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Review

The Response Mechanism of Soil Microbial Carbon Use Efficiency to Land-Use Change: A Review

Engineering Research Center of Agricultural Microbiology Technology, Ministry of Education & Heilongjiang Provincial Key Laboratory of Ecological Restoration and Resource Utilization for Cold Region & Key Laboratory of Microbiology, College of Heilongjiang Province & School of Life Sciences, Heilongjiang University, Harbin 150080, China
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Author to whom correspondence should be addressed.
Sustainability 2025, 17(15), 7023; https://doi.org/10.3390/su17157023 (registering DOI)
Submission received: 9 June 2025 / Revised: 23 July 2025 / Accepted: 30 July 2025 / Published: 2 August 2025
(This article belongs to the Special Issue Soil Ecology and Carbon Cycle)

Abstract

Microbial carbon use efficiency (CUE) is an important indicator of soil organic carbon accumulation and loss and a key parameter in biogeochemical cycling models. Its regulatory mechanism is highly dependent on microbial communities and their dynamic mediation of abiotic factors. Land-use change (e.g., agricultural expansion, deforestation, urbanization) profoundly alter carbon input patterns and soil physicochemical properties, further exacerbating the complexity and uncertainty of CUE. Existing carbon cycle models often neglect microbial ecological processes, resulting in an incomplete understanding of how microbial traits interact with environmental factors to regulate CUE. This paper provides a comprehensive review of the microbial regulation mechanisms of CUE under land-use change and systematically explores how microorganisms drive organic carbon allocation through community compositions, interspecies interactions, and environmental adaptability, with particular emphasis on the synergistic response between microbial communities and abiotic factors. We found that the buffering effect of microbial communities on abiotic factors during land-use change is a key factor determining CUE change patterns. This review not only provides a theoretical framework for clarifying the microbial-dominated carbon turnover mechanism but also lays a scientific foundation for the precise implementation of sustainable land management and carbon neutrality goals.

1. Introduction

Land-use change refers to the transformation of land cover types caused by human activities, and it profoundly impacts the global carbon cycle and ecosystem stability [1]. Under the context of land-use change, soil microbial carbon use efficiency (CUE) has garnered significant attention in carbon cycle-related research as a key microbial characteristic that directly affects soil organic carbon (SOC) dynamics [2]. A higher CUE indicates that more carbon is retained in the microbial biomass, which ultimately contributes to the formation of stable SOC through the decomposition of microbial residues, thereby promoting long-term carbon stabilization and enhancing the carbon-storage capacity of ecosystems [3]. When CUE is low, a greater proportion of carbon is released back into the atmosphere as CO2, accelerating the soil carbon turnover rate. Existing carbon cycle models generally ignore soil microbial communities and their ecological processes, leading to significant biases in predicting SOC dynamics and their response to climate change [4]. Incorporating microbial carbon allocation strategies (microbial CUE) into models can provide a comprehensive understanding of microbially mediated carbon cycle pathways [5]. However, most carbon cycle models either lack microbial CUE indicators or treat them as constants [6]. Therefore, scientifically assessing CUE and accurately integrating it into soil carbon models remains a major challenge.
Given the key role of CUE in carbon cycle models and its inherent dynamic characteristics, it is particularly important to understand the key factors driving these dynamic changes (Figure 1). CUE is strictly regulated by the trade-offs between microbial growth and respiration, extracellular enzyme production, substrate utilization efficiency, and nutrient acquisition strategies. At the same time, these ecological processes are influenced by changes in soil physical and chemical properties, resource availability, and microbial communities caused by land-use change. This paper reviews the definition and measurement methods of CUE, and based on recent research findings, summarizes the variability characteristics of CUE under different land-use changes and their main influencing factors. It emphasizes the core driving role of microorganisms in regulating CUE as well as their synergistic response and dynamic coupling with abiotic environmental factors (e.g., soil temperature, humidity, pH, resources, and their stoichiometric ratios.).
The core objectives of this review were to (1) systematically integrate microbial communities as active regulators of the core drivers of CUE in response to land-use change and its induced changes in environmental factors; (2) deeply analyze how microbial response strategies dynamically couple with abiotic factors to jointly determine the direction and magnitude of CUE changes under land-use change; (3) emphasize that microbially mediated biotic–abiotic synergistic responses under land-use change are critical for understanding the complexity and uncertainty of CUE. In-depth investigation of the response patterns and regulatory mechanisms of microbial CUE under land-use change not only is essential for uncovering the microbial mechanisms driving the carbon cycle, but also holds significant implications for predicting and assessing soil carbon dynamics under land use change and formulating carbon management strategies for sustainability.

2. Definition of CUE and Its Impact on SOC

Microbial CUE refers to the efficiency with which microorganisms convert absorbed carbon into their own biomass, reflecting their allocation strategy for SOC. It is typically expressed as the ratio of microbial growth to absorption. Microorganisms absorb carbon from the external environment primarily for four purposes: microbial growth, respiratory metabolism, secretion of extracellular enzymes and metabolic products, and microbial death. In natural ecosystems, compared with growth and respiration, the other two processes consume so little carbon that they are considered negligible [7,8]. Essentially, CUE refers to the balance between the processes of growth and respiration. A high CUE value indicates that microorganisms use more carbon for biomass synthesis, which helps increase soil carbon storage, while a low CUE value means that more carbon is used for respiration, leading to carbon release [9].
Microorganisms regulate CUE in response to environmental changes induced by land-use change, creating positive or negative feedback on SOC accumulation. Positive feedback is reflected in high CUE, meaning SOC accumulation, and low CUE, meaning SOC loss. The microbial growth–respiratory trade-off is the core regulatory mechanism of CUE. At higher CUE, microorganisms tend to reduce the secretion of degradative enzymes such as cellulases and lignin peroxidases, thereby lowering the rate of SOC mineralization. Simultaneously, they enhance the activity of synthetic enzymes (such as transpeptidase), promoting biomass synthesis [10,11]. After the death of the microorganisms, their residues (e.g., amino sugars and peptidoglycans) become the main source of stable SOC [3,12], contributing to SOC formation through mechanisms like the entombing effect. The high CUE of actinomycetes results in their residues contributing more than 50% of the recalcitrant SOC in forest soils, such as chitin [13]. When CUE is low, microorganisms tend to secrete large amounts of hydrolytic and oxidative enzymes to meet energy demands, thereby accelerating the decomposition of SOC. For instance, the activity of β-glucosidase is negatively correlated with CUE [14], leading to a net loss of SOC [15]. Conversion of tropical rainforest to farmland has been shown to increase hydrolytic enzyme activity by 30%, decrease microbial CUE by 20%, and result in a 40% reduction in SOC stocks [16]. Low CUE of nutrient-rich bacteria in agricultural soils is closely related to the rapid decline of SOC after tillage [10]. In contrast, high CUE may promote microbial biomass formation and subsequently enhance extracellular enzyme production, potentially leading to SOC loss over time through mechanisms such as the priming effect. In addition, it is worth noting that CUE is more sensitive to environmental changes than SOC and can quickly reach a new equilibrium, while SOC requires a slow process [17,18]. This asynchrony not only significantly affects the carbon cycle processes and sustainability of ecosystems, but also greatly increases the complexity of studying the interactions between the CUE and SOC.

3. Measurement Methods of CUE

Currently, research on microbial CUE predominantly relies on single-method datasets, often neglecting the fact that different measurement techniques emphasize distinct ecological processes. The selection of CUE measurement methods should carefully balance accuracy, ecological relevance, and operational feasibility, while ensuring that the chosen approach can effectively capture the key variables of the targeted ecological processes. The methods for measuring CUE mainly include isotope tracing, stoichiometric modeling, metagenomic data estimation, and other methods. However, each method has its own advantages and limitations (Table 1). At present, there is an urgent need to improve these measurement techniques to enhance the accuracy and comparability of CUE across different habitats.
(1) The most commonly used method for measuring CUE is isotope tracing, which typically employs substrates labeled with 14C or 13C or 18O-labeled water. Typically, oxygen isotope labeling is utilized to measure the CUE of the entire microbial communities, while carbon isotope labeling is utilized to measure the CUE of specific substrates [24]. The results of carbon isotope labeling may be affected by the substrate specificity, meaning that the measured CUE reflects only the efficiency of microorganisms utilizing that substrate, rather than the overall efficiency of the microbial communities. Furthermore, variations in incubation time and temperature between different studies hinder the measurement of standardized CUE [5]. In contrast, the 18O-labeled water method is more accurate, as it does not require the consideration of substrate specificity or interference from exogenous substrate additions affecting microbial metabolism, and it exhibits minimal temporal variability [25]. However, this method faces the limitation of being both costly and technically demanding. Concerns also arise from the underlying assumptions of the method, such as the assumption that water is the sole source of oxygen for microbial DNA synthesis and that all microbial cells maintain a consistent DNA-to-biomass C ratio [26]. Furthermore, the method is not applicable to dry soils [27].
(2) The stoichiometric model method is a method commonly used for indirectly estimating CUE. Its core principle is that microorganisms adjust their carbon allocation strategies (such as enzyme production) when decomposing plant residues and other organic matter in order to obtain the optimal ratio of carbon, nitrogen, and phosphorus elements required for growth. The advantage of this approach is that it requires relatively few parameters, including the C:N:P ratio of enzymes, substrates, and microbial biomass. However, its limitation lies in the highly simplified assumptions regarding microbial elemental requirements and carbon allocation behavior [28]. Specifically, in environments with high SOC, nutrients such as nitrogen and phosphorus are relatively scarce, forcing microorganisms to invest more carbon to acquire these nutrients, which leads to a reduction in CUE. This assumption stands in stark contrast to the positive correlation between SOC and CUE often observed in isotope tracing studies [5].
(3) Metagenomic data approaches for estimating CUE have emerged with the advancement of high-throughput sequencing technologies, offering novel tools to uncover the functional potential and carbon metabolic pathways of microbial communities. By conducting metagenomic sequencing of soil microbial communities, researchers can identify the functional genes associated with carbon assimilation (anabolic metabolism) and carbon loss (respiratory metabolism), thereby inferring the carbon allocation tendencies of microbial communities. Research has found that, based on metagenomic data, the relative abundance of biosynthetic genes is positively correlated with higher CUE [13]. Although this method is still in its early stages of development and faces challenges such as high technical barriers and unproven ecological adaptability, it provides a new solution to overcome the spatial limitations and process ambiguities of traditional CUE measurements in complex natural systems.
(4) In addition to the methods mentioned above, several less commonly used approaches have also been developed. For example, the metabolic respiration method determines CUE by tracking the production of 13CO2 at specific locations and analyzing the balance between biosynthesis and respiration. This method is suitable for studying dynamic changes in substrate utilization [25]. The microbial biomass method calculates CUE by measuring the ratio of microbial biomass to total respiration, and it is suitable for simplified analyses of soil microbial communities, especially for rapid assessment of total microbial biomass [22]. Therefore, there is still an urgent need to improve the methodology to increase the accuracy and comparability of CUE.

4. Variability of CUE Under Land-Use Change

Land-use change is the most critical factor affecting microbial CUE [29]. Globally, the impact of land-use change on CUE varies significantly depending on the ecosystem type and land management practices. Studies have shown that the general pattern of CUE in terrestrial ecosystems is forest ecosystems < farmland ecosystems < grassland ecosystems [30]. This variation is driven by complex ecological mechanisms.
In forest ecosystems, trees have well-developed root systems and high biomass, and their litter is mainly composed of difficult-to-degrade components such as lignin and cellulose. These organic compounds have complex structures, and the extracellular enzymes required for microbial decomposition are costly and have long decomposition cycles [30,31]. These factors limit the rapid conversion of carbon and biomass synthesis, thereby resulting in relatively low CUE.
In contrast, the root systems of plants in grassland ecosystems are relatively shallow, and they produce abundant rhizosphere exudates. These exudates primarily consist of simple carbohydrates that are easily utilized by microorganisms, such as soluble sugars and organic acids [32]. These carbon sources can be rapidly absorbed and assimilated by microorganisms into biomass, thereby improving CUE. Additionally, grassland soils typically exhibit better aeration and moisture conditions [33], providing favorable environmental conditions for microbial growth and metabolism, further promoting efficient microbial carbon utilization.
Land-use change affects the ecosystem carbon cycle [34] and regulates CUE by altering factors such as biomass and community compositions of aboveground vegetation [35], root exudates, litter quality [36], soil resource availability and other physicochemical properties [37], and soil microbial communities [38]. The conversion of grassland to cropland alters plant functional traits, leading to increased respiratory activity and, consequently, an 18% decline in CUE [39]. This shift replaces root exudates with crop residues and introduces disturbances like tillage, while fertilization causes nutrient imbalances [20]. The reduction in available carbon sources and increased disturbance typically lead to a significant decrease in CUE. After farmland was converted to shrubland and forest, CUE decreased by 13% and 11%, respectively [29]. This is because the litter input from shrubs or trees contains components that are more difficult to degrade, which impose high metabolic costs on the decomposer community. This shift toward complex substrates is the main driver of the decline in CUE. The transition from grassland to shrubland reduces CUE by 34% [29], which is caused by the shift from the easily decomposable carbon sources in grassland root exudates to difficult-to-decompose carbon sources in shrub litter. CUE decreases significantly, likely due to the sudden reduction in carbon source availability and the high cost of decomposing complex litter, while the microbial communities have not yet fully adapted. Natural grassland restoration significantly increased CUE by 41%, which is related to the ease with which grassland rhizosphere exudates are absorbed and utilized by soil microorganisms (Figure 2) [20]. Reestablishing grassland vegetation can restore the input of available carbon sources, promoting the efficient assimilation and growth of microorganisms, thereby significantly increasing CUE. It is evident that CUE varies among different land-use types and is influenced by a complex array of factors.

5. The Impact of Microbial Communities and Interactions on CUE

5.1. Microbial Community Diversity

Microbial community diversity is an important factor affecting CUE. The higher the community diversity, the greater the functional complementarity between microbial taxa (i.e., complementarity effects), and the greater the adaptive capacity in complex environments. Microorganisms contribute to CUE by making full use of multiple carbon sources. However, under drought conditions, an increase in microbial diversity does not increase CUE [38]. Therefore, when exploring the relationship between microbial community diversity and CUE based on complementarity effects, the regulatory role of abiotic factors must be taken into account [40]. Different land-use types exert different selective pressures on microorganisms, which directly affects microbial community diversity and compositions, and then, affects CUE. Generally, agricultural land is prone to a decrease in microbial diversity and CUE due to the long-term application of chemical fertilizers and pesticides [41,42]. In contrast, natural grasslands and forests, which possess higher microbial diversity, enrich the metabolic functional spectrum of microorganisms, facilitating efficient carbon source utilization and exhibiting higher CUE [30]. However, the relative contribution of soil bacterial and fungal community diversity to CUE remains poorly understood, although some studies have suggested that bacterial α-diversity has a positive effect on CUE [38,43].

5.2. Key Microbial Groups

Bacteria are the most common and diverse microbial taxa in soils and play a central role in carbon transformation [44,45]. Different bacterial groups influence CUE through different metabolic pathways. For example, Gram-positive and Gram-negative bacteria have different carbon metabolic pathways, resulting in differences in their CUE [46]. Additionally, in resource-rich environments, eutrophic bacteria (r-strategists) typically exhibit rapid growth rates but lower CUE, as they expend considerable energy on enzyme production to accelerate organic matter decomposition in order to satisfy their high resource demands, thereby reducing CUE. In contrast, oligotrophic bacteria (K-strategists) are capable of maintaining relatively high CUE even under carbon-limited conditions [47]. The transition from r-strategists to K-strategists has been proposed as a key mechanism underlying the observed increase in CUE along the successional gradient in the southeastern Tibetan Plateau [48]. Rhizobium can form symbiotic nitrogen-fixing structures with leguminous plants, significantly increasing the supply of soil nitrogen [49]. Research shows that this biological nitrogen fixation system not only promotes plant growth, but also improves the nitrogen limitation status of the microbial communities, thereby indirectly increasing CUE [50]. However, such interactions are highly dependent on signal molecule recognition and symbiotic regulatory mechanisms, exhibiting a high degree of host specificity. For example, some C4 plants tend to enrich microbial communities with high metabolic flexibility and higher CUE [51].
Saprotrophic fungi can decompose complex organic matter by secreting extracellular enzymes, thereby releasing available carbon sources, promoting the growth of microbial communities, and enhancing overall CUE. At the same time, CUE may decrease due to the high cost of resource acquisition [52,53]. Arbuscular mycorrhizal fungi (AMF), a type of mycorrhizal fungi, form mutually beneficial symbiotic relationships with plants and can enhance CUE by improving soil nutrient availability, particularly of phosphorus [54,55]. Under the crust of moss inoculated with AMF, these fungi may facilitate the mineralization of organic phosphorus by transporting phosphate-solubilizing bacteria through their external hyphae to areas of organic phosphorus enrichment in the soil, thereby enhancing soil phosphorus availability [56]. This process effectively alleviates the microbial phosphorus limitation, reducing the carbon investment required for phosphorus acquisition and allowing a greater proportion of carbon to be allocated to microbial growth [57]. Previous studies have reported a significant negative correlation between microbial phosphorus limitation and CUE [43,58].
In addition, an increasing body of research underscores the importance of trait- and phylogeny-based approaches to microbial functional classification for understanding differences in CUE. This method views microorganisms as ecological units with different life history traits (e.g., growth rate, carbon source preference, and resource investment strategy) and reveals the mechanisms of their CUE through metabolic genomics, enzyme profiles, and transcriptomic data. For example, some bacteria exhibit high enzyme synthesis capacity and metabolic flexibility, enabling them to more effectively obtain complex carbon sources in heterogeneous environments and achieve high potential CUE [59,60]. Phylogenetic conservation has also been shown to be significantly correlated with microbial CUE. Certain phyla, such as Actinobacteria, exhibit higher CUE due to their strong tolerance and resource integration capabilities [61].
In recent years, molecular biology techniques have provided molecular-level evidence for the regulatory mechanisms of microbial CUE. Based on isotope probing and metagenomic sequencing studies, microorganisms in high-CUE soils exhibit stronger synthetic metabolic activity for biomass accumulation. Genes related to glucose metabolism and glycogen synthesis are upregulated, contributing to anabolic processes and microbial biomass production [41]. Meanwhile, microorganisms with low CUE are more active in expressing respiratory-related genes [62]. The expression levels of these genes can serve as molecular biomarkers of respiratory metabolic activity, indirectly reflecting the CUE status of microbial communities. Based on this molecular-level evidence, microbial CUE is not only regulated by community-level factors but is also closely related to specific gene expressions and metabolic pathways.

5.3. Microbial Community Interactions

Interactions among microorganisms, such as competition, cooperation, symbiosis, parasitism, and predation, play a crucial role in regulating microbial CUE. Long-term competition for resources may result in some species being unable to access sufficient resources, limiting their growth and thereby reducing the community CUE [19]. Research has found that interspecific competition among fungi significantly increases respiratory metabolic costs, with the resulting energy expenditure exceeding even the effects of temperature or nitrogen input, leading to a decrease in CUE [63]. Bacteria tend to rapidly uptake low-molecular-weight carbon sources secreted by fungi, such as organic acids. This process is thought to cause nutritional competition pressure on fungi, thereby inhibiting their growth and indirectly reducing the CUE of the microbial communities [64]. However, microbial communities can improve CUE by cooperating to optimize resource utilization, broaden the actual ecological niche of species, alleviate environmental stress, and reduce the cost of extracellular enzyme production [65]. Research shows that microorganisms with high CUEs tend to rely on extracellular enzymes secreted by groups with low CUEs for resource utilization. The complementarity between microbial groups enables various microorganisms to reduce metabolic input and improve resource conversion efficiency, thereby increasing overall CUE [66]. Therefore, the balance between cooperation and competition is crucial to the CUE of microbial communities [30]. In addition, symbiotic interactions facilitate more efficient carbon source utilization through resource sharing and metabolic cooperation [67]. Interactions at higher trophic levels, such as predation, can influence CUE to varying degrees by altering microbial density and affecting the outcomes of interspecific competition [68,69].
Recent studies have found that the regulation of CUE is highly dependent on the complexity of microbial networks [70]. In soils with high CUE, microbial co-occurrence networks typically exhibit higher connectivity, stronger modularity, and a greater proportion of positive correlations. This collaborative network structure helps reduce individual energy input, enables resource sharing, and thereby improves overall CUE [65,71]. Furthermore, functional redundancy and complementarity also enable microbial communities to exhibit greater stability and carbon metabolism sustainability in the face of environmental fluctuations [72]. The effects of microbial interactions on CUE arise from a range of mechanisms [38,71]. Therefore, when assessing the impact of land-use change on CUE, it is necessary to explore the complex influence of microbial interactions on CUE in greater depth.

6. Microorganisms Mediate the Effects of Abiotic Factors on CUE

Beyond microbial influence, abiotic factors have also received increasing attention for their impact on CUE [65]. A global analysis of the impact of land-use change on microbial CUE reveals significant variations across different climate regions. Typically, land-use changes in tropical regions have a significant impact on microbial CUE, particularly in areas of large-scale deforestation and agricultural expansion. Although tropical soils store large amounts of carbon, land-use change causes SOC loss, limits microbial carbon use, and reduces diversity, collectively lowering CUE [73,74]. In colder regions, land-use change has less of an effect on CUE, though prolonged disturbances like overgrazing or tillage still reduce it [75,76]. In an assessment of the impact of land-use change on CUE in the subarctic region of Canada, it was found that CUE significantly increased after the conversion of forests to grasslands and farmlands, and was strongly influenced by soil pH and the C:N ratio [75]. In summary, the effects of land-use change on CUE are regionally specific and may be influenced by local climate and the complex interactions of soil properties with microbial communities [77].
Land-use change alters microbial communities by directly affecting soil properties (e.g., pH, C:N ratio, moisture) and indirectly through shifts in plant inputs like root exudates and litter quality [21]. Through their metabolic activities, microorganisms further regulate the efficiency of soil resource transformation, thereby shaping the response patterns of CUE. This bidirectional regulation underscores the intricate and dynamic nature of the processes controlling CUE. In fact, microbial communities regulate and buffer the effects of abiotic factors through adaptive strategies. These strategies include changes in community compositions (e.g., conversion between r- and K-strategists), physiological adaptation, and functional redundancy [48]. Microbial functional traits, such as stoichiometric balance and metabolic plasticity, contribute to the ability of microbial communities to resist or adapt to environmental fluctuations [78]. Functional redundancy maintains processes like decomposition despite species turnover or environmental filtering [79]. In ecosystems with high microbial richness, such as restored grasslands or mature forests, these mechanisms collectively contribute to more stable microbial CUE across time and space.

6.1. Temperature and Moisture Sensitivity of CUE

According to the thermal adaptation theory, soil microbial respiration is generally lower at higher temperatures. Based on this, it can be inferred that CUE may increase with rising environmental temperatures or long-term warming. Research indicates that under long-term warming conditions, microbial communities may shift toward heat-tolerant groups, optimizing the growth–respiration ratio [66]. In addition, some bacteria reduced respiratory losses while maintaining biomass, thereby maintaining high CUE even at higher temperatures [80]. However, in temperate or tropical soils, CUE may increase with rising temperatures, while in boreal soils with an annual average temperature of less than 10 °C, CUE decreases with rising temperatures. Microorganisms are capable of adjusting their optimal growth temperature, enabling them to adapt to varying environmental conditions [81]. Evidence suggests that CUE exhibits a threshold response to temperature. A recent study suggests that when the mean annual temperature exceeds approximately 15 °C, temperature increases can significantly increase CUE. This likely results from the decoupling of respiration and growth, with warming enhancing growth and lowering respiration [82,83]. Excessive heat can damage proteins and membranes, impairing microbial function and reducing CUE [19]. Overall, the effect of temperature on CUE is highly complex. Temperature increases may reduce CUE through pathways such as water stress and depletion of organic substrates, but in some cases, temperature increases may also alleviate nutrient limitations and improve CUE [84].
Soil moisture is an important environmental factor that affects microbial growth and respiration. Similar to the effect of temperature, the effectiveness of soil moisture on CUE is very complex. Under excessively dry or wet environmental conditions, microbial metabolic activities may be affected. Waterlogging generally inhibits CUE by increasing the energetic cost associated with stress-tolerance mechanisms, thereby elevating the microbial metabolic quotient (qCO2) [85]. A field survey along a 6000 km arid gradient in northern China, along with a moisture control experiment, found that the higher the degree of drought, the lower the CUE. This was closely related to a decrease in microbial diversity and reduced substrate availability (due to decreased plant carbon input) [86]. In addition, drought conditions typically select for low-nutrient microorganisms that can maintain growth under resource-limited conditions, thereby mitigating the decline in CUE associated with water scarcity to some extent [87]. In sandy loam soils in the western United States, CUE increases exponentially with higher moisture content. The underlying reason is that low moisture content restricts substrate diffusion, which in turn inhibits carbon assimilation efficiency. This indicates that moisture primarily regulates CUE by affecting the diffusion of substrates rather than through physiological stress [88]. And as soil pores are filled with water, oxygen diffusion rates decrease. Under oxygen-limited conditions, soil microorganisms shift from aerobic respiration to anaerobic respiration or fermentation, resulting in reduced productivity and subsequent declines in microbial growth and CUE. In vegetation restoration trials in semi-arid regions, as soil moisture increases during succession, microbial carbon metabolism becomes more active. However, CUE first increases and then declines, likely due to heightened phosphorus limitation and the increased costs of enzyme synthesis [89]. Additionally, after rewatering of drought-affected soils, microbial respiration rapidly increases, but growth exhibits a lag (especially after prolonged drought), resulting in initially low CUE values. Over the following days, as microbial growth recovers, CUE gradually increases and then decreases again once the available substrates are depleted [90].
Overall, under conditions of constantly changing external temperature and humidity, soil microorganisms maintain their overall metabolic balance by altering community composition, thereby stabilizing CUE and reducing its sensitivity to temperature and humidity [24,91]. This reflects microbial diversity, redundancy, and physiological adaptability [38]. Therefore, the comprehensive effects of temperature and humidity on CUE remain insufficiently studied.

6.2. Threshold Effect of Soil pH on CUE

Soil pH is a potential stressor that affects microbial community structure and metabolic activity. Extremes of pH inhibit microbial growth, with taxa differing in pH tolerance. Generally, most bacteria thrive in neutral to slightly alkaline soil environments, while some fungi exhibit stronger competitiveness under acidic soil conditions [92,93]. CUE in agricultural soils exhibits a threshold response, peaking at pH 5.5. Below this value, CUE gradually decreases, as lower pH is associated with higher Al3+ toxicity, causing microorganisms to allocate more carbon to energy-intensive metabolic pathways to cope with H+/Al3+ stress (e.g., cell repair and detoxification processes) [94]. Research has found that there is a U-shaped relationship between lime-induced soil pH and overall CUE, and that CUE may be lowest when the pH of agricultural soil is 6.4 [95]. Other studies identify pH 6.2 as a microbial threshold in response to land-use change. In acidic soils, intensive land use often increases pH, alleviating the inhibitory effect of acidity on microbial growth; however, under near-neutral conditions, increased land-use intensity actually reduces CUE, as it requires higher inputs to cope with stress or acquire resources [37]. Therefore, the dynamic relationships among soil pH, microbial communities, and CUE in the context of land-use change is more complex.

6.3. Species-Specific Effects of Resources and Their Stoichiometry on CUE

In the process of agricultural intensification, agricultural management practices such as fertilization and irrigation alter the soil nutrient supply status [96]. For example, appropriate fertilization can increase the content of soil nutrients such as nitrogen and phosphorus, which facilitates the increase in microbial activity and biomass, thus enhancing CUE. Excessive fertilization causes nutrient imbalances, suppressing certain microbial groups or promoting those that increase carbon turnover and respiratory losses, thereby reducing CUE [97]. Based on the consumer-driven nutrient cycle theory, resource requirements related to stoichiometry of microbial biomass may be important limiting factors for CUE, and this is also an important physiological mechanism underlying microbial community dynamics in natural environments. At the microbial domain level (e.g., bacteria and fungi), there are significant differences in the patterns of resource quality and quantity affecting CUE. Fungal CUE is more influenced by carbon, while bacteria are more limited by nitrogen and phosphorus. Therefore, soil resource quality and quantity have species-specific effects on CUE. Based on the stoichiometric homeostasis theory, differences in stoichiometric ratios of microbial biomass may be an important driver of CUE and are related to microbial community structure in heterogeneous resource environments [98].
The promoting effect of nitrogen on CUE is universal. Nitrogen addition enhances CUE in subalpine forests, with C:P and N:P ratios negatively correlating with CUE [99]. Continuous nitrogen addition for six years also increased CUE, not due to changes in elemental stoichiometries, but because of a weakening of the mineral protection of organic matter, which made microbial access to available carbon sources easier [100]. In subtropical forests, nitrogen addition increased CUE in both valley and slope areas, but the mechanisms of influence were different. In the valley, the increase in CUE was primarily driven by enhanced fungal abundance, while in the slope area, it was attributed to a decrease in the C:P ratio and reduced respiration [101]. A 66-year nutrient addition experiment found that nitrogen addition inhibited the activity of nitrogen acquisition-related enzymes while enhancing the expression of carbon acquisition enzymes and degradation genes, indicating that microorganisms shifted to a strategy of prioritizing carbon acquisition [102]. This adjustment in enzyme expression altered carbon allocation and affected CUE. Additionally, different types of nitrogen fertilizers have varying effects on CUE. Research has shown that applying urea significantly increases CUE, while ammonium nitrate causes a decrease in CUE at high application rates. This may be due to the slower release rate of urea, which provides a more stable nitrogen source and promotes microbial anabolic metabolism. In contrast, ammonium nitrate has a faster release rate, causing microorganisms to prefer energy metabolism, resulting in increased carbon loss through respiration [103].
Phosphorus is a key element affecting microbial energy metabolism and enzyme activities. A meta-analysis combining 389 pairs of observational data found that the effect of phosphorus addition on CUE is inconsistent. This variability depends on factors such as fertilization intensity, substrate type, and water-temperature conditions [104]. Typically, adequate phosphorus supply helps improve microbial metabolic efficiency and biomass, thereby increasing CUE, but the effect of phosphorus is often closely related to nitrogen supply [105]. Under nitrogen-rich conditions, increasing phosphorus significantly increases CUE, possibly because phosphorus promotes ATP production within cells, thereby improving the metabolic efficiency of microorganisms and reducing carbon loss during respiration [41]. However, under nitrogen-limited conditions, the effect of phosphorus may be more limited. Furthermore, excessive phosphorus input may lead to nutrient imbalances, which can subsequently affect the overall physiological state of microorganisms [106,107]. There have been reports that AMF also plays a crucial role in buffering nutrient-related stress constraints [108]. By promoting phosphorus uptake and improving nitrogen acquisition, AMF can reduce the energy costs associated with nutrient mining. This will improve microbial growth efficiency and stabilize CUE under nutrient-limited conditions [109].
Most existing studies have focused on the short-term effects of single nutrients, with limited in-depth exploration of the synergistic effects of multiple nutrients under complex environmental conditions. Future work should examine multi-nutrient effects on CUE, include long-term field trials, and optimize nutrient management under climate change scenarios.

7. Limitations and Future Directions

(1)
Lack of long-term monitoring data
Research on microbial CUE under land-use change has mostly focused on short-term experiments and lacks the support of long-term monitoring data [23,110]. It is important to establish a long-term positioning test site, collect soil samples regularly, measure the changes in microbial CUE and related environmental factors, and analyze the long-term monitoring data to reveal the evolution pattern of microbial CUE over time as well as its intrinsic connection with land-use change.
(2)
Lack of changes in deep soil CUE characteristics
Most studies have focused on surface soil (0–20 cm) [111,112], while understanding of the dynamic changes in CUE in deep soil (>30 cm) and their regulatory mechanisms remains limited. Deep soil stores approximately 50% of global SOC, and its carbon turnover processes may respond differently to land-use change compared with those of surface soil [113,114]. Therefore, systematically revealing the dynamic changes in CUE across different soil layers can enhance our ability to predict the stability of soil carbon pools under global change conditions.
(3)
Lack of multidimensional integrated research
Most existing studies have focused on a single land-use type or on local ecosystems [115,116], with few considering multiple factors such as different land-use changes, climatic conditions, and soil types, making it difficult to fully assess the sustainability of ecosystem carbon cycle functions. Microbial CUE exhibits significant variability. Future CUE research should place greater emphasis on integrating microbial community dynamics with abiotic environmental variables into a unified model framework, identifying key regulatory factors and nonlinear interactive effects, constructing a CUE regulatory network that better reflects actual conditions, and elucidating the dynamic characteristics and multidimensional influence mechanisms of CUE under land-use change. Additionally, attention should be given to quantifying the relative strength of microbial community buffering under different land-use practices, while considering the significant roles of soil animals, protozoa, and viruses in mediating microbial turnover and respiration. This is crucial for maintaining the long-term sustainability of soil ecosystems.

Author Contributions

Conceptualization, Z.L.; writing—original draft preparation, Z.L.; writing—review and editing, D.Q.; project administration, D.Q.; funding acquisition, D.Q. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Heilongjiang Provincial Natural Science Foundation of China [grant number LH2024C090], Heilongjiang Provincial Postdoctoral Science Foundation [LBH-Z24261], Heilongjiang Province provincial colleges and universities basic scientific research business expenses scientific research projects [grant number 2023-KYYWF-1447].

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
CUECarbon use efficiency
SOCSoil organic carbon
AMFArbuscular mycorrhizal fungi

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Figure 1. Mechanisms of change in CUE.
Figure 1. Mechanisms of change in CUE.
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Figure 2. CUE response to land-use change.
Figure 2. CUE response to land-use change.
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Table 1. Recommended microbial CUE measurement methods.
Table 1. Recommended microbial CUE measurement methods.
Research
Objective
Preferred
Method
Suitable
Soil Type
Notes
Substrate-
specific CUE
13C-labeled compoundsAgricultural or
lab-controlled
Sensitive to substrate selection
Whole-community CUE18O-labeled water methodMoist, temperate soils [19,20]High accuracy, costly, not for dry soils
Long-term field monitoringStoichiometric modelingGrassland or cropland [21]Simplified, less precise, for trends
Functional gene-based CUEMetagenomic data approachesAny, especially natural soils [13]Novel, promising, technical, early stage
Microbial response dynamicsMicrobial biomassAny with time series [22,23]Rapid, integrative
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Li, Z.; Qi, D. The Response Mechanism of Soil Microbial Carbon Use Efficiency to Land-Use Change: A Review. Sustainability 2025, 17, 7023. https://doi.org/10.3390/su17157023

AMA Style

Li Z, Qi D. The Response Mechanism of Soil Microbial Carbon Use Efficiency to Land-Use Change: A Review. Sustainability. 2025; 17(15):7023. https://doi.org/10.3390/su17157023

Chicago/Turabian Style

Li, Zongkun, and Dandan Qi. 2025. "The Response Mechanism of Soil Microbial Carbon Use Efficiency to Land-Use Change: A Review" Sustainability 17, no. 15: 7023. https://doi.org/10.3390/su17157023

APA Style

Li, Z., & Qi, D. (2025). The Response Mechanism of Soil Microbial Carbon Use Efficiency to Land-Use Change: A Review. Sustainability, 17(15), 7023. https://doi.org/10.3390/su17157023

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