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

Title: Soil Oxygen Limits Microbial Phosphorus Utilization in Humid Tropical Forest Soils

Abstract

Soil phosphorus (P) availability is of special interest in many humid tropical forests, especially those on highly weathered, iron (Fe)- and aluminum (Al)-rich soils where P often limits net primary productivity. Phosphorus cycling is partly dependent on the ability of microbes to compete for P with Fe and Al minerals, which strongly bind P. Soil P availability is also indirectly affected by soil redox conditions due to its effects on microbial activity and reductive dissolution of Fe oxides that may weaken Fe-O-P sorption strength. Here, we explored P sorption, soil Fe (II) concentrations, soil CO2 production, organic and inorganic P pools, and microbial biomass P in tropical soils that typically experience frequent low redox (valley soils), or fluctuating redox conditions (slope soils). Soils from both topographic positions were pre-incubated under oxic or anoxic headspaces and then amended with a mixture of P (as orthophosphate) and carbon (C, as acetate, to maintain microbial activity) and incubated in the dark for 24 h. Phosphorus sorption to the mineral phase occurred on a time scale of seconds to minutes in valley and slope soils, reflecting strong abiotic P sorption capacity. Valley soils were characterized by inherently higher Fe(II) concentrations and lower respiration rates.more » Under anoxic headspaces, Fe(II) concentrations increased 3-to 5-fold in the both soils. Soil respiration and microbial P utilization declined significantly in both soils under anoxic conditions, regardless of Fe(II) concentrations. Microbial P concentrations were highest when slope soils were incubated under an oxic headspace, despite the high P sorption under these conditions. Our results suggest that microbial P utilization is indirectly limited by low O2 availability and that microbes are able to effectively compete with minerals for P under Fe-oxidizing conditions. These results emphasize the central role of soil microorganisms in regulating P availability, even in the presence of strong abiotic sorption capacity.« less

Authors:
 [1];  [2]; ORCiD logo [3]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy, and Management; Ben Gurion Univ. of the Negev, Beer-Sheva (Israel). Dept. for Geography and Environmental Development
  2. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
  3. Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy, and Management
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1513130
Report Number(s):
LLNL-JRNL-738829
Journal ID: ISSN 2571-8789; 892108
Grant/Contract Number:  
AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
Soil Systems
Additional Journal Information:
Journal Volume: 2; Journal Issue: 4; Journal ID: ISSN 2571-8789
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; phosphorus availability; microbial biomass; tropical soils; iron reduction; anoxic conditions

Citation Formats

Gross, Avner, Pett-Ridge, Jennifer, and Silver, Whendee. Soil Oxygen Limits Microbial Phosphorus Utilization in Humid Tropical Forest Soils. United States: N. p., 2018. Web. doi:10.3390/soilsystems2040065.
Gross, Avner, Pett-Ridge, Jennifer, & Silver, Whendee. Soil Oxygen Limits Microbial Phosphorus Utilization in Humid Tropical Forest Soils. United States. https://doi.org/10.3390/soilsystems2040065
Gross, Avner, Pett-Ridge, Jennifer, and Silver, Whendee. Thu . "Soil Oxygen Limits Microbial Phosphorus Utilization in Humid Tropical Forest Soils". United States. https://doi.org/10.3390/soilsystems2040065. https://www.osti.gov/servlets/purl/1513130.
@article{osti_1513130,
title = {Soil Oxygen Limits Microbial Phosphorus Utilization in Humid Tropical Forest Soils},
author = {Gross, Avner and Pett-Ridge, Jennifer and Silver, Whendee},
abstractNote = {Soil phosphorus (P) availability is of special interest in many humid tropical forests, especially those on highly weathered, iron (Fe)- and aluminum (Al)-rich soils where P often limits net primary productivity. Phosphorus cycling is partly dependent on the ability of microbes to compete for P with Fe and Al minerals, which strongly bind P. Soil P availability is also indirectly affected by soil redox conditions due to its effects on microbial activity and reductive dissolution of Fe oxides that may weaken Fe-O-P sorption strength. Here, we explored P sorption, soil Fe (II) concentrations, soil CO2 production, organic and inorganic P pools, and microbial biomass P in tropical soils that typically experience frequent low redox (valley soils), or fluctuating redox conditions (slope soils). Soils from both topographic positions were pre-incubated under oxic or anoxic headspaces and then amended with a mixture of P (as orthophosphate) and carbon (C, as acetate, to maintain microbial activity) and incubated in the dark for 24 h. Phosphorus sorption to the mineral phase occurred on a time scale of seconds to minutes in valley and slope soils, reflecting strong abiotic P sorption capacity. Valley soils were characterized by inherently higher Fe(II) concentrations and lower respiration rates. Under anoxic headspaces, Fe(II) concentrations increased 3-to 5-fold in the both soils. Soil respiration and microbial P utilization declined significantly in both soils under anoxic conditions, regardless of Fe(II) concentrations. Microbial P concentrations were highest when slope soils were incubated under an oxic headspace, despite the high P sorption under these conditions. Our results suggest that microbial P utilization is indirectly limited by low O2 availability and that microbes are able to effectively compete with minerals for P under Fe-oxidizing conditions. These results emphasize the central role of soil microorganisms in regulating P availability, even in the presence of strong abiotic sorption capacity.},
doi = {10.3390/soilsystems2040065},
journal = {Soil Systems},
number = 4,
volume = 2,
place = {United States},
year = {Thu Nov 29 00:00:00 EST 2018},
month = {Thu Nov 29 00:00:00 EST 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Figure 1 Figure 1: Schematic illustration of the expected effects of redox conditions on Fe oxidation state, P sorption and microbial activity.

Save / Share:

Works referenced in this record:

Practical applications of ion exchange resins in agricultural and environmental soil research
journal, February 2002

  • Qian, P.; Schoenau, J. J.
  • Canadian Journal of Soil Science, Vol. 82, Issue 1
  • DOI: 10.4141/S00-091

Drought drives rapid shifts in tropical rainforest soil biogeochemistry and greenhouse gas emissions
journal, April 2018

  • O’Connell, Christine S.; Ruan, Leilei; Silver, Whendee L.
  • Nature Communications, Vol. 9, Issue 1
  • DOI: 10.1038/s41467-018-03352-3

The Structure, Distribution, and Biomass of the World's Forests
journal, November 2013


Properties and Management of Soils in the Tropics
journal, January 1977


Iron solid-phase differentiation along a redox gradient in basaltic soils
journal, January 2011

  • Thompson, Aaron; Rancourt, Denis G.; Chadwick, Oliver A.
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 1
  • DOI: 10.1016/j.gca.2010.10.005

Spatial patterns in oxygen and redox sensitive biogeochemistry in tropical forest soils
journal, November 2015


Redox Fluctuation Structures Microbial Communities in a Wet Tropical Soil
journal, November 2005


Incorporating phosphorus cycling into global modeling efforts: a worthwhile, tractable endeavor
journal, June 2015

  • Reed, Sasha C.; Yang, Xiaojuan; Thornton, Peter E.
  • New Phytologist, Vol. 208, Issue 2
  • DOI: 10.1111/nph.13521

Towards a conversion factor for soil microbial phosphorus
journal, May 2018


Temporal Dynamics in Soil Oxygen and Greenhouse Gases in Two Humid Tropical Forests
journal, December 2010


Iron Reduction and Soil Phosphorus Solubilization in Humid Tropical Forests Soils: The Roles of Labile Carbon Pools and an Electron Shuttle Compound
journal, March 2006


Iron(III) reduction and phosphorous solubilization in humid tropical forest soils
journal, July 2005


Multiple nutrients limit litterfall and decomposition in a tropical forest
journal, November 2007


Oxygen isotope ratios of plant available phosphate in lowland tropical forest soils
journal, September 2015


Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis: Errata
journal, November 2011


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

Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: a review
journal, August 2017

  • Menezes-Blackburn, Daniel; Giles, Courtney; Darch, Tegan
  • Plant and Soil, Vol. 427, Issue 1-2
  • DOI: 10.1007/s11104-017-3362-2

Anoxic microsites in upland soils dominantly controlled by clay content
journal, March 2018


Redox control of phosphorus pools in Hawaiian montane forest soils
journal, August 2001


Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions
journal, January 2010

  • Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z.
  • Ecological Applications, Vol. 20, Issue 1
  • DOI: 10.1890/08-0127.1

Redox Fluctuations Control the Coupled Cycling of Iron and Carbon in Tropical Forest Soils
journal, November 2018

  • Bhattacharyya, Amrita; Campbell, Ashley N.; Tfaily, Malak M.
  • Environmental Science & Technology, Vol. 52, Issue 24
  • DOI: 10.1021/acs.est.8b03408

Lignin decomposition is sustained under fluctuating redox conditions in humid tropical forest soils
journal, April 2015

  • Hall, Steven J.; Silver, Whendee L.; Timokhin, Vitaliy I.
  • Global Change Biology, Vol. 21, Issue 7
  • DOI: 10.1111/gcb.12908

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


Iron oxidation stimulates organic matter decomposition in humid tropical forest soils
journal, July 2013

  • Hall, Steven J.; Silver, Whendee L.
  • Global Change Biology, Vol. 19, Issue 9
  • DOI: 10.1111/gcb.12229

Nitrogen and phosphorus constrain labile and stable carbon turnover in lowland tropical forest soils
journal, January 2015


Measurement of soil microbial biomass phosphorus by an anion exchange membrane method
journal, October 1995


A modified single solution method for the determination of phosphate in natural waters
journal, January 1962


Influence of oxic/anoxic fluctuations on ammonia oxidizers and nitrification potential in a wet tropical soil
journal, April 2013

  • Pett-Ridge, Jennifer; Petersen, Dorthe G.; Nuccio, Erin
  • FEMS Microbiology Ecology, Vol. 85, Issue 1
  • DOI: 10.1111/1574-6941.12111

Biological and Geochemical Sinks for Phosphorus in Soil from a Wet Tropical Forest
journal, April 2004


The Mechanism of Phosphate Fixation by Iron Oxides1
journal, January 1975


Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium
journal, October 1998

  • Fredrickson, James K.; Zachara, John M.; Kennedy, David W.
  • Geochimica et Cosmochimica Acta, Vol. 62, Issue 19-20
  • DOI: 10.1016/S0016-7037(98)00243-9

Redistribution of Metals in a New Caledonia Ferralsol After Microbial Weathering
journal, January 2002

  • Quantin, C.; Becquer, T.; Rouiller, J. H.
  • Soil Science Society of America Journal, Vol. 66, Issue 6
  • DOI: 10.2136/sssaj2002.1797

Redox Fluctuations Frame Microbial Community Impacts on N-cycling Rates in a Humid Tropical Forest Soil
journal, July 2006

  • Pett-Ridge, Jennifer; Silver, Whendee L.; Firestone, Mary K.
  • Biogeochemistry, Vol. 81, Issue 1
  • DOI: 10.1007/s10533-006-9032-8

Breaking the enzymatic latch: impacts of reducing conditions on hydrolytic enzyme activity in tropical forest soils
journal, October 2014

  • Hall, Steven J.; Treffkorn, Jonathan; Silver, Whendee L.
  • Ecology, Vol. 95, Issue 10
  • DOI: 10.1890/13-2151.1

Refinement of the Anion Exchange Membrane Method for Soluble Phosphorus Measurement
journal, January 1999


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


Soil microbial biomass and the fate of phosphorus during long-term ecosystem development
journal, November 2012


Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction
journal, October 2006

  • Weber, Karrie A.; Achenbach, Laurie A.; Coates, John D.
  • Nature Reviews Microbiology, Vol. 4, Issue 10, p. 752-764
  • DOI: 10.1038/nrmicro1490

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


Soil organic phosphorus in lowland tropical rain forests
journal, June 2010


Measurement of microbial biomass phosphorus in soil
journal, January 1982


Phosphorus Fractionation Responds to Dynamic Redox Conditions in a Humid Tropical Forest Soil
journal, September 2018

  • Lin, Yang; Bhattacharyya, Amrita; Campbell, Ashley N.
  • Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 9
  • DOI: 10.1029/2018JG004420

Enhanced biological cycling of phosphorus increases its availability to crops in low-input sub-Saharan farming systems
journal, January 2006


CTE Soil Biogeochemistry 2014
dataset, January 2018


Niche differentiation and plasticity in soil phosphorus acquisition among co-occurring plants
journal, March 2020


An evolving view on biogeochemical cycling of iron
journal, February 2021


Variations in Belowground Carbon Storage and Soil CO2 Flux Rates along a Wet Tropical Climate Gradient1
journal, December 2000


CTE Soil Biogeochemistry 2014
dataset, January 2018


Works referencing / citing this record:

The role of soil redox conditions in microbial phosphorus cycling in humid tropical forests
journal, September 2019

  • Gross, Avner; Lin, Yang; Weber, Peter K.
  • Ecology, Vol. 101, Issue 2
  • DOI: 10.1002/ecy.2928

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.