Microbial carbon use efficiency promotes global soil carbon storage

nature Open access Published: 24 May 2023

Abstract

Soils store more carbon than other terrestrial ecosystems1,2. How soil organic carbon (SOC) forms and persists remains uncertain1,3, which makes it challenging to understand how it will respond to climatic change3,4. It has been suggested that soil microorganisms play an important role in SOC formation, preservation and loss5,6,7. Although microorganisms affect the accumulation and loss of soil organic matter through many pathways4,6,8,9,10,11, microbial carbon use efficiency (CUE) is an integrative metric that can capture the balance of these processes12,13. Although CUE has the potential to act as a predictor of variation in SOC storage, the role of CUE in SOC persistence remains unresolved7,14,15. Here we examine the relationship between CUE and the preservation of SOC, and interactions with climate, vegetation and edaphic properties, using a combination of global-scale datasets, a microbial-process explicit model, data assimilation, deep learning and meta-analysis. We find that CUE is at least four times as important as other evaluated factors, such as carbon input, decomposition or vertical transport, in determining SOC storage and its spatial variation across the globe. In addition, CUE shows a positive correlation with SOC content. Our findings point to microbial CUE as a major determinant of global SOC storage. Understanding the microbial processes underlying CUE and their environmental dependence may help the prediction of SOC feedback to a changing climate.

Main

Losses of soil organic carbon (SOC) could accelerate global warming, whereas sequestering carbon dioxide (CO2) into soils as SOC can help mitigate climate change2,16. How organic carbon is formed and preserved in the soil has been debated for over a century and remains controversial3,17,18. A classical paradigm emphasizes the roles of plant carbon inputs and soil organic matter decomposition in driving SOC storage and persistence. The rates of plant primary production determine the amount of organic carbon delivered to soils through litterfall, root turnover and exudation. In addition, organic matter decomposition is the major component in determining the rate of SOC loss, as soil decomposers (mainly microorganisms) break down organic matter and release carbon back to the atmosphere as CO2. Tremendous efforts have been made to track the quantity19 and decomposability20 of external carbon sources to soils, and their rate of decomposition21, variations in space and time22,23, and the nuanced interactions with complex local environments (for example, temperature, moisture and the soil mineral matrix)3,24,25. Nevertheless, studies of these controls have not led to sufficiently improved quantification of SOC storage26. The mechanisms underlying the magnitude of global SOC storage and its spatial distributions remain largely unknown27, hindering reliable projections of terrestrial biosphere feedback to a changing climate28.

Recent studies have highlighted the critical roles that soil microorganisms play not only in organic carbon loss via microbial decomposition8 but also in SOC formation and persistence as indicated by the covariance between microbial biomass, necromass and SOC content4,6,9,10,11 (Fig. 1). Although there are many pathways through which microorganisms affect both the accumulation and loss of soil organic matter, microbial carbon use efficiency (CUE) is an integrative metric that captures the balance of these processes. CUE describes the microbial partitioning of carbon used in metabolism that goes towards growth versus respiration and, thereby, expresses a dual microbial control point between SOC accumulation and loss. Although it has the potential to act as a strong predictor of variation in SOC storage around the world, the role of CUE in SOC persistence is ambiguous in at least two ways. First, whether CUE is positively or negatively correlated with SOC storage is under debate7,14,15. Second, the relative influence of CUE vis-a-vis other controls on SOC storage remains poorly resolved3,4. Here we examined the relationship between CUE and the preservation of carbon as SOC, and interactions with climate, vegetation and edaphic properties, using a combination of global-scale datasets, a microbial-process explicit model, data assimilation, deep learning and meta-analysis.

A high CUE promotes biosynthesis in microbial carbon metabolism12,13, causes the accumulation of microbial by-products and necromass that favours SOC formation (for example, via the entombing effect)5,9,29,30, and could generate a positive relationship between CUE and SOC storage (Fig. 1a). Alternatively, a high CUE promotes microbial biomass production, enhances extracellular enzyme production31 and could eventually trigger SOC loss over time (for example, via the priming effect)7,30,32 (Fig. 1b). If the second pathway dominates the role of CUE in SOC storage, a negative CUE–SOC relationship would be expected. To distinguish the relative strength of these two pathways, we first collated 132 pairs of measured CUE and SOC content at 46 locations across continents from 16 experimental studies previously published in the peer-reviewed literature (Extended Data Fig. 1a and Supplementary Table 1). Microbial CUE is positively correlated with SOC content after accounting for the methodological differences across studies (Fig. 2a and Extended Data Table 1). A high CUE not only accompanies high microbial biomass carbon but also has a positive correlation with non-microbial biomass carbon (that is, the remaining amount of organic carbon after excluding microbial biomass; Supplementary Table 2). Thus, our meta-analysis supports the idea that the first pathway plays a dominant role in SOC storage, and that high microbial CUE is mainly associated with high SOC storage. (Click here to continue reading from the original article)