Dual role of lignin in plant litter decomposition in terrestrial ecosystems

Abstract

Plant litter decomposition is a critical step in the formation of soil organic matter, the mineralization of organic nutrients, and the carbon balance in terrestrial ecosystems. Biotic decomposition in mesic ecosystems is generally negatively correlated with the concentration of lignin, a group of complex aromatic polymers present in plant cell walls that is recalcitrant to enzymatic degradation and serves as a structural barrier impeding microbial access to labile carbon compounds. Although photochemical mineralization of carbon has recently been shown to be important in semiarid ecosystems, litter chemistry controls on photodegradative losses are not understood. We evaluated the importance of litter chemistry on photodegradation of grass litter and cellulose substrates with varying levels of lignin [cellulose-lignin (CL) substrates] under field conditions. Using wavelength-specific light attenuation filters, we found that light-driven mass loss was promoted by both UV and visible radiation. The spectral dependence of photodegradation correlated with the absorption spectrum of lignin but not of cellulose. Field incubations demonstrated that increasing lignin concentration reduced biotic decomposition, as expected, but linearly increased photodegradation. In addition, lignin content in CL substrates consistently decreased in photodegradative incubations. We conclude that lignin has a dual role affecting litter decomposition, depending on the dominant driver (biotic or abiotic) controlling carbon turnover. Under photodegradative conditions, lignin is preferentially degraded because it acts as an effective light-absorbing compound over a wide range of wavelengths. This mechanistic understanding of the role of lignin in plant litter decomposition will allow for more accurate predictions of carbon dynamics in terrestrial ecosystems.

Fig. 1.

Experimental attenuation of specific regions of the solar spectrum demonstrates that both UV and visible radiation can drive photodegradation in the field. (A) Mass loss of grass litter in a semiarid grassland. Initial lignin concentration of litter was 7.3%. (B) Mass loss of cellulose-lignin (CL) substrates with 10% lignin concentration. Bars denote treatment means (n = 5 + SEM). Different letters indicate significant differences for Tukey HSD posthoc comparisons.

Fig. 2.

Radiation absorbance spectra of CL substrates enriched with different quantities of lignin (0, 5, 10, and 15%). The cutoffs of the spectral filters used for the sunlight attenuation experiments (Fig. 1) are indicated for comparison.

Fig. 3.

Dual role of lignin in litter decomposition. Decomposition of CL substrates under abiotic conditions of full solar radiation (pink diamonds) and under biotic conditions (green circles), both under field conditions during summer and early fall. Symbols indicate mean values (n = 5 ± SEM). Solid lines are least-squares fits of the original data, which in both cases were simple linear regressions. Equations: Photodegradation = 0.0091 × (%lignin) + 0.0002. r² = 0.92; Biotic decomposition = −0.0105 × (%lignin) + 0.0024. r² = 0.45.

Fig. 4.

Lignin concentration decreases with photodegradation and increases during biotic decomposition. (A) Initial and final lignin concentrations for photodegradation and biotic incubation experiments. CL substrates exposed to solar radiation consistently demonstrated a reduction in lignin concentration, whereas biotically incubated CL substrates overall showed increased lignin concentrations. Each data point corresponds to an individual sample exposed to full solar radiation (pink diamonds) or biotic conditions (green circles). (B) Predicted and observed changes in lignin for photodegradation: predicted changes were calculated assuming that all mass loss was due to the photodegradation of lignin. Regression for data points shown: Observed % = 0.99 × (Predicted %), r² = 0.88, which does not deviate significantly from the 1:1 line. (C) Predicted and observed changes in lignin for biotic decomposition: predicted changes were calculated assuming that all mass loss was due to cellulose respiration. Regression for data points shown: Observed % = 1.06 × (Predicted %), r² = 0.77, which does not deviate significantly from the 1:1 line.