Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling

Abstract

Microbial nitrogen use efficiency (NUE) describes the partitioning of organic N taken up between growth and the release of inorganic N to the environment (that is, N mineralization), and is thus central to our understanding of N cycling. Here we report empirical evidence that microbial decomposer communities in soil and plant litter regulate their NUE. We find that microbes retain most immobilized organic N (high NUE), when they are N limited, resulting in low N mineralization. However, when the metabolic control of microbial decomposers switches from N to C limitation, they release an increasing fraction of organic N as ammonium (low NUE). We conclude that the regulation of NUE is an essential strategy of microbial communities to cope with resource imbalances, independent of the regulation of microbial carbon use efficiency, with significant effects on terrestrial N cycling.

Figure 1. Conceptual diagram illustrating the regulation of NUE in a homeostatic heterotrophic microbial community.

The threshold elemental ratio denotes the threshold of the resource C:N below which N will be in excess in relation to the demand of the microbial community (C limitation). Excess N is expected to be released causing a reduction in microbial NUE. In contrast, above this threshold the microbial community is expected to be limited by N. Consequently, microbial NUE reaches a maximum value.

Figure 2. Microbial NUE.

(a) Box plots showing microbial NUE in mineral (n=36), organic soil horizons (n=19) and in decomposing plant litter (n=38). Different letters indicate significant differences in NUE between substrate types (Kruskal–Wallis test followed by Dunn’s test). The box plots show the medians (solid line within boxes), 25th and 75th percentiles as vertical bars, 10th and 90th percentiles as error bars and 5th and 95th percentiles as circles. (b) Relationship between resource C:N (R_C:N; mass basis) and microbial NUE for litter, organic and mineral soil horizons. Solid lines are linear regression lines of the piece-wise regression model (R²=0.301; F_3,89=12.74; P<0.001; n=93). A significant break point was found at a resource C:N of 20 with a corresponding value of 0.83 for microbial NUE. (c) Relationship between C:N imbalance and microbial NUE for litter, organic and mineral soil horizons. The stoichiometric imbalance between microbial decomposers and their resource can be represented by resource C:N (R_C:N) normalized to microbial biomass C:N (B_C:N). The relationship was best described by a saturating nonlinear regression model as follows: NUE=1.03 × (R_C:N/B_C:N)/[0.92+(R_C:N/B_C:N)] (R²=0.431; F_1,69=52.27; P<0.001; n=71).

Figure 3. Homeostasis in microbial decomposer communities.

Stoichiometric homeostasis can be described by a linear relationship between the logarithm of resource C:N (R_C:N) and microbial biomass C:N (B_C:N) (slope=0.14; P<0.05; n=71). Non-log-transformed values for R_C:N and B_C:N are given in parentheses.