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.

Photodegradation alleviates the lignin bottleneck for carbon turnover in terrestrial ecosystems

“…1 C and D and Tables S3 and S4). In general, these results are quantitatively consistent with other studies that explored photodegradation of plant litter under field conditions (12,16,17,20) although the breadth of species evaluated here, which ranged from annual herbaceous species to conifer and angiosperm tree species, establishes a general pattern for the spectral dependence of photodegradation of plant litter in terrestrial ecosystems.…”

“…First, whereas it has been demonstrated that litter mass loss is directly caused by exposure to solar radiation (12,17,20), we suggest that the principal and quantitatively most important effect of photodegradation on the global carbon cycle may be the facilitation of biotically mediated carbon turnover. We demonstrate here, with a direct comparison of direct photodegradation and biotic decomposition (Table S4), that biotic decomposition overall had a much larger effect on organic matter loss for the same species (range 4-65%) than the direct effect of photodegradation, which was generally small (range 1.5-4.5%) (Table S4).…”

“…In terrestrial ecosystems, accumulating evidence has demonstrated the importance of photochemical mineralization of organic carbon compounds (photodegradation) as a control on organic matter turnover in arid and semiarid ecosystems (12)(13)(14)(15). Losses of volatile carbon compounds, including CO 2 , CO, and methane (CH 4 ), from recently senesced plant material exposed to natural or artificial radiation have been documented (16)(17)(18) and have been linked to photochemical degradation of cellulose (16) and partial or complete degradation of lignin (19)(20)(21). Recent studies have demonstrated stimulation of litter decomposition and respiration with prior exposure to ultraviolet (UV) (22,23) or full solar radiation (24) in dry Mediterranean ecosystems.…”

“…In addition, for historical reasons related to studies of the effects of stratospheric ozone depletion (29,30), there has been a strong emphasis on evaluating the effects of UV (200-400 nm) radiation (particularly UV-B, 280-315 nm) on litter decomposition, and these studies have yielded equivocal results with respect to the importance of this spectral region as a driver of photodegradation (31,32). Recent evidence has demonstrated that the visible component of sunlight [blue and green wavelengths, 400-550 nm (BG)] can have a large impact on photodegradation (17,20), suggesting…”

Management practices amplify the effects of N deposition on leaf litter decomposition of the Moso bamboo forest

“…Nitrogen addition can enhance N availability and soil enzyme activity, thereby accelerating litter decomposition (Knorr et al 2005;Manning et al 2008). Lignin is a key factor in the regulation of litter decomposition, especially during the later decay stage (Austin and Ballaré 2010). Excessive N inputs have been demonstrated to suppress ligninolytic enzyme activity in the long term and correspondingly reduce litter decomposition (Fog 1988;Carreiro et al 2000;Thirukkumaran and Parkinson 2000;Hobbie et al 2012), although a few studies have found no evidence of negative effects (Hobbie et al 2006).…”