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. 2018 Nov 23;9:1662.
doi: 10.3389/fpls.2018.01662. eCollection 2018.

Plant Nutrient Resource Use Strategies Shape Active Rhizosphere Microbiota Through Root Exudation

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Free PMC article

Plant Nutrient Resource Use Strategies Shape Active Rhizosphere Microbiota Through Root Exudation

Julien P Guyonnet et al. Front Plant Sci. .
Free PMC article

Abstract

Plant strategies for soil nutrient uptake have the potential to strongly influence plant-microbiota interactions, due to the competition between plants and microorganisms for soil nutrient acquisition and/or conservation. In the present study, we investigate whether these plant strategies could influence rhizosphere microbial activities via root exudation, and contribute to the microbiota diversification of active bacterial communities colonizing the root-adhering soil (RAS) and inhabiting the root tissues. We applied a DNA-based stable isotope probing (DNA-SIP) approach to six grass species distributed along a gradient of plant nutrient resource strategies, from conservative species, characterized by low nitrogen (N) uptake, a long lifespans and low root exudation level, to exploitative species, characterized by high rates of photosynthesis, rapid rates of N uptake and high root exudation level. We analyzed their (i) associated microbiota composition involved in root exudate assimilation and soil organic matter (SOM) degradation by 16S-rRNA-based metabarcoding. (ii) We determine the impact of root exudation level on microbial activities (denitrification and respiration) by gas chromatography. Measurement of microbial activities revealed an increase in denitrification and respiration activities for microbial communities colonizing the RAS of exploitative species. This increase of microbial activities results probably from a higher exudation rate and more diverse metabolites by exploitative plant species. Furthermore, our results demonstrate that plant nutrient resource strategies have a role in shaping active microbiota. We present evidence demonstrating that plant nutrient use strategies shape active microbiota involved in root exudate assimilation and SOM degradation via root exudation.

Keywords: active bacterial community; denitrification; microbial activities; microbiota; plant nutrient use strategies; rhizosphere; root exudation; stable isotope probing (SIP).

Figures

FIGURE 1
FIGURE 1
Correlation between (A) root exudation rate and SIR and (B) root exudation rate and DEA in the rhizosphere of six grasses, distributed on a gradient of plant resource use strategies. Specimens include Sesleria caerulea (SC), Festuca paniculata (FP), Anthoxanthum odoratum (AO), Berectu erectus (BE), Trisetum flavescens (TF) and Dactylis glomerata (DG), as well as BS (control, in the absence of plants). Data represent the means, and error bars represent SE. Significance level is at p < 0.05 between plants and BS.
FIGURE 2
FIGURE 2
Incorporation of 13C-root exudates into microbial community DNA derived from the RAS of Dactylis glomerata plants after 1 week of 13CO2 labeling. 12C (light) and 13C (heavy) DNA were separated by CsCl density gradient centrifugation. Total DNA was quantified fluorometrically (formula image), and 13C (∂13C) values were measured by IRMS within gradient fractions (1–10) (formula image).
FIGURE 3
FIGURE 3
Relative abundance of five major bacterial phyla in the rhizosphere of two conservative plants (Festuca paniculata and Sesleria caerulea) and four exploitative plants (Bromus erectus, Anthoxanthum odoratum, Dactylis glomerata, and Trisetum flavescens). The relative abundances were calculated as the ratio of the abundance of a phylum in a given plant divided by the mean abundance of this phylum in all plants. This was performed for every compartment: (A) bacteria feeding on SOM (light-DNA), (B) root exudate consumers (heavy-DNA), and (C) bacteria colonizing the root tissues.
FIGURE 4
FIGURE 4
Venn diagram displaying the shared and unique bacterial OTUs at 100% identity among light-DNA (SOM degraders), heavy-DNA, and root-DNA fractions (root exudate consumers) retrieved from (A) exploitative species [Bromus erectus (BE), Anthoxanthum odoratum (AO), Dactylis glomerata (DG), and Trisetum flavescens (TF)], (B) conservative species [Festuca paniculata (FP) and Sesleria caerulea (SC)], and (C) exploitative and conservative species [Bromus erectus (BE), Anthoxanthum odoratum (AO), Dactylis glomerata (DG), Trisetum flavescens (TF), Festuca paniculata (FP), and Sesleria caerulea (SC)].
FIGURE 5
FIGURE 5
Microbial networks of bacteria inhabiting (A) the RAS and involved in root exudate assimilation (heavy-DNA) or SOM degradation (light-DNA). Microbial networks of bacteria colonizing (B) the root tissues of conservative plants (Festuca paniculata and Sesleria caerulea) and exploitative plants (Bromus erectus, Anthoxanthum odoratum, Dactylis glomerata, and Trisetum flavescens). Each node represents a gene rRNA sequence, whereas the color indicates the phylum. Bacteria co-occurrence patterns, represented by gray lines, were assessed using a Bray–Curtis distance based on the repartition of OTUs in different plants and compartments. The resulting networks are positioned on a graph representing the gradient from conservative to exploitative plant species on the horizontal axis, and the gradient from SOM degraders (light-DNA) to root exudate consumers (heavy-DNA) on the vertical axis in graph (A). Overlapping nodes were scattered.

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