Prevalent root-derived phenolics drive shifts in microbial community composition and prime decomposition in forest soil

Zwetsloot, Marie J.; Ucros, Juana Muñoz; Wickings, Kyle; Wilhelm, Roland C.; Sparks, Jed P.; Buckley, Daniel H.; Bauerle, Taryn L.

doi:10.1016/j.soilbio.2020.107797

Cited by 84 publications

(74 citation statements)

References 103 publications

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“…In RPLnC and BLLnC, identical Paraburkholderia phylotypes responded to both glucose and PHB additions ( Figure 2), yet only PHB induced positive priming (Figure 1). This phenomenon was apparent in a related study on soil priming, where the same Paraburkholderia phylotypes responded to benzoic acid and glucose amendment (also identical to our two major phylotypes), yet only benzoic acid elicited positive priming [11]. Notably, the co-addition of glucose and benzoic acid enhanced priming and coincided with an even greater increase in Paraburkholderia.…”

Section: Characteristics Of Phb-induced Soil Primingsupporting

confidence: 76%

“…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]…”

Section: Discussionmentioning

confidence: 95%

“…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].…”

Section: Introductionmentioning

confidence: 99%

“…Populations of Alpha-and Betaproteobacteriales are also abundant during white-rot decay of wood, where phenolic acid concentrations are high [41,42]; and in the rhizosphere, where roots exude phenolic acids to facilitate plant-microbe interactions [43,44]. Tree roots can exude high concentrations of PHB and benzoic acid [24,36], and benzoic acid can stimulate the growth of Paraburkholderia and Caballeronia (Burkholderiaceae) and prime decomposition [11]. Accordingly, we expect PHBdegraders to be relatively specialized and phylogenetically clustered relative to microbes that mediate priming from the addition of glucose [45].…”

Section: Introductionmentioning

confidence: 99%

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Phenolic acid-degradingParaburkholderiaprime decomposition in forest soil

Wilhelm

DeRito

Shapleigh

et al. 2020

Preprint

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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.

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Section: Characteristics Of Phb-induced Soil Primingsupporting

confidence: 76%

Section: Discussionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Phenolic acid-degradingParaburkholderiaprime decomposition in forest soil

Wilhelm

DeRito

Shapleigh

et al. 2020

Preprint

Self Cite

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“…However, plant roots, especially fine roots, which account for approximately 33% of the total primary production, have a high turnover rate (Shen et al 2017). Roots are increasingly regarded as one of the main carbon pools in belowground ecosystems because of their close contact with soil and long residence time during decomposition (Lehmann and Kleber 2015;Huangfu et al 2019;Zwetsloot et al, 2020). Wang et al (2017) also found that aboveground and belowground litter contribute equally to soil CO2 emissions.…”

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confidence: 99%

Leaf and Root Litter Species Identity Influences Bacterial Community Composition in Short-Term Litter Decomposition

et al. 2020

Preprint

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Background: Microorganisms play a crucial role in litter decomposition in terrestrial ecosystems. However, it remains unclear, which effects of leaf litter and root species on bacterial community composition and diversity after one year's decomposition. Methods: The leaf and fine roots litters of Robinia pseudoacacia , Quercus acutissima , Pinus tabulaeformis and Pinus densiflora , which are the dominant afforestation species in Mount Tai, were analysed using the Nylon litterbag method and Illumina Miseq high-throughput sequencing for the amplification of bacterial 16S rRNA V4-V5. We measured the remaining litter mass and the bacterial community composition and assessed the effects of leaf and root litter species on the bacterial community after one-year decomposition periods.Results: (1) The remaining masses of leaf and fine roots litters of the four plant species were significantly influenced by organ type and species. The remaining mass of fine root litter was smaller than that of leaf litter for broad-leaved species, and the opposite result was found for coniferous species. (2) The observed species Chao1 and phylogenetic diversity values were significantly lower for leaf litters than for fine root litter. The community richness index was positively correlated with the C content, C:N and lignin content and negatively correlated with N:P, N content and P content. The bacterial community structure differed significantly among leaf and root litter decomposition for the four species ( p <0.05). The bacterial community structure in leaf litter was most highly correlated with the initial N content and N:P. The bacterial community structure in fine roots was most highly correlated with the lignin content. (3) The bacterial phyla Bacteroidetes , Acidobacteria and Gemmatimonadetes were significantly affected by litter and species type, and the relative abundances of Firmicutes and Chloroflexi were only affected by litter type. The relative abundances of Acidobacteria , Firmicutes and Chloroflexi in fine root litter were higher than those in leaf litter, while the opposite result was found for Bacteroidetes . The bacterial genera Burkholderia-Paraburkholderia , Sphingomonas and Mucilaginibacter were affected by litter type ( p <0.05). The relative abundance of Burkholderia-Paraburkholderia in fine root litter was higher than that in leaf litter, while the opposite result was found for Bradyrhizobium , Sphingomonas and Mucilaginibacter . Pearson correlation analysis showed that the average relative abundance of the dominant phyla and genera was affected by the initial litter properties, especially for Bacteroides , Acidobacteria , Burkholderia , and Sphingomonas . Conclusions: Litter type, interaction between litter type and species were important than species in shaping the bacterial diversity and community composition in decomposing litter. And this were affected by initial chemical properties of the litter.

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Plants use rhizosphere metabolites to regulate soil microbial diversity

Wang

Zhang

et al. 2021

Land Degrad Dev

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Specific metabolites and secondary metabolites produced by plants and soil microbes play key roles in regulating organismal behaviour. At present, the variations in soil microbial communities mediated by plant rhizosphere metabolism in arid environments are still poorly understood. Therefore, we investigated the rhizosphere soil (RS) and bulk soil (BS) associated with five plant species adapted to the climate in the Mu Us Sandy Land and analysed the chemical composition of soil metabolites, microbial community composition and diversity, edaphic factors, and their relationships. Some metabolites with ecological functions (such as fatty acids, monoacylglycerides and diterpenoids) were detected in the RS and BS of the five plants. Correlation analysis results show that fatty acids and diterpenoids were significantly negatively correlated with drought‐adapted bacterial (Actinobacteria, Chloroflexi) and fungal taxa (class Glomeromycetes and family Nectriaceae), and the bacterial class Rubrobacteria and two fungal phyla Ascomycota and Glomeromycota were significantly negatively correlated with fatty acids and diterpenoids, respectively. Redundancy analysis (RDA) and Monte Carlo permutation results confirm that fatty acids and diterpenoids played critical roles in the variation in the soil microbial communities. Although soil edaphic factors (such as microbial biomass carbon and basal respiration) played important roles in shaping the microbial community, the results of partial least squares path modelling (PLS‐PM) show that plant‐mediated rhizosphere metabolism was the primary factor that affected microbial alpha and beta diversities. We conclude that plants under drought stress regulate microbial community structures by releasing certain fatty acids and secondary metabolites (such as diterpenoids). In addition, the bioactive metabolites released from the rhizosphere affect the soil microbial community more significantly and directly than edaphic factors. Overall, our study provides insight into the underground ecological processes mediated by plant rhizosphere metabolism.

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Prevalent root-derived phenolics drive shifts in microbial community composition and prime decomposition in forest soil

Cited by 84 publications

References 103 publications

Phenolic acid-degradingParaburkholderiaprime decomposition in forest soil

Phenolic acid-degradingParaburkholderiaprime decomposition in forest soil

Leaf and Root Litter Species Identity Influences Bacterial Community Composition in Short-Term Litter Decomposition

Plants use rhizosphere metabolites to regulate soil microbial diversity

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