16_PNAS_Photodegradation alleviates the lignin bottleneck for carbon turnover in terrestrial ecosystems

DOI: https://doi.org/10.1073/pnas.1516157113

Intro

  • Plant litter decomposition is an important first step for carbon and nutrient turnover, and litter inputs and losses are essential in determining soil organic matter pools and the carbon balance in terrestrial ecosystems
  • In past studies of photodegradation of plant litter, there was an emphasis on UV radiation, but recent evidence suggested that visible component (BG: blue and green) can have a large impact.

Results

UV and BG radiation significantly promote organic mass loss from litter across a broad range of species

Fig. 1.

Exposure to solar radiation strongly enhances microbial decomposition of plant litter

  • Once plant litter was placed in contact with soil microorganisms, observed organic mass loss was significantly greater in litter previously exposed to solar radiation, suggesting that photodegradation primed the material for subsequent biological processing (“photopriming”)
  • Across all species, previous exposure to visible (BG) light enhanced subsequent biotic decomposition by 30%, on average (Fig. 2 A and B). In contrast, the UV component alone had no significant photopriming effect when considered across all species (Fig. 2 A and B).
  • UV actually has a negative photopriming effect for woody species (Fig. 2C and D)
Fig. 2.
  • 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%)
  • Nevertheless, these relatively small rates of mass loss during the photodegradative phase had an inordinately large impact on total decomposition, by promoting microbially driven losses of carbon during biotic degradation

Exposure to solar radiation consistently reduces lignin concentration of plant leaf litter

  • In the group of species used in our study, lignin concentration varied by a factor of nearly 10 (from 4% to 40%)
  • lignin concentration was significantly reduced in litter exposed to full solar radiation, and the BG component of sunlight had a much larger effect than the UV component (Fig. 3 A and B).
  • The large impact of BG light in reducing lignin can be explained on the basis of the spectral properties of lignin, which, in contrast to cellulose, has strong light absorbance in the BG region
Fig. 3.

Photodegradation facilitates access of microbial enzymes to cell wall polysaccharides through lignin degradation

  • positive effect of previous exposure to solar radiation on microbial decomposition of litter in the soil (Fig. 2 A and B) may be associated with the alleviation of lignin inhibition on cellulose–enzyme interactions.
  • lignin functions as a structural and hydrophobic barrier impeding access of microbial enzymes to plant cell wall polysaccharides, such as cellulose, making cell walls virtually impermeable to enzymatic degradation.
  • lignin inhibits cellulose hydrolysis by binding active sites of cellulolitic enzymes and reducing enzymatic efficiency
  • For all species, previous exposure of leaf litter to solar radiation significantly in- creased in vitro saccharification—in some cases up to 150% above nonexposed litter (Fig. 3 C and D)
  • These changes were almost certainly not due to thermal effects during photodegradation, because extended exposure of plant litter to high temperatures (60 °C) had no de- monstrable effect on these variables

Discussion

  • The lack of photopriming in litter of woody species (Fig. 2 C and D) may be related to the optical shielding of lignin molecules by other cell wall components, as woody species’ leaf litters are characterized by high leaf mass per unit area (LMA) and high abundance of other aromatic compounds such as polyphenols