Alternate wetting-drying had no preferences for rice P uptake but increased microbial P allocation to phospholipids: Evidence from dual 32P and 33P labeling

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Chaoqun Wang
  • Tianpeng Li
  • Michaela A. Dippold
  • Georg Guggenberger
  • Yakov Kuzyakov
  • Callum C. Banfield
  • Jan Muhr
  • Maxim Dorodnikov

Research Organisations

External Research Organisations

  • University of Göttingen
  • University of Münster
  • University of Tübingen
  • Chinese Academy of Sciences (CAS)
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Details

Original languageEnglish
Article number109359
Number of pages12
JournalSoil Biology and Biochemistry
Volume191
Early online date11 Feb 2024
Publication statusPublished - Apr 2024

Abstract

Alternate wetting-drying (AWD) in rice cultivation controls soil redox conditions and consequently nutrient solubility. Under low redox potential, ferric iron reduction leads to bound phosphate (Fe(III)–P) dissolution, but lack of oxygen retards organic phosphorus (Porg) mineralization. Microorganisms accelerate Porg mineralization as the redox potential increases during drying, but it is not known which P source will be preferentially taken up by microorganisms and plants. Using double 32/33P labeling, we traced for the first time the P released from inorganic (32P) and organic (33P) sources into microbial biomass P (MBP), phospholipids, and plants under continuous flooding (CF) and AWD. The CF rapidly induced reducing conditions that increased Fe–P dissolution and thus P availability. The AWD had no preference for 32P and 33P incorporation into plants. However, the ratios of 32P in roots to 32P in MBP or to 32P in phospholipids in rooted soil were 4–9 times higher than the respective ratios of 33P. Moreover, the ratios of 33P in roots to 33P in MBP or to 33P in phospholipids were always <0.6. Thus, plants and microorganisms were more competitive for P from Fe–P and from Porg, respectively. The AWD increased 32P and 33P incorporation into phospholipids in rooted soil by 53–56% as compared to CF. Also, the ratio of 32P in phospholipids to 32P in MBP was 1.4–2.2 times higher under AWD than under CF. Thus, AWD stimulated microorganisms to allocate more P for cell membrane synthesis as compared to CF. Plants were similarly effective to take up P from inorganic and organic sources. Increased root biomass stimulated arbuscular mycorrhizal symbiosis (represented by 16:1ω5c) and thus 33P recovery in roots under AWD. In turn, the acceleration of microbial P turnover and the microbe-specific preference for Porg highlight the importance of arbuscular mycorrhiza for plant P uptake under fluctuating water conditions.

Keywords

    Fe and P interactions, Organic P mineralization, Phospholipid fatty acids, Phosphorus isotopes, Phosphorus mobilization and immobilization, Plant-microbial competition

ASJC Scopus subject areas

Cite this

Alternate wetting-drying had no preferences for rice P uptake but increased microbial P allocation to phospholipids: Evidence from dual 32P and 33P labeling. / Wang, Chaoqun; Li, Tianpeng; Dippold, Michaela A. et al.
In: Soil Biology and Biochemistry, Vol. 191, 109359, 04.2024.

Research output: Contribution to journalArticleResearchpeer review

Wang C, Li T, Dippold MA, Guggenberger G, Kuzyakov Y, Banfield CC et al. Alternate wetting-drying had no preferences for rice P uptake but increased microbial P allocation to phospholipids: Evidence from dual 32P and 33P labeling. Soil Biology and Biochemistry. 2024 Apr;191:109359. Epub 2024 Feb 11. doi: 10.1016/j.soilbio.2024.109359
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title = "Alternate wetting-drying had no preferences for rice P uptake but increased microbial P allocation to phospholipids: Evidence from dual 32P and 33P labeling",
abstract = "Alternate wetting-drying (AWD) in rice cultivation controls soil redox conditions and consequently nutrient solubility. Under low redox potential, ferric iron reduction leads to bound phosphate (Fe(III)–P) dissolution, but lack of oxygen retards organic phosphorus (Porg) mineralization. Microorganisms accelerate Porg mineralization as the redox potential increases during drying, but it is not known which P source will be preferentially taken up by microorganisms and plants. Using double 32/33P labeling, we traced for the first time the P released from inorganic (32P) and organic (33P) sources into microbial biomass P (MBP), phospholipids, and plants under continuous flooding (CF) and AWD. The CF rapidly induced reducing conditions that increased Fe–P dissolution and thus P availability. The AWD had no preference for 32P and 33P incorporation into plants. However, the ratios of 32P in roots to 32P in MBP or to 32P in phospholipids in rooted soil were 4–9 times higher than the respective ratios of 33P. Moreover, the ratios of 33P in roots to 33P in MBP or to 33P in phospholipids were always <0.6. Thus, plants and microorganisms were more competitive for P from Fe–P and from Porg, respectively. The AWD increased 32P and 33P incorporation into phospholipids in rooted soil by 53–56% as compared to CF. Also, the ratio of 32P in phospholipids to 32P in MBP was 1.4–2.2 times higher under AWD than under CF. Thus, AWD stimulated microorganisms to allocate more P for cell membrane synthesis as compared to CF. Plants were similarly effective to take up P from inorganic and organic sources. Increased root biomass stimulated arbuscular mycorrhizal symbiosis (represented by 16:1ω5c) and thus 33P recovery in roots under AWD. In turn, the acceleration of microbial P turnover and the microbe-specific preference for Porg highlight the importance of arbuscular mycorrhiza for plant P uptake under fluctuating water conditions.",
keywords = "Fe and P interactions, Organic P mineralization, Phospholipid fatty acids, Phosphorus isotopes, Phosphorus mobilization and immobilization, Plant-microbial competition",
author = "Chaoqun Wang and Tianpeng Li and Dippold, {Michaela A.} and Georg Guggenberger and Yakov Kuzyakov and Banfield, {Callum C.} and Jan Muhr 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 ). The authors would like to thank Marvin Blaue of the Laboratory for Radioisotopes (LARI) of the University of G{\"o}ttingen for his advice, support, and measurements. We also thank Jake Beyer and Dr. Florian Carstens for constructive advice. ",
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Download

TY - JOUR

T1 - Alternate wetting-drying had no preferences for rice P uptake but increased microbial P allocation to phospholipids

T2 - Evidence from dual 32P and 33P labeling

AU - Wang, Chaoqun

AU - Li, Tianpeng

AU - Dippold, Michaela A.

AU - Guggenberger, Georg

AU - Kuzyakov, Yakov

AU - Banfield, Callum C.

AU - Muhr, Jan

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 ). The authors would like to thank Marvin Blaue of the Laboratory for Radioisotopes (LARI) of the University of Göttingen for his advice, support, and measurements. We also thank Jake Beyer and Dr. Florian Carstens for constructive advice.

PY - 2024/4

Y1 - 2024/4

N2 - Alternate wetting-drying (AWD) in rice cultivation controls soil redox conditions and consequently nutrient solubility. Under low redox potential, ferric iron reduction leads to bound phosphate (Fe(III)–P) dissolution, but lack of oxygen retards organic phosphorus (Porg) mineralization. Microorganisms accelerate Porg mineralization as the redox potential increases during drying, but it is not known which P source will be preferentially taken up by microorganisms and plants. Using double 32/33P labeling, we traced for the first time the P released from inorganic (32P) and organic (33P) sources into microbial biomass P (MBP), phospholipids, and plants under continuous flooding (CF) and AWD. The CF rapidly induced reducing conditions that increased Fe–P dissolution and thus P availability. The AWD had no preference for 32P and 33P incorporation into plants. However, the ratios of 32P in roots to 32P in MBP or to 32P in phospholipids in rooted soil were 4–9 times higher than the respective ratios of 33P. Moreover, the ratios of 33P in roots to 33P in MBP or to 33P in phospholipids were always <0.6. Thus, plants and microorganisms were more competitive for P from Fe–P and from Porg, respectively. The AWD increased 32P and 33P incorporation into phospholipids in rooted soil by 53–56% as compared to CF. Also, the ratio of 32P in phospholipids to 32P in MBP was 1.4–2.2 times higher under AWD than under CF. Thus, AWD stimulated microorganisms to allocate more P for cell membrane synthesis as compared to CF. Plants were similarly effective to take up P from inorganic and organic sources. Increased root biomass stimulated arbuscular mycorrhizal symbiosis (represented by 16:1ω5c) and thus 33P recovery in roots under AWD. In turn, the acceleration of microbial P turnover and the microbe-specific preference for Porg highlight the importance of arbuscular mycorrhiza for plant P uptake under fluctuating water conditions.

AB - Alternate wetting-drying (AWD) in rice cultivation controls soil redox conditions and consequently nutrient solubility. Under low redox potential, ferric iron reduction leads to bound phosphate (Fe(III)–P) dissolution, but lack of oxygen retards organic phosphorus (Porg) mineralization. Microorganisms accelerate Porg mineralization as the redox potential increases during drying, but it is not known which P source will be preferentially taken up by microorganisms and plants. Using double 32/33P labeling, we traced for the first time the P released from inorganic (32P) and organic (33P) sources into microbial biomass P (MBP), phospholipids, and plants under continuous flooding (CF) and AWD. The CF rapidly induced reducing conditions that increased Fe–P dissolution and thus P availability. The AWD had no preference for 32P and 33P incorporation into plants. However, the ratios of 32P in roots to 32P in MBP or to 32P in phospholipids in rooted soil were 4–9 times higher than the respective ratios of 33P. Moreover, the ratios of 33P in roots to 33P in MBP or to 33P in phospholipids were always <0.6. Thus, plants and microorganisms were more competitive for P from Fe–P and from Porg, respectively. The AWD increased 32P and 33P incorporation into phospholipids in rooted soil by 53–56% as compared to CF. Also, the ratio of 32P in phospholipids to 32P in MBP was 1.4–2.2 times higher under AWD than under CF. Thus, AWD stimulated microorganisms to allocate more P for cell membrane synthesis as compared to CF. Plants were similarly effective to take up P from inorganic and organic sources. Increased root biomass stimulated arbuscular mycorrhizal symbiosis (represented by 16:1ω5c) and thus 33P recovery in roots under AWD. In turn, the acceleration of microbial P turnover and the microbe-specific preference for Porg highlight the importance of arbuscular mycorrhiza for plant P uptake under fluctuating water conditions.

KW - Fe and P interactions

KW - Organic P mineralization

KW - Phospholipid fatty acids

KW - Phosphorus isotopes

KW - Phosphorus mobilization and immobilization

KW - Plant-microbial competition

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U2 - 10.1016/j.soilbio.2024.109359

DO - 10.1016/j.soilbio.2024.109359

M3 - Article

AN - SCOPUS:85185401718

VL - 191

JO - Soil Biology and Biochemistry

JF - Soil Biology and Biochemistry

SN - 0038-0717

M1 - 109359

ER -

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