Taxonomic patterns in the nitrogen assimilation of soil prokaryotes
Abstract
Summary Nitrogen (N) is frequently a limiting nutrient in soil; its availability can govern ecosystem functions such as primary production and decomposition. Assimilation of N by microorganisms impacts the availability of N in soil. Despite its established ecological significance, the contributions of microbial taxa to N assimilation are unknown. Here we measure N uptake and use by microbial phylotypes and taxonomic groups within a diverse assemblage of soil microbes through quantitative stable isotope probing (qSIP) with 15 N. Following incubation with 15 , distinct patterns of 15 N assimilation among taxonomic groups were observed. For instance, glucose addition stimulated 15 N assimilation in most members of Actinobacteria and Proteobacteria but generally decreased 15 N use by Firmicutes and Bacteriodetes. While is considered a preferred and universal source of N to prokaryotes, the majority (> 80%) of N assimilation in our soils could be attributed to a handful of active orders. Characterizing N assimilation of taxonomic groups with 15 N qSIP may provide a basis for understanding how microbial community composition influences N availability in the environment.
- Authors:
-
- Center for Ecosystem Science and Society Northern Arizona University Flagstaff AZ USA, Division of Plant and Soil Sciences West Virginia University Morgantown WV USA
- Center for Ecosystem Science and Society Northern Arizona University Flagstaff AZ USA
- Center for Ecosystem Science and Society Northern Arizona University Flagstaff AZ USA, Department of Biological Sciences Northern Arizona University Flagstaff AZ USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1426319
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Name: Environmental Microbiology Journal Volume: 20 Journal Issue: 3; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Morrissey, Ember M., Mau, Rebecca L., Schwartz, Egbert, Koch, Benjamin J., Hayer, Michaela, and Hungate, Bruce A. Taxonomic patterns in the nitrogen assimilation of soil prokaryotes. United Kingdom: N. p., 2018.
Web. doi:10.1111/1462-2920.14051.
Morrissey, Ember M., Mau, Rebecca L., Schwartz, Egbert, Koch, Benjamin J., Hayer, Michaela, & Hungate, Bruce A. Taxonomic patterns in the nitrogen assimilation of soil prokaryotes. United Kingdom. https://doi.org/10.1111/1462-2920.14051
Morrissey, Ember M., Mau, Rebecca L., Schwartz, Egbert, Koch, Benjamin J., Hayer, Michaela, and Hungate, Bruce A. Wed .
"Taxonomic patterns in the nitrogen assimilation of soil prokaryotes". United Kingdom. https://doi.org/10.1111/1462-2920.14051.
@article{osti_1426319,
title = {Taxonomic patterns in the nitrogen assimilation of soil prokaryotes},
author = {Morrissey, Ember M. and Mau, Rebecca L. and Schwartz, Egbert and Koch, Benjamin J. and Hayer, Michaela and Hungate, Bruce A.},
abstractNote = {Summary Nitrogen (N) is frequently a limiting nutrient in soil; its availability can govern ecosystem functions such as primary production and decomposition. Assimilation of N by microorganisms impacts the availability of N in soil. Despite its established ecological significance, the contributions of microbial taxa to N assimilation are unknown. Here we measure N uptake and use by microbial phylotypes and taxonomic groups within a diverse assemblage of soil microbes through quantitative stable isotope probing (qSIP) with 15 N. Following incubation with 15 , distinct patterns of 15 N assimilation among taxonomic groups were observed. For instance, glucose addition stimulated 15 N assimilation in most members of Actinobacteria and Proteobacteria but generally decreased 15 N use by Firmicutes and Bacteriodetes. While is considered a preferred and universal source of N to prokaryotes, the majority (> 80%) of N assimilation in our soils could be attributed to a handful of active orders. Characterizing N assimilation of taxonomic groups with 15 N qSIP may provide a basis for understanding how microbial community composition influences N availability in the environment.},
doi = {10.1111/1462-2920.14051},
journal = {Environmental Microbiology},
number = 3,
volume = 20,
place = {United Kingdom},
year = {Wed Mar 14 00:00:00 EDT 2018},
month = {Wed Mar 14 00:00:00 EDT 2018}
}
https://doi.org/10.1111/1462-2920.14051
Web of Science
Works referenced in this record:
PROGRESSIVE NITROGEN LIMITATION OF ECOSYSTEM PROCESSES UNDER ELEVATED CO 2 IN A WARM-TEMPERATE FOREST
journal, January 2006
- Finzi, Adrien C.; Moore, David J. P.; DeLucia, Evan H.
- Ecology, Vol. 87, Issue 1
Small-scale spatial heterogeneity of ecosystem properties, microbial community composition and microbial activities in a temperate mountain forest soil
journal, September 2016
- Štursová, Martina; Bárta, Jiří; Šantrůčková, Hana
- FEMS Microbiology Ecology, Vol. 92, Issue 12
Microbial stoichiometry overrides biomass as a regulator of soil carbon and nitrogen cycling
journal, April 2015
- Buchkowski, Robert W.; Schmitz, Oswald J.; Bradford, Mark A.
- Ecology, Vol. 96, Issue 4
The Variability of the 16S rRNA Gene in Bacterial Genomes and Its Consequences for Bacterial Community Analyses
journal, February 2013
- Větrovský, Tomáš; Baldrian, Petr
- PLoS ONE, Vol. 8, Issue 2
Root-induced changes in nutrient cycling in forests depend on exudation rates
journal, November 2014
- Yin, Huajun; Wheeler, Emily; Phillips, Richard P.
- Soil Biology and Biochemistry, Vol. 78
Nitrogen mineralization, immobilization turnover, heterotrophic nitrification, and microbial groups in acid forest soils of subtropical China
journal, August 2012
- Zhu, Tongbin; Meng, Tianzhu; Zhang, Jinbo
- Biology and Fertility of Soils, Vol. 49, Issue 3
Variation in NH4+ mineralization and microbial communities with stand age in lodgepole pine (Pinus contorta) forests, Yellowstone National Park (USA)
journal, August 2005
- Smithwick, Erica A. H.; Turner, Monica G.; Metzger, Kristine L.
- Soil Biology and Biochemistry, Vol. 37, Issue 8
Effects of Plant Composition and Diversity on Nutrient Cycling
journal, February 1998
- Hooper, David U.; Vitousek, Peter M.
- Ecological Monographs, Vol. 68, Issue 1
Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests
journal, September 2016
- Kaiser, Kristin; Wemheuer, Bernd; Korolkow, Vera
- Scientific Reports, Vol. 6, Issue 1
Evolutionary history influences the salinity preference of bacterial taxa in wetland soils
journal, October 2015
- Morrissey, Ember M.; Franklin, Rima B.
- Frontiers in Microbiology, Vol. 6
Comparison of Sequencing Utility Programs
journal, January 2013
- Aronesty, Erik
- The Open Bioinformatics Journal, Vol. 7, Issue 1
Effect of phytoplankton cell size on transient-state nitrate and ammonium uptake kinetics
journal, May 1995
- Stolte, W.; Riegman, R.
- Microbiology, Vol. 141, Issue 5
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011
- McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
- The ISME Journal, Vol. 6, Issue 3
Pathways of nitrogen utilization by soil microorganisms – A review
journal, December 2010
- Geisseler, Daniel; Horwath, William R.; Joergensen, Rainer Georg
- Soil Biology and Biochemistry, Vol. 42, Issue 12
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package
journal, December 2011
- Revell, Liam J.
- Methods in Ecology and Evolution, Vol. 3, Issue 2
Potential nitrogen immobilization as influenced by available carbon in Japanese arable and forest soils
journal, November 2015
- Sawada, Kozue; Funakawa, Shinya; Toyota, Koki
- Soil Science and Plant Nutrition, Vol. 61, Issue 6
Phylogenetic organization of bacterial activity
journal, March 2016
- Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
- The ISME Journal, Vol. 10, Issue 9
Temperature Dependence of Inorganic Nitrogen Uptake: Reduced Affinity for Nitrate at Suboptimal Temperatures in Both Algae and Bacteria
journal, June 1999
- Reay, David S.; Nedwell, David B.; Priddle, Julian
- Applied and Environmental Microbiology, Vol. 65, Issue 6
Resistance, resilience, and redundancy in microbial communities
journal, August 2008
- Allison, S. D.; Martiny, J. B. H.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1
Identification of Nitrogen-Incorporating Bacteria in Petroleum-Contaminated Arctic Soils by Using [ 15 N]DNA-Based Stable Isotope Probing and Pyrosequencing
journal, April 2011
- Bell, Terrence H.; Yergeau, Etienne; Martineau, Christine
- Applied and Environmental Microbiology, Vol. 77, Issue 12
Atomic weights of the elements. Review 2000 (IUPAC Technical Report)
journal, January 2003
- de Laeter, John R.; Böhlke, John Karl; De Bièvre, P.
- Pure and Applied Chemistry, Vol. 75, Issue 6
Plant biomass, soil microbial community structure and nitrogen cycling under different organic amendment regimes; a 15N tracer-based approach
journal, November 2016
- Heijboer, Amber; ten Berge, Hein F. M.; de Ruiter, Peter C.
- Applied Soil Ecology, Vol. 107
Quantitative Microbial Ecology through Stable Isotope Probing
journal, August 2015
- Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert
- Applied and Environmental Microbiology, Vol. 81, Issue 21
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter
journal, April 2017
- Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
- The ISME Journal, Vol. 11, Issue 8
Bacterial nitrate reductases: Molecular and biological aspects of nitrate reduction
journal, May 2006
- González, P. J.; Correia, C.; Moura, Isabel
- Journal of Inorganic Biochemistry, Vol. 100, Issue 5-6
Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide
journal, November 2014
- Prober, Suzanne M.; Leff, Jonathan W.; Bates, Scott T.
- Ecology Letters, Vol. 18, Issue 1
DNA buoyant density shifts during 15N-DNA stable isotope probing
journal, September 2007
- Cupples, Alison M.; Shaffer, Elizabeth A.; Chee-Sanford, Joanne C.
- Microbiological Research, Vol. 162, Issue 4, p. 328-334
Prokaryotic Genome Size and SSU rDNA Copy Number: Estimation of Microbial Relative Abundance from a Mixed Population
journal, August 1999
- Fogel, G. B.; Collins, C. R.; Li, J.
- Microbial Ecology, Vol. 38, Issue 2, p. 93-113
Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest
journal, April 2005
- Balser, Teri C.; Firestone, Mary K.
- Biogeochemistry, Vol. 73, Issue 2
Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation: Rhizosphere feedbacks in CO2-enriched forests
journal, December 2010
- Phillips, Richard P.; Finzi, Adrien C.; Bernhardt, Emily S.
- Ecology Letters, Vol. 14, Issue 2
Nitrogen Mineralization and Productivity in 50 Hardwood and Conifer Stands on Diverse Soils
journal, March 1997
- Reich, Peter B.; Grigal, David F.; Aber, John D.
- Ecology, Vol. 78, Issue 2
Phylogenetic Analysis and Comparative Data: A Test and Review of Evidence
journal, December 2002
- Freckleton, R. P.; Harvey, P. H.; Pagel, M.
- The American Naturalist, Vol. 160, Issue 6
Global biogeography of microbial nitrogen-cycling traits in soil
journal, July 2016
- Nelson, Michaeline B.; Martiny, Adam C.; Martiny, Jennifer B. H.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 29
Nonlinear grassland responses to past and future atmospheric CO2
journal, May 2002
- Gill, Richard A.; Polley, H. Wayne; Johnson, Hyrum B.
- Nature, Vol. 417, Issue 6886
The role of Plant Diversity and Composition for Nitrate Leaching in Grasslands
journal, June 2003
- Scherer-Lorenzen, Michael; Palmborg, Cecilia; Prinz, Alexandra
- Ecology, Vol. 84, Issue 6
Microbial communities and their relevance for ecosystem models: Decomposition as a case study
journal, April 2010
- McGuire, Krista L.; Treseder, Kathleen K.
- Soil Biology and Biochemistry, Vol. 42, Issue 4
Technical considerations for the use of15N-DNA stable-isotope probing for functional microbial activity in soils
journal, January 2005
- Cadisch, Georg; Espana, Mingrelia; Causey, Rachel
- Rapid Communications in Mass Spectrometry, Vol. 19, Issue 11
Species effects on nitrogen cycling: a test with perennial grasses
journal, October 1990
- Wedin, David A.; Tilman, David
- Oecologia, Vol. 84, Issue 4
Stable Isotope Probing with 15N Achieved by Disentangling the Effects of Genome G+C Content and Isotope Enrichment on DNA Density
journal, March 2007
- Buckley, D. H.; Huangyutitham, V.; Hsu, S. -F.
- Applied and Environmental Microbiology, Vol. 73, Issue 10
ATMOSPHERIC SCIENCE: Nitrogen and Climate Change
journal, November 2003
- Hungate, B. A.
- Science, Vol. 302, Issue 5650
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
journal, September 2011
- Berry, David; Ben Mahfoudh, Karim; Wagner, Michael
- Applied and Environmental Microbiology, Vol. 77, Issue 21
13C and 15N natural abundance of the soil microbial biomass
journal, November 2006
- Dijkstra, Paul; Ishizu, Ayaka; Doucett, Richard
- Soil Biology and Biochemistry, Vol. 38, Issue 11
High Rate of Uptake of Organic Nitrogen Compounds by Prochlorococcus Cyanobacteria as a Key to Their Dominance in Oligotrophic Oceanic Waters
journal, February 2003
- Zubkov, M. V.; Fuchs, B. M.; Tarran, G. A.
- Applied and Environmental Microbiology, Vol. 69, Issue 2
CO2 enhancement of forest productivity constrained by limited nitrogen availability
journal, October 2010
- Norby, R. J.; Warren, J. M.; Iversen, C. M.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis: REVIEW Elevated CO2 and soil microorganisms
journal, July 2000
- Zak, Donald R.; Pregitzer, Kurt S.; King, John S.
- New Phytologist, Vol. 147, Issue 1
Identification of growing bacteria during litter decomposition in freshwater through H218O quantitative stable isotope probing: Growing bacteria during litter decomposition in freshwater
journal, October 2016
- Hayer, Michaela; Schwartz, Egbert; Marks, Jane C.
- Environmental Microbiology Reports, Vol. 8, Issue 6
Stable Isotope Probing with 15N2 Reveals Novel Noncultivated Diazotrophs in Soil
journal, March 2007
- Buckley, D. H.; Huangyutitham, V.; Hsu, S. -F.
- Applied and Environmental Microbiology, Vol. 73, Issue 10
Drivers of microbial respiration and net N mineralization at the continental scale
journal, May 2013
- Colman, Benjamin P.; Schimel, Joshua P.
- Soil Biology and Biochemistry, Vol. 60
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
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012
- Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
- The ISME Journal, Vol. 6, Issue 8
Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits are more Labile
journal, April 2003
- Blomberg, Simon P.; Garland, Theodore; Ives, Anthony R.
- Evolution, Vol. 57, Issue 4
Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed
journal, February 2008
- LeBauer, David S.; Treseder, Kathleen K.
- Ecology, Vol. 89, Issue 2
Microbial Immobilization of Nitrogen-15 Labelled Ammonium and Nitrate in an Agricultural Soil
journal, January 2015
- Romero, Carlos M.; Engel, Richard; Chen, Chengci
- Soil Science Society of America Journal, Vol. 79, Issue 2
Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions
journal, January 2014
- Byrnes, Jarrett E. K.; Gamfeldt, Lars; Isbell, Forest
- Methods in Ecology and Evolution, Vol. 5, Issue 2