Necromass responses to warming: A faster microbial turnover in favor of soil carbon stabilisation

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Jie Zhou
  • Yuan Liu
  • Chunyan Liu
  • Kazem Zamanian
  • Wenhao Feng
  • Samuel K. Steiner
  • Lingling Shi
  • Thomas Guillaume
  • Amit Kumar

Research Organisations

External Research Organisations

  • Nanjing Agricultural University
  • Lawrence Livermore National Laboratory
  • Nanjing Institute of Agricultural Sciences in Jiangsu Hilly Area
  • Chinese Academy of Agricultural Sciences
  • Agroscope
  • University of Tübingen
  • United Arab Emirates University
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Details

Original languageEnglish
Article number176651
JournalScience of the Total Environment
Volume954
Early online date5 Oct 2024
Publication statusE-pub ahead of print - 5 Oct 2024

Abstract

Microbial byproducts and residues (hereafter ‘necromass’) potentially play the most critical role in soil organic carbon (SOC) sequestration. However, little is known about the influence of climate warming on necromass accumulation in the agroecosystem and the underlying mechanisms associated with microbial life strategies. In order to address these knowledge gaps, we used amino sugars as biomarkers of microbial necromass, and investigated their variation through an 8-year trial in an agroecosystem with two warming levels (+1.6 and + 3.2 °C) compared to ambient temperature. The results showed that the lower warming level had no impact on total microbial necromass carbon. Conversely, warming the soil 3.2 °C above ambient increased total microbial necromass by 17 % and its contribution to SOC by 21.3 %, mainly by increasing fungal necromass (+19.8 %), whereas +3.2 °C warming had no impact on bacterial necromass. At the phylum level, compared with the ambient control, +3.2 °C warming induced an increase in the abundance of Proteobacteria and a decrease in both Acidobacteria and Actinobacteria, whereas in the fungal community, Ascomycota increased and Mortierellomycota decreased. This indicates that r-strategists outcompete K-strategists in warmer climates, which led to increased microbial necromass production and accumulation, as supported by the positive correlation between r-strategists and microbial necromass. Stronger microbial competition for resources also resulted in a higher biomass turnover rate, greater cell death, and greater production of microbial necromass. This was supported by the lower bacterial and fungal network complexity and trophic links under warming conditions. In addition, the necromass generated from accelerated microbial turnover further offsets warming-induced deceases in microbial biomass. Consequently, bulk SOC did not change, despite microbial necromass having a much greater response to warming than the soil C pool. Therefore, future climate warming may influence the composition and persistence of SOC during microbial degradation.

Keywords

    Agroecosystem, Global warming, Microbial life strategy, Microbial necromass, Soil carbon sequestration

ASJC Scopus subject areas

Sustainable Development Goals

Cite this

Necromass responses to warming: A faster microbial turnover in favor of soil carbon stabilisation. / Zhou, Jie; Liu, Yuan; Liu, Chunyan et al.
In: Science of the Total Environment, Vol. 954, 176651, 01.12.2024.

Research output: Contribution to journalArticleResearchpeer review

Zhou, J., Liu, Y., Liu, C., Zamanian, K., Feng, W., Steiner, S. K., Shi, L., Guillaume, T., & Kumar, A. (2024). Necromass responses to warming: A faster microbial turnover in favor of soil carbon stabilisation. Science of the Total Environment, 954, Article 176651. Advance online publication. https://doi.org/10.1016/j.scitotenv.2024.176651
Zhou J, Liu Y, Liu C, Zamanian K, Feng W, Steiner SK et al. Necromass responses to warming: A faster microbial turnover in favor of soil carbon stabilisation. Science of the Total Environment. 2024 Dec 1;954:176651. Epub 2024 Oct 5. doi: 10.1016/j.scitotenv.2024.176651
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title = "Necromass responses to warming: A faster microbial turnover in favor of soil carbon stabilisation",
abstract = "Microbial byproducts and residues (hereafter {\textquoteleft}necromass{\textquoteright}) potentially play the most critical role in soil organic carbon (SOC) sequestration. However, little is known about the influence of climate warming on necromass accumulation in the agroecosystem and the underlying mechanisms associated with microbial life strategies. In order to address these knowledge gaps, we used amino sugars as biomarkers of microbial necromass, and investigated their variation through an 8-year trial in an agroecosystem with two warming levels (+1.6 and + 3.2 °C) compared to ambient temperature. The results showed that the lower warming level had no impact on total microbial necromass carbon. Conversely, warming the soil 3.2 °C above ambient increased total microbial necromass by 17 % and its contribution to SOC by 21.3 %, mainly by increasing fungal necromass (+19.8 %), whereas +3.2 °C warming had no impact on bacterial necromass. At the phylum level, compared with the ambient control, +3.2 °C warming induced an increase in the abundance of Proteobacteria and a decrease in both Acidobacteria and Actinobacteria, whereas in the fungal community, Ascomycota increased and Mortierellomycota decreased. This indicates that r-strategists outcompete K-strategists in warmer climates, which led to increased microbial necromass production and accumulation, as supported by the positive correlation between r-strategists and microbial necromass. Stronger microbial competition for resources also resulted in a higher biomass turnover rate, greater cell death, and greater production of microbial necromass. This was supported by the lower bacterial and fungal network complexity and trophic links under warming conditions. In addition, the necromass generated from accelerated microbial turnover further offsets warming-induced deceases in microbial biomass. Consequently, bulk SOC did not change, despite microbial necromass having a much greater response to warming than the soil C pool. Therefore, future climate warming may influence the composition and persistence of SOC during microbial degradation.",
keywords = "Agroecosystem, Global warming, Microbial life strategy, Microbial necromass, Soil carbon sequestration",
author = "Jie Zhou and Yuan Liu and Chunyan Liu and Kazem Zamanian and Wenhao Feng and Steiner, {Samuel K.} and Lingling Shi and Thomas Guillaume and Amit Kumar",
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T1 - Necromass responses to warming

T2 - A faster microbial turnover in favor of soil carbon stabilisation

AU - Zhou, Jie

AU - Liu, Yuan

AU - Liu, Chunyan

AU - Zamanian, Kazem

AU - Feng, Wenhao

AU - Steiner, Samuel K.

AU - Shi, Lingling

AU - Guillaume, Thomas

AU - Kumar, Amit

N1 - Publisher Copyright: © 2024 Elsevier B.V.

PY - 2024/10/5

Y1 - 2024/10/5

N2 - Microbial byproducts and residues (hereafter ‘necromass’) potentially play the most critical role in soil organic carbon (SOC) sequestration. However, little is known about the influence of climate warming on necromass accumulation in the agroecosystem and the underlying mechanisms associated with microbial life strategies. In order to address these knowledge gaps, we used amino sugars as biomarkers of microbial necromass, and investigated their variation through an 8-year trial in an agroecosystem with two warming levels (+1.6 and + 3.2 °C) compared to ambient temperature. The results showed that the lower warming level had no impact on total microbial necromass carbon. Conversely, warming the soil 3.2 °C above ambient increased total microbial necromass by 17 % and its contribution to SOC by 21.3 %, mainly by increasing fungal necromass (+19.8 %), whereas +3.2 °C warming had no impact on bacterial necromass. At the phylum level, compared with the ambient control, +3.2 °C warming induced an increase in the abundance of Proteobacteria and a decrease in both Acidobacteria and Actinobacteria, whereas in the fungal community, Ascomycota increased and Mortierellomycota decreased. This indicates that r-strategists outcompete K-strategists in warmer climates, which led to increased microbial necromass production and accumulation, as supported by the positive correlation between r-strategists and microbial necromass. Stronger microbial competition for resources also resulted in a higher biomass turnover rate, greater cell death, and greater production of microbial necromass. This was supported by the lower bacterial and fungal network complexity and trophic links under warming conditions. In addition, the necromass generated from accelerated microbial turnover further offsets warming-induced deceases in microbial biomass. Consequently, bulk SOC did not change, despite microbial necromass having a much greater response to warming than the soil C pool. Therefore, future climate warming may influence the composition and persistence of SOC during microbial degradation.

AB - Microbial byproducts and residues (hereafter ‘necromass’) potentially play the most critical role in soil organic carbon (SOC) sequestration. However, little is known about the influence of climate warming on necromass accumulation in the agroecosystem and the underlying mechanisms associated with microbial life strategies. In order to address these knowledge gaps, we used amino sugars as biomarkers of microbial necromass, and investigated their variation through an 8-year trial in an agroecosystem with two warming levels (+1.6 and + 3.2 °C) compared to ambient temperature. The results showed that the lower warming level had no impact on total microbial necromass carbon. Conversely, warming the soil 3.2 °C above ambient increased total microbial necromass by 17 % and its contribution to SOC by 21.3 %, mainly by increasing fungal necromass (+19.8 %), whereas +3.2 °C warming had no impact on bacterial necromass. At the phylum level, compared with the ambient control, +3.2 °C warming induced an increase in the abundance of Proteobacteria and a decrease in both Acidobacteria and Actinobacteria, whereas in the fungal community, Ascomycota increased and Mortierellomycota decreased. This indicates that r-strategists outcompete K-strategists in warmer climates, which led to increased microbial necromass production and accumulation, as supported by the positive correlation between r-strategists and microbial necromass. Stronger microbial competition for resources also resulted in a higher biomass turnover rate, greater cell death, and greater production of microbial necromass. This was supported by the lower bacterial and fungal network complexity and trophic links under warming conditions. In addition, the necromass generated from accelerated microbial turnover further offsets warming-induced deceases in microbial biomass. Consequently, bulk SOC did not change, despite microbial necromass having a much greater response to warming than the soil C pool. Therefore, future climate warming may influence the composition and persistence of SOC during microbial degradation.

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