Digging deeper into microbial carbon use efficiency in soil: Perspectives from microbial growth and respiration

Digging deeper into microbial carbon use efficiency in soil: Perspectives from microbial growth and respiration

Microbial carbon use efficiency, a key regulator of soil organic carbon dynamics, reflects carbon allocation between microbial growth and respiration. Separate investigation of microbial growth and respiration helps to clarify the role of carbon use efficiency in the carbon balance and consequently, in the carbon cycle in soil. First, in terms of microbial resource acquisition, the drivers of microbial growth and respiration differ: microbial growth is primarily regulated by synergistic availability of carbon, nitrogen, and phosphorus, whereas respiration is more strongly influenced by substrate quality, such as the carbon-to-nitrogen ratio. Second, synchronized responses of microbial growth and respiration rates under climate change, for example, warming, drought, elevated carbon dioxide often mask underlying carbon use efficiency regulatory mechanisms. Thus, we propose: one explicitly representing microbial growth and respiration in models to raise the precision of soil organic carbon dynamics predictions; and two applying approaches such as isotope probing and metagenomic functional annotation to resolve carbon use efficiency mechanisms from the community to the single-species level. Overall, decoupling carbon use efficiency into its growth and respiration components establishes a mechanistic framework that explicitly links carbon use efficiency to microbially mediated soil organic carbon dynamics.

Microbial carbon use efficiency is the ratio of carbon channeled into microbial growth to the carbon that is taken up, serving as a pivotal indicator governing the initial step of organic matter utilization by microorganisms that can have some relevance for soil organic carbon accrual. Carbon use efficiency increases as more carbon is allocated to microbial growth than to respiration, and carbon use efficiency declines when respiratory costs rise. Because carbon use efficiency combines two processes, growth and respiration, we suggest that understanding these two components independently will improve our representation of the role of carbon use efficiency in the soil carbon cycle. For example, growth and respiration rates may vary in concert, as when both processes increased in response to climate change factors, causing no change in carbon use efficiency.

Indeed, an improved understanding of microbial growth and respiration is crucial to raise our comprehension of carbon use efficiency and its driving factors. For example, a meta-analysis reported that microbial growth rate increased with contents of soil organic carbon, total nitrogen, and total phosphorus, while these factors showed no direct relationship with carbon use efficiency. Regarding microbial resource acquisition, microbial growth is generally driven by the availability and accessibility of carbon and nutrient resources in soil. Carbon serves as both the energy source and the structural substrate of microbial biomass. Nitrogen is critical for structural protein and nucleic acid synthesis, and phosphorus supports nucleic acid production and energy metabolism. Together, these elements establish a three-dimensional resource limitations framework that governs microbial growth. In contrast, respiration is more directly regulated by soil organic carbon quality, for example, substrate carbon-to-nitrogen ratio, labile and stable soil organic carbon pools, than by the availability of carbon or nitrogen, because the stoichiometric balance of soil organic carbon determines the enzymatic activity and energy investment required for organic matter decomposition, which in turn directly affects the rate of microbial respiration. This distinction is supported by a meta-analysis showing that nitrogen or combined nitrogen-phosphorus additions altered carbon use efficiency primarily by affecting microbial growth rather than respiration. Soil microorganisms may adjust their physiological processes and metabolic pathways to alter their growth and respiration under resource limitations, further complicating the factors affecting carbon use efficiency. For example, in soils with a high carbon availability but low phosphorus levels, microorganisms accelerate phosphorus recycling within biomass to sustain growth or trigger overflow respiration. Thus, the differential driving mechanisms of microbial growth and respiration may explain the lack of consistent relationships between carbon use efficiency and other factors.

Gaining more knowledge on the components of carbon use efficiency can deepen our understanding of carbon use efficiency in response to climate change. A meta-analysis revealed that warming did not affect carbon use efficiency, but strongly decreased microbial growth rate due to substrate limitation, declined soil moisture and higher maintenance metabolism investments. Microorganisms can invest resources for growth only after the costs for maintenance, for example, respiration, are covered. Additionally, carbon use efficiency was not sensitive to the interactive effects of drought, elevated carbon dioxide concentration, and warming, while both microbial growth and respiration rates were increased by their interactions. These synchronous changes in microbial growth and respiration rates reflect an intrinsic regulatory mechanism that underpins their adaptation strategies to long-term climate change. Therefore, focusing on microbial growth and respiration instead of carbon use efficiency helps to uncover the regulatory mechanisms of climate change on carbon use efficiency, as well as the driving factors.

Breaking down carbon use efficiency into two observable pathways, microbial growth and respiration, can improve the accuracy of soil carbon models. Current models simplify carbon use efficiency as a constant or a temperature-dependent parameter, which result in unrealistic predictions for soil organic carbon dynamics, as carbon use efficiency varies across ecosystems, temporal scales, and environmental factors. To better align with current understanding of microbial physiology, carbon use efficiency should be represented not as a fixed input parameter but as an emergent property arising from multiple interacting microbial processes. Explicitly modeling microbial growth and respiration as separate, dynamic modules allows simulations to capture their asynchronous responses and directly match empirical carbon use efficiency measurements from isotope-labeling studies, thereby substantially reducing model uncertainties. Furthermore, linking microbial growth to the associated necromass accumulation rather than associating carbon use efficiency with soil organic carbon accumulation, as in the Century model, provides a more mechanistic understanding of the varied relationships between carbon use efficiency and soil organic carbon.

Emerging advanced molecular biotechnologies will help understanding the carbon use efficiency components. Of these two carbon use efficiency components, microbial growth is the less studied than respiration, as respiration is well documented. DNA- and RNA-based stable isotope probing enables direct tracking of isotopically labelled substrates into specific microbial taxa, allowing quantification of growth rates and corresponding carbon use efficiency at both community and single-species scales. For example, stable isotope probing coupled with high-throughput sequencing has been used to identify growing bacterial and fungal taxa, revealing which microbial groups dominate carbon assimilation and how their growth dynamics contribute to overall microbial carbon use efficiency. Metagenomic functional annotation provides insights into the potential functions of microbial communities, linking gene abundance in growth-related pathways, for example, biofilm formation, fatty acid biosynthesis, and in respiration-associated pathways, such as carbohydrate metabolism, for example, lignin, chitin, cellulose. These technological innovations offer the possibility of exploring carbon use efficiency components from the community to the single-species level, thereby opening promising pathways for advancing understanding of carbon use efficiency and its ecological impacts.

However, the interpretations of microbial respiration and growth remain some limitations. First, current methods for estimating microbial growth rates rely primarily on isotope tracing techniques, which track the synthesis of key biomolecules such as DNA, lipids, or proteins. These approaches typically involve the incorporation of stable isotopes, for example, carbon thirteen, deuterium, oxygen eighteen, into microbial biomolecules over a defined period, from which gross microbial growth rates can be inferred. Accurate isotope recovery requires controlled incubation conditions to minimize interference from environmental variability. However, technical constraints currently prevent the direct application of these methods in field settings. As a result, the potential rates of microbial respiration and growth measured under optimized incubation conditions do not correspond to in-situ rates. Second, widely used proxies, such as biomass carbon accrual and DNA synthesis, may systematically underestimate carbon use efficiency by neglecting non-growth anabolic processes, for example, extracellular polymeric substances production and the repair of damaged cell structures. Third, carbon use efficiency estimation methods based on various microbial growth proxies may produce divergent or even contradictory results, especially under climate change. For example, the addition of carbon thirteen-labelled substrates alleviated substrate limitation caused by nitrogen deposition, activating dormant microorganisms and thereby reducing CUE estimates, which contradicts results obtained using the H two eighteen O labelling method. Therefore, selecting appropriate microbial CUE measurement methods under climate change is essential to minimize methodological artifacts. Fourth, interspecific interactions within microbial communities (e.g., predation, cross-feeding, endo- versus exoenzymes) can substantially modulate microbial respiration and growth dynamics, yet these processes remain underexplored. To address these uncertainties, developing direct and in-situ measurement techniques, combined with investigating microbial interactions within the soil food web, is essential.

Altogether, decoupling CUE into growth and respiration components establishes a mechanistic framework that explicitly links apparent CUE to microbially mediated SOC dynamics. However, current methodologies for measuring CUE components, particularly the quantification of microbial growth rate, remain technically constrained. Future research should integrate multi-omics approaches to microbial physiology, cross-scale spatiotemporal observations, and process-explicit models to test conceptual and quantitative frameworks of how CUE components will determine overall variations in CUE and the associated the soil carbon cycling.