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

Abstract

Tropical ecosystems are an important sink for atmospheric CO 2; 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 PO 4 3- under controlled laboratory conditions. P amendment increased CO 2 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 amore » 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.« 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 Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1502579
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: 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. 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., and Konstantinidis, Konstantinos T. Thu . "Phosphate addition increases tropical forest soil respiration primarily by deconstraining microbial population growth". United States. doi:10.1016/j.soilbio.2018.11.026.
@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},
issn = {0038-0717},
number = C,
volume = 130,
place = {United States},
year = {2018},
month = {11}
}

Journal Article:
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