Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

Abstract

Background: In a warmer world, microbial decomposition of previously frozen organic carbon (C) is one of the most likely positive climate feedbacks of permafrost regions to the atmosphere. However, mechanistic understanding of microbial mediation on chemically recalcitrant C instability is limited; thus, it is crucial to identify and evaluate active decomposers of chemically recalcitrant C, which is essential for predicting C-cycle feedbacks and their relative strength of influence on climate change. Using stable isotope probing of the active layer of Arctic tundra soils after depleting soil labile C through a 975-day laboratory incubation, the identity of microbial decomposers of lignin and, their responses to warming were revealed. Results: The β-Proteobacteria genus Burkholderia accounted for 95.1% of total abundance of potential lignin decomposers. Consistently, Burkholderia isolated from our tundra soils could grow with lignin as the sole C source. A 2.2°C increase of warming considerably increased total abundance and functional capacities of all potential lignin decomposers. In addition to Burkholderia, α-Proteobacteria capable of lignin decomposition (e.g. Bradyrhizobium and Methylobacterium genera) were stimulated by warming by 82-fold. Those community changes collectively doubled the priming effect, i.e., decomposition of existing C after fresh C input to soil. Consequently, warming aggravates soil C instability, as verified by microbially enabled climate-C modeling. Conclusions: Our findings are alarming, which demonstrate that accelerated C decomposition under warming conditions will make tundra soils a larger biospheric C source than anticipated.

Phenolic acid-degradingParaburkholderiaprime decomposition in forest soil

“…P. madseniana RP11 T also grows on phthalic acid [63], a major by-product of lignin degradation [89][90][91]. Indeed, our analysis demonstrated that the two major PHB-degrading phylotypes of Paraburkholderia predominated in studies of lignin degradation [40], and white rot decay [41], and were the principal degraders in all soil priming experiments where phenolic/aromatic compounds were utilized [10][11][12] (see Supplementary Results). All evidence indicates that Paraburkholderia, and close relatives, monopolize phenolic acid degradation in soil and co-metabolize SOC, resulting in priming of SOC stocks.…”

“…While glucose addition stimulated growth of Paraburkholderia, it also stimulates a wide diversity of microorganisms whose competitive interactions likely govern the magnitude and direction of the priming response. In contrast, additions of PHB (Figure 1), benzoate [11] or vanillin [10,12]…”

“…Amplicon libraries were deposited in the European Sequence Archive under the BioProject accession PRJEB23740. Following sequencing processing (described below), amplicon sequence variants (phylotypes) were designated as PHB-degraders when their relative abundance was at least 8-fold greater in heavy CsCl fractions (F3-F8) in 13 C-enriched versus 12 Ccontrol amplicon libraries, after variance stabilization by DESeq2 (v. 1.24.0) [61]. Phylotypes increasing in response to substrate additions in the priming experiment were identified by indicator species analyses using the R package 'indicspecies' [62].…”

“…Paraburkholderia are commonly associated with poplar roots [114,115] where phenolic acids may stimulate their priming, nitrogen fixing [105,111,116] or mineral phosphorus-solubilizing activities [117,118]. We hypothesize that certain tree species, and likely other plants, modulate the phenolic acid content of root exudates to recruit and stimulate phenolic acid-degrading bacteria to prime SOC degradation and access soil nutrients ( Figure 7E [12]. Together, these findings illustrate the potential utility for tracking priming dynamics with PobA, a key enzyme in the peripheral degradation of phenolic acids [50].…”

“…Phenolic acid concentrations fluctuate widely in soils (3-to 4-fold) in response to seasonal plant inputs and phenolic aciddegrading activity [1][2][3][4][5][6]. Several studies have linked the activity of phenolic acid-degrading populations to the soil priming effect [7][8][9][10][11][12], a key component of terrestrial C-cycling [13,14].…”