Trade-offs in carbon-degrading enzyme activities limit long-term soil carbon sequestration with biochar addition

Jiao Feng, Dailin Yu, Robert L. Sinsabaugh, Daryl L. Moorhead, Mathias Neumann Andersen, Pete Smith, Yanting Song, Xinqi Li, Qiaoyun Huang, Yu-Rong Liu* (Corresponding Author), Ji Chen* (Corresponding Author)

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

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Abstract

Biochar amendment is one of the most promising agricultural approaches to tackle climate change by enhancing soil carbon (C) sequestration. Microbial-mediated decomposition processes are fundamental for the fate and persistence of sequestered C in soil, but the underlying mechanisms are uncertain. Here, we synthesise 923 observations regarding the effects of biochar addition (over periods ranging from several weeks to several years) on soil C-degrading enzyme activities from 130 articles across five continents worldwide. Our results showed that biochar addition increased soil ligninase activity targeting complex phenolic macromolecules by 7.1%, but suppressed cellulase activity degrading simpler polysaccharides by 8.3%. These shifts in enzyme activities explained the most variation of changes in soil C sequestration across a wide range of climatic, edaphic and experimental conditions, with biochar-induced shift in ligninase:cellulase ratio correlating negatively with soil C sequestration. Specifically, short-term (<1 year) biochar addition significantly reduced cellulase activity by 4.6% and enhanced soil organic C sequestration by 87.5%, whereas no significant responses were observed for ligninase activity and ligninase:cellulase ratio. However, long-term (≥1 year) biochar addition significantly enhanced ligninase activity by 5.2% and ligninase:cellulase ratio by 36.1%, leading to a smaller increase in soil organic C sequestration (25.1%). These results suggest that shifts in enzyme activities increased ligninase:cellulase ratio with time after biochar addition, limiting long-term soil C sequestration with biochar addition. Our work provides novel evidence to explain the diminished soil C sequestration with long-term biochar addition and suggests that earlier studies may have overestimated soil C sequestration with biochar addition by failing to consider the physiological acclimation of soil microorganisms over time.
Original languageEnglish
Pages (from-to)1184-1199
Number of pages16
JournalBiological Reviews
Volume98
Issue number4
Early online date13 Mar 2023
DOIs
Publication statusPublished - Aug 2023

Bibliographical note

ACKNOWLEDGEMENTS
We would like to thank all the authors whose data and work are included in this
meta-analysis. This study was supported by the National Natural Science Foundation of China (32071595, 41830756 and 42177022). We also thank the Fundamental Research Funds for the Central Universities (Program no. 2662019QD055). We acknowledge Cunbin Gao, Qianqian Zhao and Qin Liu for their assistance in data collection. Dr. Chen is granted by Aarhus Universitets Forskningsfond (AUFF-E-2019-7-1), EU H2020 Marie Skłodowska-Curie Actions (839806), Danish Independent Research Foundation (1127-00015B), and Nordic Committee of Agriculture and Food Research (https://nordicagriresearch.org/2020-5/

Data Availability Statement

The raw data used in the meta-analysis are available in the online digital repository figshare at https://doi.org/10.6084/m9.figshare.21769979.

Keywords

  • Biochar addition
  • enzyme activities
  • soil carbon sequestration
  • experimental duration
  • soil microorganism
  • meta-analysis
  • enzyme activity
  • biochar addition

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