Phenolic acid-degradingParaburkholderiaprime decomposition in forest soil

Abstract

Plant-derived phenolic acids are metabolized by soil microorganisms whose activity may enhance the decomposition of soil organic carbon (SOC). We characterized whether phenolic acid-degrading bacteria would enhance SOC mineralization in forest soils when primed with 13C-labeled p-hydroxybenzoic acid (PHB). We further investigated whether PHB-induced priming could explain differences in SOC content among mono-specific tree plantations in a 70-year-old common garden experiment. The activity of Paraburkholderia and Caballeronia dominated PHB degradation in all soils regardless of tree species or soil type. We isolated the principal PHB-degrading phylotype (Paraburkholderia madseniana RP11T), which encoded numerous oxidative enzymes, including secretion signal-bearing laccase, aryl-alcohol oxidase and DyP-type peroxidase, and confirmed its ability to degrade phenolics. The addition of PHB to soil led to significant enrichment (23-fold) of the RP11T phylotype (RP11ASV), as well as enrichment of other phylotypes of Paraburkholderia and Caballeronia. Metabolism of PHB primed significant loss of SOC (3 to 13 µmols C g-1 dry wt soil over 7 days). In contrast, glucose addition reduced SOC mineralization (−3 to -8 µmols C g-1 dry wt soil over 7 days). RP11ASV abundance and the expression of PHB monooxygenase (pobA) correlated with PHB respiration and were inversely proportional to SOC content in the field. We propose that plant-derived phenolics stimulate the activity of phenolic acid-degrading bacteria thereby causing soil priming and SOC loss. We show that Burkholderiaceae dominate soil priming in diverse forest soils and this observation counters the prevailing view that priming phenomena are a generalized non-specific response of community metabolism.

Paraburkholderia madseniana sp. nov., a phenolic acid-degrading bacterium isolated from acidic forest soil

“…The unique capacity of P. madseniana to degrade phthalic acid supports its role in decomposition, since phthalic acids are common by-products of lignin-degradation [75–77] and phthalate dioxygenase and phthalate transporter genes were among several to confer high-levels of fitness to soil bacteria [78, 79]. P. madseniana was shown to prime the degradation of soil organic matter [49, 50], raising speculation about the role of its oxidative enzymes in carbon cycling.…”

“…Its isolation was part of an effort to characterize phenolic acid-degrading populations involved in soil priming and was isolated by enrichment culturing with 4-hydroxybenzoate. Of several 4-hydroxybenzoate-degrading bacteria isolated, strain RP11 T was identified as a principle agent of priming [50]. After serial dilution, a soil slurry was spread plated onto mineral salts media containing 3 mM 4-hydroxybenzoate as the sole carbon source (MSM-PHB; recipe in Table S2).…”

“…The capacity of soil isolates to degrade polycyclic aromatic hydrocarbons and halogenated phenols indicates a diverse role in degrading soil aromatics [11, 17, 47, 48]. In addition, aromatic- and phenolic acid-degrading Paraburkholderia have been implicated as principle contributors to the soil priming effect [49, 50].…”

Expression of macromolecular organic nitrogen degrading enzymes identifies potential mediators of soil organic N availability to an annual grass

“…Similar to its extracellular protease expression pattern, this clade also increased CAZy expression over time in litter-amended rhizosphere and at the last time point in unamended rhizosphere. Recent evidence shows that some Burkholderiales can be primed by root exudates to decompose soil organic carbon [50]. On the flip side, at the last time point the roots begin to age and potentially become a target for degradation, as evidenced by several of the upregulated CAZy groups targeting plant polysaccharides and their downstream byproducts [20].…”