Multifaceted Links Between Microbial Carbon Use Efficiency and Soil Organic Carbon Sequestration

Conceptual framework to unlock the mechanisms for microbial carbon use efficiency and SOC formation. Soil organic carbon (SOC) is the largest carbon (C) pool in terrestrial ecosystems. Even minor changes in the SOC pool can significantly impact soil fertility and climate change (Lal et al. 2018). The potential and scale of stable C pools are therefore paramount to global climate mitigation and local food security, whereas SOC sequestration is a critical determinant for the successful restoration of vulnerable ecosystems (Lu et al. 2018). SOC sequestration is a dynamic and continuous process encompassing both decomposition and stabilisation. Soil microorganisms, often regarded as key ‘engines’ of the Earth's biogeochemical cycles, play a dual regulatory role in regulating SOC formation and decomposition (Crowther et al. 2019). For instance, soil microorganisms decompose substrate C into carbon dioxide during growth and metabolism, resulting in the loss of SOC (Lehmann and Kleber 2015). Simultaneously, they can also promote SOC accumulation through the generation of microbial products and necromass, as suggested by the ‘microbial C pump’ (MCP) concept (Liang, Schimel, and Jastrow 2017). Although there are many pathways through which microorganisms affect SOC accumulation and decomposition, microbial C use efficiency (CUE) is an integrative metric that largely captures the balance of these processes. CUE describes the microbial partitioning of C utilised for metabolism that goes towards growth versus respiration (He et al. 2024). Current theory and biogeochemical models have widely demonstrated that CUE correlates positively with SOC. Tao et al. (2023) demonstrated that CUE is at least four times more influential in predicting SOC than other factors, including C input allocation, non-microbial C transfer, substrate decomposability, environmental modifications and vertical transport. However, some empirical studies indicated that high microbial CUE may have negligible effects or even produce declines in SOC (Kallenbach et al. 2016; Sokol et al. 2019). In a recent paper in Global Change Biology, along a 160-year vegetation restoration chronosequence, Shi et al. (2024) demonstrated a negative relationship between CUE and SOC. Combined with a meta-analysis, they first determined the prevalence of this relationship during natural restoration, highlighting the need for sustainable C sink management in mature forests. Moreover, they further revealed that afforestation-induced soil acidification is the main factor driving the inhibition of SOC storage by microbial CUE. From a microscopic perspective, the availability of organic substrates is lower in acidic soils than in alkaline soils, triggering additional SOC mineralisation by microorganisms (Malik et al. 2018). Overall, after long-term vegetation restoration to the mature forest stage, the SOC sequestration rate saturates and thereafter diminishes, resulting in a reduced capacity to mitigate climate change. This study offers solid evidence on the negative relationship between CUE and SOC, underscoring the need for cautious consideration of indiscriminate afforestation practices. Although microbial CUE has been widely reported as a strong predictor of SOC storage, its actual role is ambiguous in at least two ways. On the one hand, whether CUE is positively or negatively correlated with SOC storage is still under debate. On the other hand, the relative influence of CUE versus other controlling factors remains poorly resolved. This is because the formation of SOC is jointly affected by multiple biological, chemical and physical processes. More data on microbial growth, respiration and necromass are required to avoid biased analyses. Our current understanding of SOC stabilisation mechanisms is highly fragmented from empirical research. Establishing a globally causal link between CUE and SOC needs to fully leverage the potential of field observations, process-based models and machine learning (He et al. 2024). When considering the mechanistic processes involved in SOC formation, it is crucial not to oversimplify the intricate systems. The ‘mineral C pump’ (MnCP) concept has highlighted the pivotal role of soil minerals in enhancing SOC accumulation and stabilisation. Through various abiotic pathways, such as adsorption, occlusion, and aggregation, soil minerals associate with organic C to form stable organic–inorganic complexes, thereby promoting SOC sequestration (Xiao et al. 2023). Consequently, the relationship between CUE and SOC is also closely linked to MnCP. To better understand SOC storage and controlling processes, it is essential to monitor the interactions among microbial CUE, MCP and MnCP. A promising approach is to utilise isotope labelling methods to connect microbial life and death pathways with soil C cycling (Canarini et al. 2020). By integrating short- and long-term field tracing with state-of-the-art techniques, such as nano- and microscale imaging data (Xiao et al. 2023), we can decipher the microbial mechanisms underlying SOC accumulation, enabling the development of innovative land-based strategies under a changing climate. Linchuan Fang: conceptualization, writing – original draft, writing – review and editing. The author declares no conflicts of interest. Data sharing not applicable to this article as no datasets were generated or analysed for the current article.