Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Jun Cui
  • Zhenke Zhu
  • Xingliang Xu
  • Shoulong Liu
  • Davey L. Jones
  • Yakov Kuzyakov
  • Olga Shibistova
  • Jinshui Wu
  • Tida Ge

External Research Organisations

  • Chinese Academy of Sciences (CAS)
  • Yancheng Teachers University
  • Institute of Geographical Sciences and Natural Resources Research Chinese Academy of Sciences
  • Bangor University
  • University of Göttingen
  • Russian Academy of Sciences (RAS)
  • Kazan Volga Region Federal University
  • Peoples' Friendship University of Russia (RUDN)
  • Universidad de la Frontera
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Details

Original languageEnglish
Article number107720
JournalSoil Biology and Biochemistry
Volume142
Early online date17 Jan 2020
Publication statusPublished - Mar 2020
Externally publishedYes

Abstract

The impact of increasing amounts of labile C input on priming effects (PE) on soil organic matter (SOM) mineralization remains unclear, particularly under anoxic conditions and under high C input common in microbial hotspots. PE and their mechanisms were investigated by a 60-day incubation of three flooded paddy soils amended with13C-labeled glucose equivalent to 50–500% of microbial biomass C (MBC). PE (14–55% of unamended soil) peaked at moderate glucose addition rates (i.e., 50–300% of MBC). Glucose addition above 300% of MBC suppressed SOM mineralization but intensified microbial N acquisition, which contradicted the common PE mechanism of accelerating SOM decomposition for N-supply (frequently termed as “N mining”). Particularly at glucose input rate higher than 3 g kg−1 (i.e., 300–500% of MBC), mineral N content dropped on day 2 close to zero (1.1–2.5 mg N kg−1) because of microbial N immobilization. To cope with the N limitation, microorganisms greatly increased N-acetyl glucosaminidase and leucine aminopeptidase activities, while SOM decomposition decreased. Several discrete peaks of glucose-derived CO2 (contributing >80% to total CO2) were observed between days 13–30 under high glucose input (300–500% of MBC), concurrently with CH4 peaks. Such CO2 dynamics was distinct from the common exponential decay pattern, implicating the recycling and mineralization of 13C-enriched microbial necromass driven by glucose addition. Therefore, N recycling from necromass was hypothesized as a major mechanism to alleviate microbial N deficiency without SOM priming under excess labile C input. Compound-specific 13C-PLFA confirmed the redistribution of glucose-derived C among microbial groups, i.e., necromass recycling. Following glucose input, more than 4/5 of total 13C-PLFA was in the gram-negative and some non-specific bacteria, suggesting these microorganisms as r-strategists capable of rapidly utilizing the most labile C. However, their 13C-PLFA content decreased by 70% after 60 days, probably as a result of death of these r-strategists. On the contrary, the 13C-PLFA in gram-positive bacteria, actinomycetes and fungi (K-strategists) was initially minimal but increased by 0.5–5 folds between days 2 and 60. Consequently, the necromass of dead r-strategists provided a high-quality C–N source to the K-strategists. We conclude that under severe C excess, N recycling from necromass is a much more efficient microbial strategy to cover the acute N demand than N acquisition from the recalcitrant SOM.

Keywords

    Compound-specific C-PLFA analysis, Glucose mineralization, Necromass recycling, Priming effects, Soil carbon, Stoichiometric imbalance

ASJC Scopus subject areas

Cite this

Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming. / Cui, Jun; Zhu, Zhenke; Xu, Xingliang et al.
In: Soil Biology and Biochemistry, Vol. 142, 107720, 03.2020.

Research output: Contribution to journalArticleResearchpeer review

Cui, J., Zhu, Z., Xu, X., Liu, S., Jones, D. L., Kuzyakov, Y., Shibistova, O., Wu, J., & Ge, T. (2020). Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming. Soil Biology and Biochemistry, 142, Article 107720. https://doi.org/10.1016/j.soilbio.2020.107720
Cui J, Zhu Z, Xu X, Liu S, Jones DL, Kuzyakov Y et al. Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming. Soil Biology and Biochemistry. 2020 Mar;142:107720. Epub 2020 Jan 17. doi: 10.1016/j.soilbio.2020.107720
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@article{273770174bf14832b004abfc797aae26,
title = "Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming",
abstract = "The impact of increasing amounts of labile C input on priming effects (PE) on soil organic matter (SOM) mineralization remains unclear, particularly under anoxic conditions and under high C input common in microbial hotspots. PE and their mechanisms were investigated by a 60-day incubation of three flooded paddy soils amended with13C-labeled glucose equivalent to 50–500% of microbial biomass C (MBC). PE (14–55% of unamended soil) peaked at moderate glucose addition rates (i.e., 50–300% of MBC). Glucose addition above 300% of MBC suppressed SOM mineralization but intensified microbial N acquisition, which contradicted the common PE mechanism of accelerating SOM decomposition for N-supply (frequently termed as “N mining”). Particularly at glucose input rate higher than 3 g kg−1 (i.e., 300–500% of MBC), mineral N content dropped on day 2 close to zero (1.1–2.5 mg N kg−1) because of microbial N immobilization. To cope with the N limitation, microorganisms greatly increased N-acetyl glucosaminidase and leucine aminopeptidase activities, while SOM decomposition decreased. Several discrete peaks of glucose-derived CO2 (contributing >80% to total CO2) were observed between days 13–30 under high glucose input (300–500% of MBC), concurrently with CH4 peaks. Such CO2 dynamics was distinct from the common exponential decay pattern, implicating the recycling and mineralization of 13C-enriched microbial necromass driven by glucose addition. Therefore, N recycling from necromass was hypothesized as a major mechanism to alleviate microbial N deficiency without SOM priming under excess labile C input. Compound-specific 13C-PLFA confirmed the redistribution of glucose-derived C among microbial groups, i.e., necromass recycling. Following glucose input, more than 4/5 of total 13C-PLFA was in the gram-negative and some non-specific bacteria, suggesting these microorganisms as r-strategists capable of rapidly utilizing the most labile C. However, their 13C-PLFA content decreased by 70% after 60 days, probably as a result of death of these r-strategists. On the contrary, the 13C-PLFA in gram-positive bacteria, actinomycetes and fungi (K-strategists) was initially minimal but increased by 0.5–5 folds between days 2 and 60. Consequently, the necromass of dead r-strategists provided a high-quality C–N source to the K-strategists. We conclude that under severe C excess, N recycling from necromass is a much more efficient microbial strategy to cover the acute N demand than N acquisition from the recalcitrant SOM.",
keywords = "Compound-specific C-PLFA analysis, Glucose mineralization, Necromass recycling, Priming effects, Soil carbon, Stoichiometric imbalance",
author = "Jun Cui and Zhenke Zhu and Xingliang Xu and Shoulong Liu and Jones, {Davey L.} and Yakov Kuzyakov and Olga Shibistova and Jinshui Wu and Tida Ge",
note = "Funding information: The study was supported by the National Key Research and Development Program of China (2017YFD0800104), the National Natural Science Foundation of China (41430860, 41771337, 41977093 and 31872695), State Key Laboratory of Organic Geochemistry, GIGCAS (SKLOG-201728), Hunan Province Base for Scientific and Technological Innovation Cooperation (2018WK4012), the Youth Innovation Team Project of Institute of Subtropical Agriculture, Chinese Academy of Sciences (2017QNCXTD_GTD), NSFC-RFBR joint project (N 19-54-53026) and Innovation Groups of National Natural Science Foundation of Hunan Province (2019JJ10003). We thank the Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences for technical assistance. The publication was supported by the Government Program of Competitive Growth of Kazan Federal University and with the support of the “RUDN University program 5–100.” The study was supported by the National Key Research and Development Program of China ( 2017YFD0800104 ), the National Natural Science Foundation of China ( 41430860 , 41771337 , 41977093 and 31872695 ), State Key Laboratory of Organic Geochemistry , GIGCAS ( SKLOG-201728 ), Hunan Province Base for Scientific and Technological Innovation Cooperation ( 2018WK4012 ), the Youth Innovation Team Project of Institute of Subtropical Agriculture, Chinese Academy of Sciences ( 2017QNCXTD_GTD ), NSFC- RFBR joint project ( N 19-54-53026 ) and Innovation Groups of National Natural Science Foundation of Hunan Province ( 2019JJ10003 ). We thank the Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences for technical assistance. The publication was supported by the Government Program of Competitive Growth of Kazan Federal University and with the support of the “RUDN University program 5–100.”",
year = "2020",
month = mar,
doi = "10.1016/j.soilbio.2020.107720",
language = "English",
volume = "142",
journal = "Soil Biology and Biochemistry",
issn = "0038-0717",
publisher = "Elsevier Ltd.",

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Download

TY - JOUR

T1 - Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming

AU - Cui, Jun

AU - Zhu, Zhenke

AU - Xu, Xingliang

AU - Liu, Shoulong

AU - Jones, Davey L.

AU - Kuzyakov, Yakov

AU - Shibistova, Olga

AU - Wu, Jinshui

AU - Ge, Tida

N1 - Funding information: The study was supported by the National Key Research and Development Program of China (2017YFD0800104), the National Natural Science Foundation of China (41430860, 41771337, 41977093 and 31872695), State Key Laboratory of Organic Geochemistry, GIGCAS (SKLOG-201728), Hunan Province Base for Scientific and Technological Innovation Cooperation (2018WK4012), the Youth Innovation Team Project of Institute of Subtropical Agriculture, Chinese Academy of Sciences (2017QNCXTD_GTD), NSFC-RFBR joint project (N 19-54-53026) and Innovation Groups of National Natural Science Foundation of Hunan Province (2019JJ10003). We thank the Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences for technical assistance. The publication was supported by the Government Program of Competitive Growth of Kazan Federal University and with the support of the “RUDN University program 5–100.” The study was supported by the National Key Research and Development Program of China ( 2017YFD0800104 ), the National Natural Science Foundation of China ( 41430860 , 41771337 , 41977093 and 31872695 ), State Key Laboratory of Organic Geochemistry , GIGCAS ( SKLOG-201728 ), Hunan Province Base for Scientific and Technological Innovation Cooperation ( 2018WK4012 ), the Youth Innovation Team Project of Institute of Subtropical Agriculture, Chinese Academy of Sciences ( 2017QNCXTD_GTD ), NSFC- RFBR joint project ( N 19-54-53026 ) and Innovation Groups of National Natural Science Foundation of Hunan Province ( 2019JJ10003 ). We thank the Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences for technical assistance. The publication was supported by the Government Program of Competitive Growth of Kazan Federal University and with the support of the “RUDN University program 5–100.”

PY - 2020/3

Y1 - 2020/3

N2 - The impact of increasing amounts of labile C input on priming effects (PE) on soil organic matter (SOM) mineralization remains unclear, particularly under anoxic conditions and under high C input common in microbial hotspots. PE and their mechanisms were investigated by a 60-day incubation of three flooded paddy soils amended with13C-labeled glucose equivalent to 50–500% of microbial biomass C (MBC). PE (14–55% of unamended soil) peaked at moderate glucose addition rates (i.e., 50–300% of MBC). Glucose addition above 300% of MBC suppressed SOM mineralization but intensified microbial N acquisition, which contradicted the common PE mechanism of accelerating SOM decomposition for N-supply (frequently termed as “N mining”). Particularly at glucose input rate higher than 3 g kg−1 (i.e., 300–500% of MBC), mineral N content dropped on day 2 close to zero (1.1–2.5 mg N kg−1) because of microbial N immobilization. To cope with the N limitation, microorganisms greatly increased N-acetyl glucosaminidase and leucine aminopeptidase activities, while SOM decomposition decreased. Several discrete peaks of glucose-derived CO2 (contributing >80% to total CO2) were observed between days 13–30 under high glucose input (300–500% of MBC), concurrently with CH4 peaks. Such CO2 dynamics was distinct from the common exponential decay pattern, implicating the recycling and mineralization of 13C-enriched microbial necromass driven by glucose addition. Therefore, N recycling from necromass was hypothesized as a major mechanism to alleviate microbial N deficiency without SOM priming under excess labile C input. Compound-specific 13C-PLFA confirmed the redistribution of glucose-derived C among microbial groups, i.e., necromass recycling. Following glucose input, more than 4/5 of total 13C-PLFA was in the gram-negative and some non-specific bacteria, suggesting these microorganisms as r-strategists capable of rapidly utilizing the most labile C. However, their 13C-PLFA content decreased by 70% after 60 days, probably as a result of death of these r-strategists. On the contrary, the 13C-PLFA in gram-positive bacteria, actinomycetes and fungi (K-strategists) was initially minimal but increased by 0.5–5 folds between days 2 and 60. Consequently, the necromass of dead r-strategists provided a high-quality C–N source to the K-strategists. We conclude that under severe C excess, N recycling from necromass is a much more efficient microbial strategy to cover the acute N demand than N acquisition from the recalcitrant SOM.

AB - The impact of increasing amounts of labile C input on priming effects (PE) on soil organic matter (SOM) mineralization remains unclear, particularly under anoxic conditions and under high C input common in microbial hotspots. PE and their mechanisms were investigated by a 60-day incubation of three flooded paddy soils amended with13C-labeled glucose equivalent to 50–500% of microbial biomass C (MBC). PE (14–55% of unamended soil) peaked at moderate glucose addition rates (i.e., 50–300% of MBC). Glucose addition above 300% of MBC suppressed SOM mineralization but intensified microbial N acquisition, which contradicted the common PE mechanism of accelerating SOM decomposition for N-supply (frequently termed as “N mining”). Particularly at glucose input rate higher than 3 g kg−1 (i.e., 300–500% of MBC), mineral N content dropped on day 2 close to zero (1.1–2.5 mg N kg−1) because of microbial N immobilization. To cope with the N limitation, microorganisms greatly increased N-acetyl glucosaminidase and leucine aminopeptidase activities, while SOM decomposition decreased. Several discrete peaks of glucose-derived CO2 (contributing >80% to total CO2) were observed between days 13–30 under high glucose input (300–500% of MBC), concurrently with CH4 peaks. Such CO2 dynamics was distinct from the common exponential decay pattern, implicating the recycling and mineralization of 13C-enriched microbial necromass driven by glucose addition. Therefore, N recycling from necromass was hypothesized as a major mechanism to alleviate microbial N deficiency without SOM priming under excess labile C input. Compound-specific 13C-PLFA confirmed the redistribution of glucose-derived C among microbial groups, i.e., necromass recycling. Following glucose input, more than 4/5 of total 13C-PLFA was in the gram-negative and some non-specific bacteria, suggesting these microorganisms as r-strategists capable of rapidly utilizing the most labile C. However, their 13C-PLFA content decreased by 70% after 60 days, probably as a result of death of these r-strategists. On the contrary, the 13C-PLFA in gram-positive bacteria, actinomycetes and fungi (K-strategists) was initially minimal but increased by 0.5–5 folds between days 2 and 60. Consequently, the necromass of dead r-strategists provided a high-quality C–N source to the K-strategists. We conclude that under severe C excess, N recycling from necromass is a much more efficient microbial strategy to cover the acute N demand than N acquisition from the recalcitrant SOM.

KW - Compound-specific C-PLFA analysis

KW - Glucose mineralization

KW - Necromass recycling

KW - Priming effects

KW - Soil carbon

KW - Stoichiometric imbalance

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U2 - 10.1016/j.soilbio.2020.107720

DO - 10.1016/j.soilbio.2020.107720

M3 - Article

AN - SCOPUS:85078001183

VL - 142

JO - Soil Biology and Biochemistry

JF - Soil Biology and Biochemistry

SN - 0038-0717

M1 - 107720

ER -