Increased temperature enhances microbial-mediated lignin decomposition in river sediment.

Abstract

Background: Lignin, as the most abundant recalcitrant organic carbon in terrestrial ecosystems, plays a crucial role in the Earth's carbon cycle. After lignin entering aquatic environments, portion of it tends to accumulate in sediments, forming a stable carbon relatively reservoir. However, the increasing temperature caused by human activities may impact microbial-mediated lignin decomposition, thereby affecting sedimentary carbon reservoirs. Therefore, revealing how temperature affects microbial-mediated lignin decomposition in river sediment, a topic that remains elusive, is essential for comprehending the feedbacks between river carbon reservoirs and climate. To address this, we conducted stable isotope probing of river surface sediment using ¹³C-lignin and ¹³C-vanillin, and utilized a series of techniques, including CO₂ production analysis, 16S rRNA gene amplicon sequencing, metagenomics, and metatranscriptomics, to identify the lignin-decomposing microbes and the effects of temperature on microbial-mediated lignin decomposition.

Results: We found that elevated temperatures not only increased the total sediment respiration (total CO₂) and the CO₂ emissions from lignin/vanillin decomposition, but also enhanced priming effects. The ¹³C-labled taxa, including Burkholderiales, Sphingomonadales, and Pseudomonadales, were identified as the main potential lignin/vanillin decomposers, and their abundances and activity significantly increased as temperature increased. Furthermore, we observed that increasing temperature significantly increased the activity of lignin decomposing pathways, including β-aryl ether fragments and 4,5-PDOG pathway. Additionally, as temperature increases, the transcriptional abundances of other carbon cycling related genes, such as pulA (starch decomposition) and xyla (hemicellulose decomposition), also exhibited increasing trends. Overall, our study elucidated the potential lignin-decomposing microbes and pathways in river sediment and their responses to temperature increasing.

Conclusions: Our study demonstrated that the temperature increasing can increase the rate of lignin/vanillin decomposition via affecting the activity of lignin-decomposing microbes. This finding indicates that the ongoing intensification of global warming may enhance the decomposition of recalcitrant organic carbon in river sediment, thereby impacting global carbon cycling. Video Abstract.