaud; Martiny, Adam C. Applied and Environmental Microbiology, Vol. 79, Issue 5 https://doi.org/10.1128/AEM.03305-12	journal	December 2012
Incorporating phosphorus cycling into global modeling efforts: a worthwhile, tractable endeavor Reed, Sasha C.; Yang, Xiaojuan; Thornton, Peter E. New Phytologist, Vol. 208, Issue 2 https://doi.org/10.1111/nph.13521	journal	June 2015
Do microorganism stoichiometric alterations affect carbon sequestration in paddy soil subjected to phosphorus input? Zhang, ZhiJian; Li, HongYi; Hu, Jiao Ecological Applications, Vol. 25, Issue 3 https://doi.org/10.1890/14-0189.1	journal	April 2015
N : P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms Güsewell, Sabine; Gessner, Mark O. Functional Ecology, Vol. 23, Issue 1 https://doi.org/10.1111/j.1365-2435.2008.01478.x	journal	February 2009
Distribution of phosphatase activity and various bacterial phyla in the rhizosphere of Hordeum vulgare L. depending on P availability Spohn, Marie; Treichel, Nicole Simone; Cormann, Michael Soil Biology and Biochemistry, Vol. 89 https://doi.org/10.1016/j.soilbio.2015.06.018	journal	October 2015
Microbial response to simulated global change is phylogenetically conserved and linked with functional potential Amend, Anthony S.; Martiny, Adam C.; Allison, Steven D. The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.96	journal	June 2015
Thermodynamic constraints on the utility of ecological stoichiometry for explaining global biogeochemical patterns Helton, Ashley M.; Ardón, Marcelo; Bernhardt, Emily S. Ecology Letters, Vol. 18, Issue 10 https://doi.org/10.1111/ele.12487	journal	August 2015
Organism Size, Life History, and N:P Stoichiometry Elser, James J.; Dobberfuhl, Dean R.; MacKay, Neil A. BioScience, Vol. 46, Issue 9 https://doi.org/10.2307/1312897	journal	October 1996
Microbiomes in light of traits: A phylogenetic perspective Martiny, J. B. H.; Jones, S. E.; Lennon, J. T. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aac9323	journal	November 2015
Cellulolytic potential under environmental changes in microbial communities from grassland litter Berlemont, Renaud; Allison, Steven D.; Weihe, Claudia Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00639	journal	November 2014
A Three-Way Trade-Off Maintains Functional Diversity under Variable Resource Supply Edwards, Kyle F.; Klausmeier, Christopher A.; Litchman, Elena The American Naturalist, Vol. 182, Issue 6 https://doi.org/10.1086/673532	journal	December 2013
Growth rate-stoichiometry couplings in diverse biota Elser, J. J.; Acharya, K.; Kyle, M. Ecology Letters, Vol. 6, Issue 10 https://doi.org/10.1046/j.1461-0248.2003.00518.x	journal	October 2003
Trait-Based Representation of Biological Nitrification: Model Development, Testing, and Predicted Community Composition Bouskill, Nicholas J.; Tang, Jinyun; Riley, William J. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00364	journal	January 2012
The ecological coherence of high bacterial taxonomic ranks Philippot, Laurent; Andersson, Siv G. E.; Battin, Tom J. Nature Reviews Microbiology, Vol. 8, Issue 7 https://doi.org/10.1038/nrmicro2367	journal	June 2010
The worldwide leaf economics spectrum Wright, Ian J.; Reich, Peter B.; Westoby, Mark Nature, Vol. 428, Issue 6985 https://doi.org/10.1038/nature02403	journal	April 2004
Resistance, resilience, and redundancy in microbial communities Allison, S. D.; Martiny, J. B. H. Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1 https://doi.org/10.1073/pnas.0801925105	journal	August 2008
The Systemic Imprint of Growth and Its Uses in Ecological (Meta)Genomics Vieira-Silva, Sara; Rocha, Eduardo P. C. PLoS Genetics, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pgen.1000808	journal	January 2010
Phylogenetic identity, growth-response time and rRNA operon copy number of soil bacteria indicate different stages of community succession Shrestha, Pravin Malla; Noll, Matthias; Liesack, Werner Environmental Microbiology, Vol. 9, Issue 10 https://doi.org/10.1111/j.1462-2920.2007.01364.x	journal	October 2007
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z. Ecological Applications, Vol. 20, Issue 1 https://doi.org/10.1890/08-0127.1	journal	January 2010
Soil carbon quality and nitrogen fertilization structure bacterial communities with predictable responses of major bacterial phyla Cederlund, Harald; Wessén, Ella; Enwall, Karin Applied Soil Ecology, Vol. 84 https://doi.org/10.1016/j.apsoil.2014.06.003	journal	December 2014
A fully traits-based approach to modeling global vegetation distribution van Bodegom, P. M.; Douma, J. C.; Verheijen, L. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 38 https://doi.org/10.1073/pnas.1304551110	journal	September 2014
Microbial resource utilization traits and trade-offs: implications for community structure, functioning, and biogeochemical impacts at present and in the future Litchman, Elena; Edwards, Kyle F.; Klausmeier, Christopher A. Frontiers in Microbiology, Vol. 06 https://doi.org/10.3389/fmicb.2015.00254	journal	April 2015
Carbon mineralization is promoted by phosphorus and reduced by nitrogen addition in the organic horizon of northern hardwood forests Fisk, Melany; Santangelo, Sharon; Minick, Kevan Soil Biology and Biochemistry, Vol. 81 https://doi.org/10.1016/j.soilbio.2014.11.022	journal	February 2015
Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils Bradford, M. A.; Fierer, N.; Reynolds, J. F. Functional Ecology, Vol. 22, Issue 6 https://doi.org/10.1111/j.1365-2435.2008.01404.x	journal	December 2008
CATS regression - a model-based approach to studying trait-based community assembly Warton, David I.; Shipley, Bill; Hastie, Trevor Methods in Ecology and Evolution, Vol. 6, Issue 4 https://doi.org/10.1111/2041-210X.12280	journal	October 2014
Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling Allen, Andrew P.; Gillooly, James F. Ecology Letters, Vol. 12, Issue 5 https://doi.org/10.1111/j.1461-0248.2009.01302.x	journal	May 2009
Fundamental Connections Among Organism C:N:P Stoichiometry, Macromolecular Composition, and Growth Vrede, Tobias; Dobberfuhl, Dean R.; Kooijman, S. A. L. M. Ecology, Vol. 85, Issue 5 https://doi.org/10.1890/02-0249	journal	May 2004
Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M. Proceedings of the National Academy of Sciences, Vol. 112, Issue 35 https://doi.org/10.1073/pnas.1508382112	journal	August 2015
Functional traits explain phytoplankton community structure and seasonal dynamics in a marine ecosystem Edwards, Kyle F.; Litchman, Elena; Klausmeier, Christopher A. Ecology Letters, Vol. 16, Issue 1 https://doi.org/10.1111/ele.12012	journal	October 2012
Ocean nutrient ratios governed by plankton biogeography Weber, Thomas S.; Deutsch, Curtis Nature, Vol. 467, Issue 7315 https://doi.org/10.1038/nature09403	journal	September 2010
Evaluating community–environment relationships along fine to broad taxonomic resolutions reveals evolutionary forces underlying community assembly Lu, Hsiao-Pei; Yeh, Yi-Chun; Sastri, Akash R. The ISME Journal, Vol. 10, Issue 12 https://doi.org/10.1038/ismej.2016.78	journal	May 2016
Marine microorganisms and global nutrient cycles Arrigo, Kevin R. Nature, Vol. 437, Issue 7057 https://doi.org/10.1038/nature04159	journal	September 2004
A soil carbon proxy to predict CH4 and N2O emissions from rewetted agricultural peatlands Ye, Rongzhong; Espe, Matthew B.; Linquist, Bruce Agriculture, Ecosystems & Environment, Vol. 220 https://doi.org/10.1016/j.agee.2016.01.008	journal	March 2016
Microbial Nitrogen Limitation Increases Decomposition Craine, Joseph M.; Morrow, Carl; Fierer, Noah Ecology, Vol. 88, Issue 8 https://doi.org/10.1890/06-1847.1	journal	August 2007
Expanded microbial genome coverage and improved protein family annotation in the COG database Galperin, Michael Y.; Makarova, Kira S.; Wolf, Yuri I. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1223	journal	November 2014
Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling Goll, D. S.; Brovkin, V.; Parida, B. R. Biogeosciences, Vol. 9, Issue 9 https://doi.org/10.5194/bg-9-3547-2012	journal	January 2012
Nitrogen and phosphorus constrain labile and stable carbon turnover in lowland tropical forest soils Nottingham, Andrew T.; Turner, Benjamin L.; Stott, Andrew W. Soil Biology and Biochemistry, Vol. 80 https://doi.org/10.1016/j.soilbio.2014.09.012	journal	January 2015
Biogeographic patterns in below-ground diversity in New York City's Central Park are similar to those observed globally Ramirez, Kelly S.; Leff, Jonathan W.; Barberán, Albert Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1795 https://doi.org/10.1098/rspb.2014.1988	journal	November 2014
Exploiting rRNA operon copy number to investigate bacterial reproductive strategies Roller, Benjamin R. K.; Stoddard, Steven F.; Schmidt, Thomas M. Nature Microbiology, Vol. 1, Issue 11 https://doi.org/10.1038/nmicrobiol.2016.160	journal	September 2016
Microbial dormancy improves development and experimental validation of ecosystem model Wang, Gangsheng; Jagadamma, Sindhu; Mayes, Melanie A. The ISME Journal, Vol. 9, Issue 1 https://doi.org/10.1038/ismej.2014.120	journal	July 2014
Bridging the gap between omics and earth system science to better understand how environmental change impacts marine microbes Mock, Thomas; Daines, Stuart J.; Geider, Richard Global Change Biology, Vol. 22, Issue 1 https://doi.org/10.1111/gcb.12983	journal	July 2015
Linking Microbial and Ecosystem Ecology Using Ecological Stoichiometry: A Synthesis of Conceptual and Empirical Approaches Hall, E. K.; Maixner, F.; Franklin, O. Ecosystems, Vol. 14, Issue 2 https://doi.org/10.1007/s10021-010-9408-4	journal	December 2010
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
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
Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter Manzoni, Stefano; Trofymow, John A.; Jackson, Robert B. Ecological Monographs, Vol. 80, Issue 1 https://doi.org/10.1890/09-0179.1	journal	February 2010
Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients Fierer, Noah; Lauber, Christian L.; Ramirez, Kelly S. The ISME Journal, Vol. 6, Issue 5 https://doi.org/10.1038/ismej.2011.159	journal	December 2011
Elemental stoichiometry of a heterotrophic bacterial community in a freshwater lake: implications for growth- and resource-dependent variations Makino, W.; Cotner, Jb Aquatic Microbial Ecology, Vol. 34 https://doi.org/10.3354/ame034033	journal	January 2004
Ecological stoichiometry: An elementary approach using basic principles Hessen, Dag O.; Elser, James J.; Sterner, Robert W. Limnology and Oceanography, Vol. 58, Issue 6 https://doi.org/10.4319/lo.2013.58.6.2219	journal	November 2013
An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system Fanin, Nicolas; Fromin, Nathalie; Buatois, Bruno Ecology Letters, Vol. 16, Issue 6 https://doi.org/10.1111/ele.12108	journal	March 2013
RNA:protein ratio of the unicellular organism as a characteristic of phosphorous and nitrogen stoichiometry and of the cellular requirement of ribosomes for protein synthesis Karpinets, Tatiana V.; Greenwood, Duncan J.; Sams, Carl E. BMC Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1741-7007-4-30	journal	September 2006
Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton Edwards, Kyle F.; Thomas, Mridul K.; Klausmeier, Christopher A. Limnology and Oceanography, Vol. 57, Issue 2 https://doi.org/10.4319/lo.2012.57.2.0554	journal	March 2012
Microbial communities and their relevance for ecosystem models: Decomposition as a case study McGuire, Krista L.; Treseder, Kathleen K. Soil Biology and Biochemistry, Vol. 42, Issue 4 https://doi.org/10.1016/j.soilbio.2009.11.016	journal	April 2010
An enzymic 'latch' on a global carbon store Freeman, Chris; Ostle, Nick; Kang, Hojeong Nature, Vol. 409, Issue 6817 https://doi.org/10.1038/35051650	journal	January 2001
Biogeochemistry of paddy soils Kögel-Knabner, Ingrid; Amelung, Wulf; Cao, Zhihong Geoderma, Vol. 157, Issue 1-2 https://doi.org/10.1016/j.geoderma.2010.03.009	journal	June 2010
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
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data Hamady, Micah; Lozupone, Catherine; Knight, Rob The ISME Journal, Vol. 4, Issue 1 https://doi.org/10.1038/ismej.2009.97	journal	August 2009
metaxa 2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data Bengtsson-Palme, Johan; Hartmann, Martin; Eriksson, Karl Martin Molecular Ecology Resources, Vol. 15, Issue 6 https://doi.org/10.1111/1755-0998.12399	journal	March 2015
Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies: Functional traits of methane-oxidizing bacteria Ho, Adrian; Kerckhof, Frederiek-Maarten; Luke, Claudia Environmental Microbiology Reports, Vol. 5, Issue 3 https://doi.org/10.1111/j.1758-2229.2012.00370.x	journal	August 2012
Metabolic specialization and the assembly of microbial communities Johnson, David R.; Goldschmidt, Felix; Lilja, Elin E. The ISME Journal, Vol. 6, Issue 11 https://doi.org/10.1038/ismej.2012.46	journal	May 2012
Microbial control over carbon cycling in soil Schimel, Joshua P.; Schaeffer, Sean M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00348	journal	January 2012
Differential Growth Responses of Soil Bacterial Taxa to Carbon Substrates of Varying Chemical Recalcitrance Goldfarb, Katherine C.; Karaoz, Ulas; Hanson, China A. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00094	journal	January 2011
Explicitly representing soil microbial processes in Earth system models: Soil microbes in earth system models Wieder, William R.; Allison, Steven D.; Davidson, Eric A. Global Biogeochemical Cycles, Vol. 29, Issue 10 https://doi.org/10.1002/2015GB005188	journal	October 2015
rRNA Operon Copy Number Reflects Ecological Strategies of Bacteria Klappenbach, J. A.; Dunbar, J. M.; Schmidt, T. M. Applied and Environmental Microbiology, Vol. 66, Issue 4 https://doi.org/10.1128/AEM.66.4.1328-1333.2000	journal	April 2000
Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment: Evolutionary trade-offs among decomposers Treseder, Kathleen K.; Kivlin, Stephanie N.; Hawkes, Christine V. Ecology Letters, Vol. 14, Issue 9 https://doi.org/10.1111/j.1461-0248.2011.01650.x	journal	July 2011
Modeling Diverse Communities of Marine Microbes Follows, Michael J.; Dutkiewicz, Stephanie Annual Review of Marine Science, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-marine-120709-142848	journal	January 2011
A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production: A BIOGEOCHEMICAL MODEL OF C, N, AND P Wang, Y. -P.; Houlton, B. Z.; Field, C. B. Global Biogeochemical Cycles, Vol. 21, Issue 1 https://doi.org/10.1029/2006GB002797	journal	March 2007
Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes Ramirez, Kelly S.; Craine, Joseph M.; Fierer, Noah Global Change Biology, Vol. 18, Issue 6 https://doi.org/10.1111/j.1365-2486.2012.02639.x	journal	February 2012
Nitrogen and Lignin Control of Hardwood Leaf Litter Decomposition Dynamics Melillo, Jerry M.; Aber, John D.; Muratore, John F. Ecology, Vol. 63, Issue 3 https://doi.org/10.2307/1936780	journal	June 1982
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
The role of phosphorus dynamics in tropical forests – a modeling study using CLM-CNP Yang, X.; Thornton, P. E.; Ricciuto, D. M. Biogeosciences, Vol. 11, Issue 6 https://doi.org/10.5194/bg-11-1667-2014	journal	January 2014
Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change: Research review Sistla, Seeta A.; Schimel, Joshua P. New Phytologist, Vol. 196, Issue 1 https://doi.org/10.1111/j.1469-8137.2012.04234.x	journal	July 2012
Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems Ramirez, Kelly S.; Lauber, Christian L.; Knight, Rob Ecology, Vol. 91, Issue 12 https://doi.org/10.1890/10-0426.1	journal	December 2010
Constraints and Tradeoffs: Toward a Predictive Theory of Competition and Succession Tilman, David Oikos, Vol. 58, Issue 1 https://doi.org/10.2307/3565355	journal	May 1990
Biological stoichiometry from genes to ecosystems Elser, J. J.; Sterner, R. W.; Gorokhova, E. Ecology Letters, Vol. 3, Issue 6 https://doi.org/10.1046/j.1461-0248.2000.00185.x	journal	November 2000
Toward an Ecological Classification of soil Bacteria Fierer, Noah; Bradford, Mark A.; Jackson, Robert B. Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/05-1839	journal	June 2007
The global spectrum of plant form and function Díaz, Sandra; Kattge, Jens; Cornelissen, Johannes H. C. Nature, Vol. 529, Issue 7585 https://doi.org/10.1038/nature16489	journal	December 2015
Biological stoichiometry from genes to ecosystems Elser, J. J.; Sterner, R. W.; Gorokhova, E. Ecology Letters, Vol. 3, Issue 6 https://doi.org/10.1111/j.1461-0248.2000.00185.x	journal	November 2000
Microbial Dysbiosis During Simian Immunodeficiency Virus Infection is Partially Reverted with Combination Anti-retroviral Therapy Blum, Faith C.; Hardy, Britney L.; Bishop-Lilly, Kimberly A. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-63196-0	journal	April 2020
The role of phosphorus dynamics in tropical forests – a modeling study using CLM-CNP Yang, X.; Thornton, P. E.; Ricciuto, D. M. Biogeosciences Discussions, Vol. 10, Issue 8 https://doi.org/10.5194/bgd-10-14439-2013	journal	January 2013
Does Microbial Diversity Confound General Predictions? Duhamel, Marie; Peay, Kabir G. Trends in Plant Science, Vol. 20, Issue 11 https://doi.org/10.1016/j.tplants.2015.10.006	journal	November 2015
Importance of feedback loops between soil inorganic nitrogen and microbial communities in the heterotrophic soil respiration response to global warming Xu, Chonggang; Liang, Chao; Wullschleger, Stan Nature Reviews Microbiology, Vol. 9, Issue 3 https://doi.org/10.1038/nrmicro2439-c1	journal	February 2011
Primer and platform effects on 16S rRNA tag sequencing Alison, Fern,; Feng, Chen,; Julien, Tremblay, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/wgfs-e050	text	January 2015
Natural Antibiotic Resistance and Contamination by Antibiotic Resistance Determinants: The Two Ages in the Evolution of Resistance to Antimicrobials Martínez, José L. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00001	journal	January 2012
High resolution depth distribution of Bacteria, Archaea, methanotrophs, and methanogens in the bulk and rhizosphere soils of a flooded rice paddy Lee, Hyo Jung; Jeong, Sang Eun; Kim, Pil Joo Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00639	journal	June 2015
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? Graham, Emily B.; Knelman, Joseph E.; Schindlbacher, Andreas Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00214	journal	February 2016

Cited By (17)

The bioelements, the elementome, and the biogeochemical niche Peñuelas, Josep; Fernández‐Martínez, Marcos; Ciais, Philippe Ecology, Vol. 100, Issue 5 https://doi.org/10.1002/ecy.2652	journal	March 2019
Advancements in Microbial Genome Sequencing and Microbial Community Characterization Reddy, Bhaskar Microbial Genomics in Sustainable Agroecosystems https://doi.org/10.1007/978-981-13-8739-5_5	book	January 2019
Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea Albright, Michaeline B. N.; Timalsina, Bibek; Martiny, Jennifer B. H. Microbial Ecology, Vol. 77, Issue 3 https://doi.org/10.1007/s00248-018-1239-4	journal	August 2018
Effects of parent material on soil microbial biomass carbon and basal respiration within young afforested areas Babur, Emre Scandinavian Journal of Forest Research, Vol. 34, Issue 2 https://doi.org/10.1080/02827581.2018.1561936	journal	December 2018
Straw input can parallelly influence the bacterial and chemical characteristics of maize rhizosphere Li, Rong; Liu, Jun; Li, Jiani Environmental Pollutants and Bioavailability, Vol. 32, Issue 1 https://doi.org/10.1080/26395940.2019.1710260	journal	January 2020
Constraining Carbon and Nutrient Flows in Soil With Ecological Stoichiometry Buchkowski, Robert W.; Shaw, Alanna N.; Sihi, Debjani Frontiers in Ecology and Evolution, Vol. 7 https://doi.org/10.3389/fevo.2019.00382	journal	October 2019
Shrub Encroachment Shapes Soil Nutrient Concentration, Stoichiometry and Carbon Storage in an Abandoned Subalpine Grassland Ding, Leilei; Wang, Puchang; Zhang, Wen Sustainability, Vol. 11, Issue 6 https://doi.org/10.3390/su11061732	journal	March 2019
Cowpi: A Rumen Microbiome Focussed Version Of The Picrust Functional Inference Software Wilkinson, Toby James; Huws, Sharon Ann; Elizabeth, Edwards. Joan Zenodo https://doi.org/10.5281/zenodo.1252857	text	January 2018
Cowpi: A Rumen Microbiome Focussed Version Of The Picrust Functional Inference Software Wilkinson, Toby James; Huws, Sharon Ann; Elizabeth, Edwards. Joan Zenodo https://doi.org/10.5281/zenodo.1252858	text	January 2018
Constraining carbon and nutrient flows in soil with ecological stoichiometry Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani Zenodo https://doi.org/10.5281/zenodo.3464584	text	January 2019
Straw input can parallelly influence the bacterial and chemical characteristics of maize rhizosphere Li, Rong; Liu, Jun; Li, Jiani Taylor & Francis https://doi.org/10.6084/m9.figshare.11506416.v1	text	January 2020
Distinct microbial communities alter litter decomposition rates in a fertilized coastal plain wetland Koceja, Megan E.; Bledsoe, Regina B.; Goodwillie, Carol Ecosphere, Vol. 12, Issue 6 https://doi.org/10.1002/ecs2.3619	journal	June 2021
Multi 'omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone Graham, Emily B.; Crump, Alex R.; Kennedy, David W. Science of The Total Environment, Vol. 642 https://doi.org/10.1016/j.scitotenv.2018.05.256	journal	November 2018
Straw input can parallelly influence the bacterial and chemical characteristics of maize rhizosphere Li, Rong; Liu, Jun; Li, Jiani Taylor & Francis https://doi.org/10.6084/m9.figshare.11506416	text	January 2020
CowPI: A Rumen Microbiome Focussed Version of the PICRUSt Functional Inference Software Wilkinson, Toby J.; Huws, Sharon A.; Edwards, Joan E. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01095	journal	May 2018
Constraining carbon and nutrient flows in soil with ecological stoichiometry Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani Zenodo https://doi.org/10.5281/zenodo.3464585	text	January 2019
Rhizosphere Bacterial Community Structure and Predicted Functional Analysis in the Water-Level Fluctuation Zone of the Danjiangkou Reservoir in China During the Dry Period Chen, Zhao-Jin; Shao, Yang; Li, Ying-Jun International Journal of Environmental Research and Public Health, Vol. 17, Issue 4 https://doi.org/10.3390/ijerph17041266	journal	February 2020