Can the reductive dissolution of ferric iron in paddy soils compensate phosphorus limitation of rice plants and microorganisms?

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Chaoqun Wang
  • Lukas Thielemann
  • Michaela A Dippold
  • Georg Guggenberger
  • Yakov Kuzyakov
  • Callum C. Banfield
  • Tida Ge
  • Stephanie Günther
  • Patrick Bork
  • Marcus A. Horn
  • Maxim Dorodnikov

External Research Organisations

  • University of Göttingen
  • University of Tübingen
  • Ningbo University
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Details

Original languageEnglish
Article number108653
JournalSoil Biology and Biochemistry
Volume168
Early online date2 Apr 2022
Publication statusPublished - May 2022

Abstract

Biogeochemical cycles of phosphorus (P) and iron (Fe) are tightly interlinked, especially in highly weathered acidic subtropical and tropical soils rich in iron (oxyhydr)oxides (Fe(III)). The quantitative contribution of the reductive dissolution of Fe(III)-bound inorganic P (Pi) (Fe–P) in low-redox paddy soils may cover the demands of rice plants (Oryza sativa L.) and microorganisms. We hypothesized that microbially-driven Fe(III) reduction and dissolution can cover the P demand of microorganisms but not of the young rice plants when the plants’ P demand is high but their root systems are not sufficiently developed. We grew pre-germinated rice plants for 33 days in flooded rhizoboxes filled with a paddy soil of low P availability. 32P-labeled ferrihydrite (30.8 mg kg−1) was supplied either (1) in polyamide mesh bags (30 μm mesh size) to prevent roots from directly mobilizing Fe–P (pellets-in-mesh bag treatment), or (2) in the same pellet form but without a mesh bag to enable roots accessing the Fe–P (pellets-no-mesh bag treatment). Without mesh bags, Pi was more available leading to increases in microbial biomass carbon (MBC) by 18–55% and nitrogen (MBN) by 4–108% in rooted soil as compared to Pi pellets not directly available to roots. The maximum enzyme activities (Vmax) of phosphomonoesterase and β-glucosidase followed this pattern. During rice root growth, day 10 to day 33, MBC and microbial biomass phosphorus (MBP) contents in both rooted and bottom bulk (15–18 cm) soil gradually decreased by 28–56% and 47–49%, respectively. In contrast to our hypothesis, the contribution of Fe–P to MBP remarkably decreased from 4.5% to almost zero from 10 to 33 days after rice transplantation, while Fe–P compensated up to 16% of the plant P uptake at 33 days after rice transplantation, thus outcompeting microorganisms. Although both plants and microorganisms obtained Pi released by Fe(III) reductive dissolution, this mechanism was not sufficient for the demand of either organism groups.

Keywords

    Anoxic conditions, Enzyme activities, Fe and P interactions, Phosphorus availability and mobilization, Plant-microbial competition, Redox potential

ASJC Scopus subject areas

Cite this

Can the reductive dissolution of ferric iron in paddy soils compensate phosphorus limitation of rice plants and microorganisms? / Wang, Chaoqun; Thielemann, Lukas; Dippold, Michaela A et al.
In: Soil Biology and Biochemistry, Vol. 168, 108653, 05.2022.

Research output: Contribution to journalArticleResearchpeer review

Wang C, Thielemann L, Dippold MA, Guggenberger G, Kuzyakov Y, Banfield CC et al. Can the reductive dissolution of ferric iron in paddy soils compensate phosphorus limitation of rice plants and microorganisms? Soil Biology and Biochemistry. 2022 May;168:108653. Epub 2022 Apr 2. doi: 10.1016/j.soilbio.2022.108653
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@article{612ff0e9ff1f48a8b720557cbcc80634,
title = "Can the reductive dissolution of ferric iron in paddy soils compensate phosphorus limitation of rice plants and microorganisms?",
abstract = "Biogeochemical cycles of phosphorus (P) and iron (Fe) are tightly interlinked, especially in highly weathered acidic subtropical and tropical soils rich in iron (oxyhydr)oxides (Fe(III)). The quantitative contribution of the reductive dissolution of Fe(III)-bound inorganic P (Pi) (Fe–P) in low-redox paddy soils may cover the demands of rice plants (Oryza sativa L.) and microorganisms. We hypothesized that microbially-driven Fe(III) reduction and dissolution can cover the P demand of microorganisms but not of the young rice plants when the plants{\textquoteright} P demand is high but their root systems are not sufficiently developed. We grew pre-germinated rice plants for 33 days in flooded rhizoboxes filled with a paddy soil of low P availability. 32P-labeled ferrihydrite (30.8 mg kg−1) was supplied either (1) in polyamide mesh bags (30 μm mesh size) to prevent roots from directly mobilizing Fe–P (pellets-in-mesh bag treatment), or (2) in the same pellet form but without a mesh bag to enable roots accessing the Fe–P (pellets-no-mesh bag treatment). Without mesh bags, Pi was more available leading to increases in microbial biomass carbon (MBC) by 18–55% and nitrogen (MBN) by 4–108% in rooted soil as compared to Pi pellets not directly available to roots. The maximum enzyme activities (Vmax) of phosphomonoesterase and β-glucosidase followed this pattern. During rice root growth, day 10 to day 33, MBC and microbial biomass phosphorus (MBP) contents in both rooted and bottom bulk (15–18 cm) soil gradually decreased by 28–56% and 47–49%, respectively. In contrast to our hypothesis, the contribution of Fe–P to MBP remarkably decreased from 4.5% to almost zero from 10 to 33 days after rice transplantation, while Fe–P compensated up to 16% of the plant P uptake at 33 days after rice transplantation, thus outcompeting microorganisms. Although both plants and microorganisms obtained Pi released by Fe(III) reductive dissolution, this mechanism was not sufficient for the demand of either organism groups.",
keywords = "Anoxic conditions, Enzyme activities, Fe and P interactions, Phosphorus availability and mobilization, Plant-microbial competition, Redox potential",
author = "Chaoqun Wang and Lukas Thielemann and Dippold, {Michaela A} and Georg Guggenberger and Yakov Kuzyakov and Banfield, {Callum C.} and Tida Ge and Stephanie G{\"u}nther and Patrick Bork and Horn, {Marcus A.} and Maxim Dorodnikov",
note = "Funding Information: The authors gratefully acknowledge the China Scholarship Council (CSC) for financial support for Chaoqun Wang. This work was supported by the research grant from German Research Foundation (DO 1533/3-1; GU 406/33-1; HO4020/8-1). Michaela Dippold was funded by the Robert Bosch Junior Professorship. The authors would like to thank Bernd Kopka and Marvin Blaue of the Laboratory for Radioisotopes (LARI) of the University of Goettingen for their advice, support, and measurements. We also thank Jake Beyer and Dr. Florian Carstens for constructive advising as well as a technical staff of the Department of Agricultural Soil Science, University of Goettingen, Karin Schmidt, for microbial biomass carbon and nitrogen measurements. Funding Information: The authors gratefully acknowledge the China Scholarship Council (CSC) for financial support for Chaoqun Wang. This work was supported by the research grant from German Research Foundation ( DO 1533/3-1; GU 406/33-1; HO4020/8-1 ). Michaela Dippold was funded by the Robert Bosch Junior Professorship. The authors would like to thank Bernd Kopka and Marvin Blaue of the Laboratory for Radioisotopes (LARI) of the University of Goettingen for their advice, support, and measurements. We also thank Jake Beyer and Dr. Florian Carstens for constructive advising as well as a technical staff of the Department of Agricultural Soil Science, University of Goettingen, Karin Schmidt, for microbial biomass carbon and nitrogen measurements. ",
year = "2022",
month = may,
doi = "10.1016/j.soilbio.2022.108653",
language = "English",
volume = "168",
journal = "Soil Biology and Biochemistry",
issn = "0038-0717",
publisher = "Elsevier Ltd.",

}

Download

TY - JOUR

T1 - Can the reductive dissolution of ferric iron in paddy soils compensate phosphorus limitation of rice plants and microorganisms?

AU - Wang, Chaoqun

AU - Thielemann, Lukas

AU - Dippold, Michaela A

AU - Guggenberger, Georg

AU - Kuzyakov, Yakov

AU - Banfield, Callum C.

AU - Ge, Tida

AU - Günther, Stephanie

AU - Bork, Patrick

AU - Horn, Marcus A.

AU - Dorodnikov, Maxim

N1 - Funding Information: The authors gratefully acknowledge the China Scholarship Council (CSC) for financial support for Chaoqun Wang. This work was supported by the research grant from German Research Foundation (DO 1533/3-1; GU 406/33-1; HO4020/8-1). Michaela Dippold was funded by the Robert Bosch Junior Professorship. The authors would like to thank Bernd Kopka and Marvin Blaue of the Laboratory for Radioisotopes (LARI) of the University of Goettingen for their advice, support, and measurements. We also thank Jake Beyer and Dr. Florian Carstens for constructive advising as well as a technical staff of the Department of Agricultural Soil Science, University of Goettingen, Karin Schmidt, for microbial biomass carbon and nitrogen measurements. Funding Information: The authors gratefully acknowledge the China Scholarship Council (CSC) for financial support for Chaoqun Wang. This work was supported by the research grant from German Research Foundation ( DO 1533/3-1; GU 406/33-1; HO4020/8-1 ). Michaela Dippold was funded by the Robert Bosch Junior Professorship. The authors would like to thank Bernd Kopka and Marvin Blaue of the Laboratory for Radioisotopes (LARI) of the University of Goettingen for their advice, support, and measurements. We also thank Jake Beyer and Dr. Florian Carstens for constructive advising as well as a technical staff of the Department of Agricultural Soil Science, University of Goettingen, Karin Schmidt, for microbial biomass carbon and nitrogen measurements.

PY - 2022/5

Y1 - 2022/5

N2 - Biogeochemical cycles of phosphorus (P) and iron (Fe) are tightly interlinked, especially in highly weathered acidic subtropical and tropical soils rich in iron (oxyhydr)oxides (Fe(III)). The quantitative contribution of the reductive dissolution of Fe(III)-bound inorganic P (Pi) (Fe–P) in low-redox paddy soils may cover the demands of rice plants (Oryza sativa L.) and microorganisms. We hypothesized that microbially-driven Fe(III) reduction and dissolution can cover the P demand of microorganisms but not of the young rice plants when the plants’ P demand is high but their root systems are not sufficiently developed. We grew pre-germinated rice plants for 33 days in flooded rhizoboxes filled with a paddy soil of low P availability. 32P-labeled ferrihydrite (30.8 mg kg−1) was supplied either (1) in polyamide mesh bags (30 μm mesh size) to prevent roots from directly mobilizing Fe–P (pellets-in-mesh bag treatment), or (2) in the same pellet form but without a mesh bag to enable roots accessing the Fe–P (pellets-no-mesh bag treatment). Without mesh bags, Pi was more available leading to increases in microbial biomass carbon (MBC) by 18–55% and nitrogen (MBN) by 4–108% in rooted soil as compared to Pi pellets not directly available to roots. The maximum enzyme activities (Vmax) of phosphomonoesterase and β-glucosidase followed this pattern. During rice root growth, day 10 to day 33, MBC and microbial biomass phosphorus (MBP) contents in both rooted and bottom bulk (15–18 cm) soil gradually decreased by 28–56% and 47–49%, respectively. In contrast to our hypothesis, the contribution of Fe–P to MBP remarkably decreased from 4.5% to almost zero from 10 to 33 days after rice transplantation, while Fe–P compensated up to 16% of the plant P uptake at 33 days after rice transplantation, thus outcompeting microorganisms. Although both plants and microorganisms obtained Pi released by Fe(III) reductive dissolution, this mechanism was not sufficient for the demand of either organism groups.

AB - Biogeochemical cycles of phosphorus (P) and iron (Fe) are tightly interlinked, especially in highly weathered acidic subtropical and tropical soils rich in iron (oxyhydr)oxides (Fe(III)). The quantitative contribution of the reductive dissolution of Fe(III)-bound inorganic P (Pi) (Fe–P) in low-redox paddy soils may cover the demands of rice plants (Oryza sativa L.) and microorganisms. We hypothesized that microbially-driven Fe(III) reduction and dissolution can cover the P demand of microorganisms but not of the young rice plants when the plants’ P demand is high but their root systems are not sufficiently developed. We grew pre-germinated rice plants for 33 days in flooded rhizoboxes filled with a paddy soil of low P availability. 32P-labeled ferrihydrite (30.8 mg kg−1) was supplied either (1) in polyamide mesh bags (30 μm mesh size) to prevent roots from directly mobilizing Fe–P (pellets-in-mesh bag treatment), or (2) in the same pellet form but without a mesh bag to enable roots accessing the Fe–P (pellets-no-mesh bag treatment). Without mesh bags, Pi was more available leading to increases in microbial biomass carbon (MBC) by 18–55% and nitrogen (MBN) by 4–108% in rooted soil as compared to Pi pellets not directly available to roots. The maximum enzyme activities (Vmax) of phosphomonoesterase and β-glucosidase followed this pattern. During rice root growth, day 10 to day 33, MBC and microbial biomass phosphorus (MBP) contents in both rooted and bottom bulk (15–18 cm) soil gradually decreased by 28–56% and 47–49%, respectively. In contrast to our hypothesis, the contribution of Fe–P to MBP remarkably decreased from 4.5% to almost zero from 10 to 33 days after rice transplantation, while Fe–P compensated up to 16% of the plant P uptake at 33 days after rice transplantation, thus outcompeting microorganisms. Although both plants and microorganisms obtained Pi released by Fe(III) reductive dissolution, this mechanism was not sufficient for the demand of either organism groups.

KW - Anoxic conditions

KW - Enzyme activities

KW - Fe and P interactions

KW - Phosphorus availability and mobilization

KW - Plant-microbial competition

KW - Redox potential

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U2 - 10.1016/j.soilbio.2022.108653

DO - 10.1016/j.soilbio.2022.108653

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AN - SCOPUS:85127560407

VL - 168

JO - Soil Biology and Biochemistry

JF - Soil Biology and Biochemistry

SN - 0038-0717

M1 - 108653

ER -

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