DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

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 PO43- 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 storagemore » 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.« less

Authors:
ORCiD logo [1];  [1];  [1];  [2];  [2];  [2]; ORCiD logo [3]; ORCiD logo [2];  [1]
  1. Georgia Inst. of Technology, Atlanta, GA (United States)
  2. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
  3. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1502579
Alternate Identifier(s):
OSTI ID: 1636051
Grant/Contract Number:  
AC05-00OR22725; 1356288
Resource Type:
Accepted Manuscript
Journal Name:
Soil Biology and Biochemistry
Additional Journal Information:
Journal Volume: 130; Journal Issue: C; Journal ID: ISSN 0038-0717
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Metagenomics; Metatranscriptomics; RNA-seq; soil microbiology; microbial 19 ecology; enzyme assays; soil respiration; phosphorus; tropical ecosystem

Citation Formats

Johnston, Eric R., Kim, Minjae, Hatt, Janet K., Phillips, Jana Randolph, Yao, Qiuming, Song, Yang, Hazen, Terry C., Mayes, Melanie A., and Konstantinidis, Konstantinos T. Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth. United States: N. p., 2018. Web. doi:10.1016/j.soilbio.2018.11.026.
Johnston, Eric R., Kim, Minjae, Hatt, Janet K., Phillips, Jana Randolph, Yao, Qiuming, Song, Yang, Hazen, Terry C., Mayes, Melanie A., & Konstantinidis, Konstantinos T. Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth. United States. https://doi.org/10.1016/j.soilbio.2018.11.026
Johnston, Eric R., Kim, Minjae, Hatt, Janet K., Phillips, Jana Randolph, Yao, Qiuming, Song, Yang, Hazen, Terry C., Mayes, Melanie A., and Konstantinidis, Konstantinos T. Thu . "Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth". United States. https://doi.org/10.1016/j.soilbio.2018.11.026. https://www.osti.gov/servlets/purl/1502579.
@article{osti_1502579,
title = {Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth},
author = {Johnston, Eric R. and Kim, Minjae and Hatt, Janet K. and Phillips, Jana Randolph and Yao, Qiuming and Song, Yang and Hazen, Terry C. and Mayes, Melanie A. and Konstantinidis, Konstantinos T.},
abstractNote = {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 PO43- 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.},
doi = {10.1016/j.soilbio.2018.11.026},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 130,
place = {United States},
year = {Thu Nov 29 00:00:00 EST 2018},
month = {Thu Nov 29 00:00:00 EST 2018}
}

Journal Article:

Citation Metrics:
Cited by: 22 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Combined climate and carbon-cycle effects of large-scale deforestation
journal, April 2007

  • Bala, G.; Caldeira, K.; Wickett, M.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 16
  • DOI: 10.1073/pnas.0608998104

Responses of soil bacterial and fungal communities to extreme desiccation and rewetting
journal, July 2013

  • Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.104

BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere
journal, June 2006

  • Cleveland, C. C.; Townsend, A. R.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 27
  • DOI: 10.1073/pnas.0600989103

Phosphorus Limitation of Microbial Processes in Moist Tropical Forests: Evidence from Short-term Laboratory Incubations and Field Studies
journal, November 2002


The transcriptional response of microbial communities in thawing Alaskan permafrost soils
journal, March 2015


SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data
journal, September 2010

  • Cox, Murray P.; Peterson, Daniel A.; Biggs, Patrick J.
  • BMC Bioinformatics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2105-11-485

Gemmatirosa kalamazoonesis gen. nov., sp. nov., a member of the rarely-cultivated bacterial phylum Gemmatimonadetes
journal, January 2013

  • DeBruyn, Jennifer M.; Fawaz, Mariam N.; Peacock, Aaron D.
  • The Journal of General and Applied Microbiology, Vol. 59, Issue 4
  • DOI: 10.2323/jgam.59.305

Comparison of factors limiting bacterial growth in different soils
journal, October 2007


Glycogen and poly- -hydroxybutyrate synthesis in Spirulina maxima
journal, August 1992


Genetic assessment of stationary phase for cells of the yeast Saccharomyces cerevisiae
journal, July 1990


Distinct Microbial Limitations in Litter and Underlying Soil Revealed by Carbon and Nutrient Fertilization in a Tropical Rainforest
journal, December 2012


New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Gene Graphics: a genomic neighborhood data visualization web application
journal, December 2017


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

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Characterization of a thermophilic 4- O -β- d -mannosyl- d -glucose phosphorylase from Rhodothermus marinus
journal, February 2014

  • Jaito, Nongluck; Saburi, Wataru; Odaka, Rei
  • Bioscience, Biotechnology, and Biochemistry, Vol. 78, Issue 2
  • DOI: 10.1080/09168451.2014.882760

Metagenomics Reveals Pervasive Bacterial Populations and Reduced Community Diversity across the Alaska Tundra Ecosystem
journal, April 2016

  • Johnston, Eric R.; Rodriguez-R, Luis M.; Luo, Chengwei
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00579

Evaluation of methods to estimate the soil microbial biomass and the relationship with soil texture and organic matter
journal, July 1992


MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data
journal, October 2012


Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation.
journal, January 1980


Effects of carbon additions on iron reduction and phosphorus availability in a humid tropical forest soil
journal, August 2009


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


Permafrost Meta-Omics and Climate Change
journal, June 2016


Parent Material and Topography Determine Soil Phosphorus Status in the Luquillo Mountains of Puerto Rico
journal, November 2012


Mash: fast genome and metagenome distance estimation using MinHash
journal, June 2016


Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere
journal, May 2001

  • Oren, Ram; Ellsworth, David S.; Johnsen, Kurt H.
  • Nature, Vol. 411, Issue 6836
  • DOI: 10.1038/35078064

Longimicrobium terrae gen. nov., sp. nov., an oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers
journal, May 2016

  • Pascual, Javier; García-López, Marina; Bills, Gerald F.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 5
  • DOI: 10.1099/ijsem.0.000974

IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Survival of starving yeast is correlated with oxidative stress response and nonrespiratory mitochondrial function
journal, July 2011

  • Petti, A. A.; Crutchfield, C. A.; Rabinowitz, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 45
  • DOI: 10.1073/pnas.1101494108

Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distances
journal, December 2004


Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes
journal, February 2012


FragGeneScan: predicting genes in short and error-prone reads
journal, August 2010

  • Rho, Mina; Tang, Haixu; Ye, Yuzhen
  • Nucleic Acids Research, Vol. 38, Issue 20
  • DOI: 10.1093/nar/gkq747

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


An essential role for the Escherichia coli DnaK protein in starvation-induced thermotolerance, H2O2 resistance, and reductive division
journal, July 1995


Nonpareil 3: Fast Estimation of Metagenomic Coverage and Sequence Diversity
journal, April 2018


Estimating coverage in metagenomic data sets and why it matters
journal, May 2014

  • Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T.
  • The ISME Journal, Vol. 8, Issue 11
  • DOI: 10.1038/ismej.2014.76

Variable Responses of Lowland Tropical Forest Nutrient Status to Fertilization and Litter Manipulation
journal, January 2012


Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils
journal, March 1999

  • Silver, Whendee L.; Lugo, A. E.; Keller, M.
  • Biogeochemistry, Vol. 44, Issue 3
  • DOI: 10.1007/BF00996995

Capturing the genetic makeup of the active microbiome in situ
journal, June 2017

  • Singer, Esther; Wagner, Michael; Woyke, Tanja
  • The ISME Journal, Vol. 11, Issue 9
  • DOI: 10.1038/ismej.2017.59

Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment
journal, December 2009

  • Sinsabaugh, Robert L.; Hill, Brian H.; Follstad Shah, Jennifer J.
  • Nature, Vol. 462, Issue 7274
  • DOI: 10.1038/nature08632

Role of Escherichia coli heat shock proteins DnaK and HtpG (C62.5) in response to nutritional deprivation
journal, December 1990


Experimental Investigation of Nutrient Limitation of Forest Growth on wet Tropical Mountains
journal, January 1998


UniProt: a hub for protein information
journal, October 2014

  • Consortium, UniPot
  • Nucleic Acids Research, Vol. 43, Issue D1, p. D204-D212
  • DOI: 10.1093/nar/gku989

Litterfall, Nutrient Cycling, and Nutrient Limitation in Tropical Forests
journal, February 1984


Link between Phosphate Starvation and Glycogen Metabolism in Corynebacterium glutamicum, Revealed by Metabolomics
journal, August 2010

  • Woo, H. M.; Noack, S.; Seibold, G. M.
  • Applied and Environmental Microbiology, Vol. 76, Issue 20
  • DOI: 10.1128/AEM.01375-10

Short-term variability in labile soil phosphorus is positively related to soil moisture in a humid tropical forest in Puerto Rico
journal, December 2015


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

Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil
journal, January 2018


Formation and function of the glycogen-like polysaccharide ofArthrobacter
journal, December 1966

  • Zevenhuizen, L. P. T. M.
  • Antonie van Leeuwenhoek, Vol. 32, Issue 1
  • DOI: 10.1007/BF02097485

PEAR: a fast and accurate Illumina Paired-End reAd mergeR
journal, October 2013


Experimental warming reveals positive feedbacks to climate change in the Eurasian Steppe
journal, December 2016


Works referencing / citing this record:

Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths
journal, July 2019

  • Johnston, Eric R.; Hatt, Janet K.; He, Zhili
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 30
  • DOI: 10.1073/pnas.1901307116

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