Phenolic acid-degrading Paraburkholderia prime decomposition in forest soil

Roland C Wilhelm,James P Shapleigh,Christopher M Derito,Daniel H Buckley,Eugene L Madsen

doi:10.1038/s43705-021-00009-z

Abstract

Plant-derived phenolic acids are catabolized by soil microorganisms whose activity may enhance the decomposition of soil organic carbon (SOC). We characterized whether phenolic acid-degrading bacteria enhance SOC mineralization in forest soils when primed with 13C-labeled p-hydroxybenzoic acid (pHB). We further tested whether pHB-induced priming could explain differences in SOC content among mono-specific tree plantations in a 70-year-old common garden experiment. pHB addition primed significant losses of SOC (3–13 µmols C g−1 dry wt soil over 7 days) compared to glucose, which reduced mineralization (-3 to -8 µmols C g−1 dry wt soil over 7 days). The principal degraders of pHB were Paraburkholderia and Caballeronia in all plantations regardless of tree species or soil type, with one predominant phylotype (RP11ASV) enriched 23-fold following peak pHB respiration. We isolated and confirmed the phenolic degrading activity of a strain matching this phylotype (RP11T), which encoded numerous oxidative enzymes, including secretion signal-bearing laccase, Dyp-type peroxidase and aryl-alcohol oxidase. Increased relative abundance of RP11ASV corresponded with higher pHB respiration and expression of pHB monooxygenase (pobA), which was inversely proportional to SOC content among plantations. pobA expression proved a responsive measure of priming activity. We found that stimulating phenolic-acid degrading bacteria can prime decomposition and that this activity, corresponding with differences in tree species, is a potential mechanism in SOC cycling in forests. Overall, this study highlights the ecology and function of Paraburkholderia whose associations with plant roots and capacity to degrade phenolics suggest a role for specialized bacteria in the priming effect.

Highlights

We have shown that an abundant aromatic microcosms was used to test whether priming could be induced acid in plant root exudates can prime decomposition mediated by the activity of phenolic-degrading bacteria.[15,54]
Our results demonstrate that the degradation of p-hydroxybenzoic acid can prime the decomposition of soil organic carbon (SOC) in a variety of forest and soil types
The predominant Paraburkholderia phylotypes were related to P. madseniana RP11T and P. xenovorans LB400T, species noted for having more genes and pathways for the degradation of phenolics and aromatics than close relatives,[54] and among the highest of any bacterial species.[80]

Summary

Introduction

Forest soils are rich in plant-derived phenolic acids which represent a sizeable proportion of fast-cycling, low-molecular weight soil organic carbon (SOC),[1] estimated at between 10 and 4000 mg · kg−1 dry organic layer soil.[2,3,4,5] Concentrations of soil phenolics fluctuate as a function of plant inputs and phenolic aciddegrading activity.[4,6,7,8,9,10] The cycling of soil phenolics has the potential to accelerate decomposition according to research linking phenolic acids, and phenol oxidase activity, to the soil priming effect.[11,12,13,14,15,16] The priming effect refers to the enhanced decomposition of SOC which can occur when an influx of new C stimulates microbial activity, which is a fundamental process in terrestrial C-cycling.[17,18] The activity of phenolic acid-degrading populations appear to be especially impactful, priming a greater loss of SOC (per unit biomass) than glucose or cellobiose.[14]. We would expect to find a link between phenolic acid-degrading populations, soil priming, and SOC accrual in nature. This link has not yet been tested and the identity and ecology of these populations, and the mechanisms behind their priming activity, remain poorly described

Methods

Results

Discussion

Conclusion