Microbial communities in terrestrial surface soils are not widely limited by carbon

Abstract

Microbial communities in soils are generally considered to be limited by carbon (C), which could be a crucial control for basic soil functions and responses of microbial heterotrophic metabolism to climate change. However, global soil microbial C limitation (MCL) has rarely been estimated and is poorly understood. Here, we predicted MCL, defined as limited availability of substrate C relative to nitrogen and/or phosphorus to meet microbial metabolic requirements, based on the thresholds of extracellular enzyme activity across 847 sites (2476 observations) representing global natural ecosystems. Results showed that only about 22% of global sites in terrestrial surface soils show relative C limitation in microbial community. This finding challenges the conventional hypothesis of ubiquitous C limitation for soil microbial metabolism. The limited geographic extent of C limitation in our study was mainly attributed to plant litter, rather than soil organic matter that has been processed by microbes, serving as the dominant C source for microbial acquisition. We also identified a significant latitudinal pattern of predicted MCL with larger C limitation at mid‐ to high latitudes, whereas this limitation was generally absent in the tropics. Moreover, MCL significantly constrained the rates of soil heterotrophic respiration, suggesting a potentially larger relative increase in respiration at mid‐ to high latitudes than low latitudes, if climate change increases primary productivity that alleviates MCL at higher latitudes. Our study provides the first global estimates of MCL, advancing our understanding of terrestrial C cycling and microbial metabolic feedback under global climate change.

Predicting microbial nutrient limitations from a stoichiometry-based threshold framework

“…Both metabolic and stoichiometric theories of ecology suggest that microorganisms could maximize growth efficiencies (i.e., maximum efficiencies of C, N and P use (CUE max , NUE max and PUE max , respectively)) when neither energy nor nutrients were limiting. 13,29,30 R d stoichiometry under unlimited conditions can thus be defined as and expressed as:…”

“…5,[7][8][9][10] The topic has thus gained increasing attention in the fields of global change ecology and soil ecology. [11][12][13][14][15] Identifying microbial nutrient limitations, however, is intrinsically difficult due to microscopic scales, overwhelming species diversity, rapid reproduction and biomass turnover as well as elusive adaptive strategies in microbial communities.…”

“…Several approaches have been used to infer microbial nutrient limitations, including laboratory substrate-added incubations, field fertilization experiments, and stoichiometry-based models. 3,11,13,16 Laboratory incubations typically add soluble substrates (e.g., glucose) that can be acquired by microorganisms without ecoenzyme catalysis to highly disturbed soil samples. 17,18 It thus measures uptake potential favoring copiotrophs and circumventing catalytic relationships within the natural saprophytic community.…”

“…Alternatively, approaches based on ecological stoichiometry can identify microbial nutrient limitations indirectly without altering existing ecosystem status. 7,13,16 A clear advantage of the stoichiometry approach is estimating microbial nutrient limitations based on their ecoenzymatic characteristics in situ rather than their responses to pulse manipulations of anthropogenically disturbed systems. 3 Specifically, most of the energy and nutrients required by microorganisms in bulk soils of natural ecosystems are originally derived from organic polymers (i.e., plant litter) through ecoenzyme catalysis.…”

“…The ecoenzyme vector model is one of the most widely used approaches to interpret ecoenzymatic stoichiometry. 13,16,24 It includes vector length and angle for estimating microbial nutrient limitations, and defines a vector angle of 45° representing the threshold of ecoenzymatic activities distinguishing microbial phosphorus (P) limitation (> 45°) and nitrogen (N) limitation (< 45°). This definition is based on the observed pattern of ecoenzymatic stoichiometry for C:N:P-acquiring activities near 1:1:1 at a global scale, so the slopes of their regression relationships are close to 45°.…”