Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth

Johnston, Eric R.; Kim, Minjae; Hatt, Janet K.; Phillips, Jana Randolph; Yao, Qiuming; Song, Yang; Hazen, Terry C.; Mayes, Melanie A.; Konstantinidis, Konstantinos T.

doi:10.1016/j.soilbio.2018.11.026

Title: Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth

Journal Article · 29 November 2018 · Soil Biology and Biochemistry

DOI: https://doi.org/10.1016/j.soilbio.2018.11.026 · OSTI ID:1502579

^[1]; Kim, Minjae ^[1]; Hatt, Janet K. ^[1]; Phillips, Jana Randolph ^[2]; Yao, Qiuming ^[2]; Song, Yang ^[2];

^[3];

^[2]; Konstantinidis, Konstantinos T. ^[1]

Georgia Inst. of Technology, Atlanta, GA (United States)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Tropical ecosystems are an important sink for atmospheric CO₂; however, plant growth is restricted by phosphorus (P) availability. Although soil microbiota facilitate organic P turnover and inorganic P mobilization, their role in carbon-phosphorus coupled processes remains poorly understood. To advance this topic, soils collected from four sites representing highly weathered tropical soils in the El Yunque National Forest, Puerto Rico were incubated with exogenous PO₄^3- under controlled laboratory conditions. P amendment increased CO₂ respiration by 14–23% relative to control incubations for soils sampled from all but the site with the greatest total and bioavailable soil P. Metatranscriptomics revealed an increase in the relative transcription of genes involved in cell growth and uptake of other nutrients in response to P amendment. A new methodology to normalize gene expression by population-level relative (DNA) abundance revealed that the pattern of increased transcription of cell growth and division genes with P amendment was community-wide. Soil communities responsive to P amendment possessed a greater relative abundance of α-glucosyl polysaccharide biosynthesis genes, suggestive of enhanced C storage under P-limiting conditions. Phosphorylase genes governing the degradation of α-glucosyl polysaccharides were also more abundant and increased in relative transcription with P amendment, indicating a shift from energy storage towards growth. Inversely, microbial communities in soils nonresponsive to P amendment were found to have metabolisms tuned for the phosphorolysis of labile plant-derived substrates, such as β-glucosyl polysaccharides. Accordingly, our results provided quantitative estimates of increased soil respiration upon alleviation of P constraints and elucidated several underlying ecological and molecular mechanisms involved in this response.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1502579

Journal Information:: Soil Biology and Biochemistry, Journal Name: Soil Biology and Biochemistry Journal Issue: C Vol. 130; ISSN 0038-0717

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (61)

Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils Silver, Whendee L.; Lugo, A. E.; Keller, M. Biogeochemistry, Vol. 44, Issue 3 https://doi.org/10.1007/BF00996995	journal	March 1999
Formation and function of the glycogen-like polysaccharide ofArthrobacter Zevenhuizen, L. P. T. M. Antonie van Leeuwenhoek, Vol. 32, Issue 1 https://doi.org/10.1007/BF02097485	journal	December 1966
Phosphorus Limitation of Microbial Processes in Moist Tropical Forests: Evidence from Short-term Laboratory Incubations and Field Studies Cleveland, Cory C.; Townsend, Alan R.; Schmidt, Steven K. Ecosystems, Vol. 5, Issue 7 https://doi.org/10.1007/s10021-002-0202-9	journal	November 2002
Variable Responses of Lowland Tropical Forest Nutrient Status to Fertilization and Litter Manipulation Sayer, Emma J.; Joseph Wright, S.; Tanner, Edmund V. J. Ecosystems, Vol. 15, Issue 3 https://doi.org/10.1007/s10021-011-9516-9	journal	January 2012
Parent Material and Topography Determine Soil Phosphorus Status in the Luquillo Mountains of Puerto Rico Mage, Susanna M.; Porder, Stephen Ecosystems, Vol. 16, Issue 2 https://doi.org/10.1007/s10021-012-9612-5	journal	November 2012
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
Short-term variability in labile soil phosphorus is positively related to soil moisture in a humid tropical forest in Puerto Rico Wood, Tana E.; Matthews, Danielle; Vandecar, Karen Biogeochemistry, Vol. 127, Issue 1 https://doi.org/10.1007/s10533-015-0150-z	journal	December 2015
Evaluation of methods to estimate the soil microbial biomass and the relationship with soil texture and organic matter Kaiser, E. A.; Mueller, T.; Joergensen, R. G. Soil Biology and Biochemistry, Vol. 24, Issue 7 https://doi.org/10.1016/0038-0717(92)90046-Z	journal	July 1992
Comparison of factors limiting bacterial growth in different soils Demoling, Fredrik; Figueroa, Daniela; Bååth, Erland Soil Biology and Biochemistry, Vol. 39, Issue 10 https://doi.org/10.1016/j.soilbio.2007.05.002	journal	October 2007
Effects of carbon additions on iron reduction and phosphorus availability in a humid tropical forest soil Liptzin, Daniel; Silver, Whendee L. Soil Biology and Biochemistry, Vol. 41, Issue 8 https://doi.org/10.1016/j.soilbio.2009.05.013	journal	August 2009
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
Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere Oren, Ram; Ellsworth, David S.; Johnsen, Kurt H. Nature, Vol. 411, Issue 6836 https://doi.org/10.1038/35078064	journal	May 2001
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
Estimating coverage in metagenomic data sets and why it matters Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. The ISME Journal, Vol. 8, Issue 11 https://doi.org/10.1038/ismej.2014.76	journal	May 2014
Experimental warming reveals positive feedbacks to climate change in the Eurasian Steppe Zhang, Ximei; Johnston, Eric R.; Li, Linghao The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2016.180	journal	December 2016
Capturing the genetic makeup of the active microbiome in situ Singer, Esther; Wagner, Michael; Woyke, Tanja The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.59	journal	June 2017
Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment Sinsabaugh, Robert L.; Hill, Brian H.; Follstad Shah, Jennifer J. Nature, Vol. 462, Issue 7274 https://doi.org/10.1038/nature08632	journal	December 2009
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
Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil Yao, Qiuming; Li, Zhou; Song, Yang Nature Ecology & Evolution, Vol. 2, Issue 3 https://doi.org/10.1038/s41559-017-0463-5	journal	January 2018
Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere Cleveland, C. C.; Townsend, A. R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 27 https://doi.org/10.1073/pnas.0600989103	journal	June 2006
Combined climate and carbon-cycle effects of large-scale deforestation Bala, G.; Caldeira, K.; Wickett, M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 16 https://doi.org/10.1073/pnas.0608998104	journal	April 2007
Survival of starving yeast is correlated with oxidative stress response and nonrespiratory mitochondrial function Petti, A. A.; Crutchfield, C. A.; Rabinowitz, J. D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 45 https://doi.org/10.1073/pnas.1101494108	journal	July 2011
Characterization of a thermophilic 4- O -β- d -mannosyl- d -glucose phosphorylase from Rhodothermus marinus Jaito, Nongluck; Saburi, Wataru; Odaka, Rei Bioscience, Biotechnology, and Biochemistry, Vol. 78, Issue 2 https://doi.org/10.1080/09168451.2014.882760	journal	February 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
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts611	journal	October 2012
PEAR: a fast and accurate Illumina Paired-End reAd mergeR Zhang, J.; Kobert, K.; Flouri, T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt593	journal	October 2013
Gene Graphics: a genomic neighborhood data visualization web application Harrison, Katherine J.; Crécy-Lagard, Valérie de; Zallot, Rémi Bioinformatics, Vol. 34, Issue 8 https://doi.org/10.1093/bioinformatics/btx793	journal	December 2017
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
FragGeneScan: predicting genes in short and error-prone reads Rho, Mina; Tang, Haixu; Ye, Yuzhen Nucleic Acids Research, Vol. 38, Issue 20 https://doi.org/10.1093/nar/gkq747	journal	August 2010
UniProt: a hub for protein information Consortium, UniPot Nucleic Acids Research, Vol. 43, Issue D1, p. D204-D212 https://doi.org/10.1093/nar/gku989	journal	October 2014
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
Glycogen and poly- -hydroxybutyrate synthesis in Spirulina maxima De Philippis, R.; Sili, C.; Vincenzini, M. Journal of General Microbiology, Vol. 138, Issue 8 https://doi.org/10.1099/00221287-138-8-1623	journal	August 1992
Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Zhang, H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 4 https://doi.org/10.1099/ijs.0.02520-0	journal	July 2003
Longimicrobium terrae gen. nov., sp. nov., an oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers Pascual, Javier; García-López, Marina; Bills, Gerald F. International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 5 https://doi.org/10.1099/ijsem.0.000974	journal	May 2016
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
Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis: Nutrients, climate and tropical NPP Cleveland, Cory C.; Townsend, Alan R.; Taylor, Philip Ecology Letters, Vol. 14, Issue 9 https://doi.org/10.1111/j.1461-0248.2011.01658.x	journal	July 2011
A Comparative Assessment of Factors Which Influence Microbial Biomass Carbon and Nitrogen Levels in soil Wardle, D. A. Biological Reviews, Vol. 67, Issue 3 https://doi.org/10.1111/j.1469-185X.1992.tb00728.x	journal	August 1992
Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distances Powers, Jennifer S.; Treseder, Kathleen K.; Lerdau, Manuel T. New Phytologist, Vol. 165, Issue 3 https://doi.org/10.1111/j.1469-8137.2004.01279.x	journal	December 2004
Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests Bonan, G. B. Science, Vol. 320, Issue 5882 https://doi.org/10.1126/science.1155121	journal	June 2008
Link between Phosphate Starvation and Glycogen Metabolism in Corynebacterium glutamicum, Revealed by Metabolomics Woo, H. M.; Noack, S.; Seibold, G. M. Applied and Environmental Microbiology, Vol. 76, Issue 20 https://doi.org/10.1128/AEM.01375-10	journal	August 2010
Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. Lillie, S. H.; Pringle, J. R. Journal of Bacteriology, Vol. 143, Issue 3 https://doi.org/10.1128/JB.143.3.1384-1394.1980	journal	January 1980
Role of Escherichia coli heat shock proteins DnaK and HtpG (C62.5) in response to nutritional deprivation Spence, J.; Cegielska, A.; Georgopoulos, C. Journal of Bacteriology, Vol. 172, Issue 12 https://doi.org/10.1128/JB.172.12.7157-7166.1990	journal	December 1990
Genetic assessment of stationary phase for cells of the yeast Saccharomyces cerevisiae Drebot, M. A.; Barnes, C. A.; Singer, R. A. Journal of Bacteriology, Vol. 172, Issue 7 https://doi.org/10.1128/JB.172.7.3584-3589.1990	journal	July 1990
Responses to nutrient starvation in Pseudomonas putida KT2442: two-dimensional electrophoretic analysis of starvation- and stress-induced proteins Givskov, M.; Eberl, L.; Molin, S. Journal of Bacteriology, Vol. 176, Issue 16 https://doi.org/10.1128/JB.176.16.4816-4824.1994	journal	August 1994
An essential role for the Escherichia coli DnaK protein in starvation-induced thermotolerance, H2O2 resistance, and reductive division Rockabrand, D.; Arthur, T.; Korinek, G. Journal of Bacteriology, Vol. 177, Issue 13 https://doi.org/10.1128/JB.177.13.3695-3703.1995	journal	July 1995
Nonpareil 3: Fast Estimation of Metagenomic Coverage and Sequence Diversity Rodriguez-R, Luis M.; Gunturu, Santosh; Tiedje, James M. mSystems, Vol. 3, Issue 3 https://doi.org/10.1128/mSystems.00039-18	journal	April 2018
Permafrost Meta-Omics and Climate Change Mackelprang, Rachel; Saleska, Scott R.; Jacobsen, Carsten Suhr Annual Review of Earth and Planetary Sciences, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-earth-060614-105126	journal	June 2016
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data Cox, Murray P.; Peterson, Daniel A.; Biggs, Patrick J. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-485	journal	September 2010
Mash: fast genome and metagenome distance estimation using MinHash Ondov, Brian D.; Treangen, Todd J.; Melsted, Páll Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0997-x	journal	June 2016
Distinct Microbial Limitations in Litter and Underlying Soil Revealed by Carbon and Nutrient Fertilization in a Tropical Rainforest Fanin, Nicolas; Barantal, Sandra; Fromin, Nathalie PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0049990	journal	December 2012
Variations in Belowground Carbon Storage and Soil CO2 Flux Rates along a Wet Tropical Climate Gradient1 McGroddy, Megan; Silver, Whendee L. BIOTROPICA, Vol. 32, Issue 4 https://doi.org/10.1646/0006-3606(2000)032[0614:VIBCSA]2.0.CO;2	journal	January 2000
Experimental Investigation of Nutrient Limitation of Forest Growth on wet Tropical Mountains Tanner, E. V. J.; Vitousek, P. M.; Cuevas, E. Ecology, Vol. 79, Issue 1 https://doi.org/10.1890/0012-9658(1998)079[0010:EIONLO]2.0.CO;2	journal	January 1998
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
Litterfall, Nutrient Cycling, and Nutrient Limitation in Tropical Forests Vitousek, Peter M. Ecology, Vol. 65, Issue 1 https://doi.org/10.2307/1939481	journal	February 1984
Gemmatirosa kalamazoonesis gen. nov., sp. nov., a member of the rarely-cultivated bacterial phylum Gemmatimonadetes DeBruyn, Jennifer M.; Fawaz, Mariam N.; Peacock, Aaron D. The Journal of General and Applied Microbiology, Vol. 59, Issue 4 https://doi.org/10.2323/jgam.59.305	journal	January 2013
The transcriptional response of microbial communities in thawing Alaskan permafrost soils Coolen, Marco J. L.; Orsi, William D. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00197	journal	March 2015
Metagenomics Reveals Pervasive Bacterial Populations and Reduced Community Diversity across the Alaska Tundra Ecosystem Johnston, Eric R.; Rodriguez-R, Luis M.; Luo, Chengwei Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00579	journal	April 2016

Cited By (2)

Seasonal changes in soil respiration linked to soil moisture and phosphorus availability along a tropical rainfall gradient Cusack, Daniela F.; Ashdown, Daniel; Dietterich, Lee H. Biogeochemistry, Vol. 145, Issue 3 https://doi.org/10.1007/s10533-019-00602-4	journal	September 2019
Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths Johnston, Eric R.; Hatt, Janet K.; He, Zhili Proceedings of the National Academy of Sciences, Vol. 116, Issue 30 https://doi.org/10.1073/pnas.1901307116	journal	July 2019

Similar Records

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

Journal Article · 2018 · Nature Ecology and Evolution · OSTI ID:1474724

Yao, Qiuming; Li, Zhou; Song, Yang; +9 more

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

Journal Article · 2018 · Nature Ecology and Evolution · OSTI ID:1439692

Yao, Qiuming; Li, Zhou; Song, Yang; +9 more

Community Proteogenomics Reveals the Systemic Impact of Phosphorus Availability on Microbial Functions in Tropical Soil

Journal Article · 2018 · Nature Ecology & Evolution · OSTI ID:1511464

Yao, Qiuming; Li, Zhou; Song, Yang; +9 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Metagenomics
Metatranscriptomics
RNA-seq
enzyme assays
microbial 19 ecology
phosphorus
soil microbiology
soil respiration
tropical ecosystem

Title: Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth

Citation Formats

References (61)

Cited By (2)

Similar Records

Related Subjects