Elsevier

European Journal of Soil Biology

Volume 61, March–April 2014, Pages 41-48
European Journal of Soil Biology

Original article
Plant traits regulating N capture define microbial competition in the rhizosphere

https://doi.org/10.1016/j.ejsobi.2014.01.002Get rights and content

Highlights

  • Plants maintain fast microbial turnover to mitigate N deficit.

  • Retardation of microbial growth in the rhizosphere as a result of N capture by plant.

  • Species-specific plant–microbial interactions based on r – K selection.

  • Plant neophytes–strong competitors for N as a threat to boost soil priming effect.

Abstract

Global warming and nitrogen (N) deposition promote the displacement of native plant species by neophytes which have similar ecological niches but stronger competitive abilities. It remains unclear how plants with different competitive abilities alter microbial growth and turnover in the rhizosphere under high and low N input. We hypothesized 1) slower microbial growth in the rhizosphere of plants with smaller roots and 2) restriction of microbial growth under low versus high N amendment. These hypotheses were tested on two strawberry species: Fragaria vesca (native species) and Duchesnea indica (an invasive plant in central Europe) grown under intra-specific and inter-specific competition at very low and high N levels.

Species-specific traits of plant–microbial interactions mitigated N deficiency in the rhizosphere. At low N addition the native species F. vesca stimulated faster microbial growth and turnover than D. indica. F. vesca did this by increasing root mass and exudation at the expense of the shoots. In contrast, the invasive plant – D. indica – did not increase root mass under low N amendment, but did increase its N uptake rate. This resulted in N deficiency, retarding microbial growth and turnover in the rhizosphere, as revealed by the dominance of slow-growing microorganisms.

A low N level in the soil promoted root growth and rhizodeposition and thus accelerated microbial turnover correspondingly to increasing root mass. Fast N uptake by roots, however, may lead to N deficiency and did retard microbial growth in the rhizosphere. In conclusion, the plant species with the stronger competitive ability at low N level controls the microbial community in the rhizosphere.

Introduction

Global warming and nitrogen (N) deposition promote the invasion of neophytes (i.e. plant species non-native to a geographical region) and the displacement of native plant species that have similar ecological niches but lower competitive abilities under new conditions. These plant community changes alter the structure and functioning of the below-ground microbial community, especially in the rhizosphere – one of the most important ‘hot spots’ in soil. This designation accurately describes this microhabitat: it is characterized not only by an accelerated turnover of microbial biomass and nutrients [34], but also by strong competition both at the population level (plant species-specific, microbial species-specific interactions) and at the community level (plant–microbial interactions). At the community level, plant species and even individual plants determine the composition of the rhizosphere microbial community [23], [21]. Remarkably, under inter-specific competition, low-biomass plant neophytes (e.g. grasses) influence the below-ground microbial community even more profoundly than do dominant high-biomass shrub species due to greater N acquisition by low- versus high-biomass plants [37]. As N is a key growth-limiting nutrient in natural ecosystems [45], the competitive strategy of microorganisms depends both on interactions with the plant community and on N availability [20]. At high N availability, grassland plants acquired N less efficiently than soil microorganisms [22]. N limitation increases the amount of exudates released [30], thus affecting the rhizosphere microorganisms' depolymerization of N-containing polymers. This increases the fraction of organic N uptake by plants [42]. Depending on the intensity of N limitation, the root growth may decrease [39] or, in contrast, increase (especially that of fine roots [25]. It remains unclear how plants with various competitive abilities alter the functions of rhizosphere microorganisms and competition for N. Despite the wide range of studies examining plant–microbial interactions, a quantitative evaluation of the microbial growth and competitive abilities in the rhizosphere is currently lacking [40], [17].

The lack of estimations characterizing the functional parameters of microbial growth kinetics is due to the absence of direct methods for satisfactorily estimating microbial growth in situ. An indirect approach suitable for estimating microbial growth parameters is based on the kinetics of substrate-induced growth respiration [10], [44]. This approach characterizes the growth rates of a whole microbial community according to the microbial growth model proposed by Ref. [35]. The model reflects the transition of soil microorganisms from a ‘sustaining’ [43] to an active state, considering both the lag-phase and phase of exponential growth after substrate addition. Although the method requires adding large amounts of substrate to provide exponential (unlimited) microbial growth, the fraction of microorganisms initially active in un-amended soil is characterized by the kinetic parameters such as microbial specific growth rate (μ), lag-time and fraction of active microbial biomass. Furthermore, the turnover rate of active microbial biomass calculated by μ (see Methods section) is linked to the intensity of nutrient cycling in microbial community [7]. Thus, the microbial turnover rate indirectly indicates the relative intensity of N uptake and release by microorganisms.

A comparison of the effects on rhizosphere microorganisms is especially meaningful between plants with similar biology and ecological niche requirements but contrasting competitive abilities [8], [9]. The Indian mock strawberry [Duchesnea indica (Andrews) Focke] is an invasive plant in central Europe. Its spontaneous distribution in Germany, Austria and Switzerland is positively correlated with the average annual temperature [32]. Thus, a warming climate could promote its distribution range. To measure its competitive ability, D. indica can be compared with Fragaria vesca L., a native species with similar growth strategy and biology. Both are perennial herbs belonging to the Rosaceae family and spread effectively via runners. Based on the differences in root anatomy [1], which may affect nutrient and water transport rates and thus determine the competitive ability for below-ground resources, we selected these species to evaluate their effect on rhizosphere microorganisms. We hypothesized: 1) slower microbial growth rates and turnover in the rhizosphere of plants with smaller root biomass, and 2) a greater effect of N availability on microbial growth in the rhizosphere of plants with high competitive abilities.

The competition belowground is revealed at both the population level: competition between (inter-specific) and within (intra-specific) plant species, and at the community level: plant–microbial interactions. Both levels of competition become more acute under conditions of nutrient limitation. This study therefore evaluates the effects of plants with different competitive abilities – F. vesca L. and D. indica growing in intra-specific and inter-specific competition – on changes of belowground microbial growth and turnover depending on level of N amendment.

Section snippets

Experimental design

Two species of strawberry – F. vesca L. and D. indica (Andrews) Focke – were grown in microcosms with a volume of 310 cm³ in a temperature-controlled greenhouse (mean temperature 19 °C). Each microcosm was filled with a 50:50 mixture of soil and quartz sand to decrease the N availability of the soil (slightly loamy stagnic gleysol, Ctotal 0.6%, Ntotal 0.05%, pH 5.1 from grassland at the Ecological- Botanical Garden of the University of Bayreuth). Prior to potting, soil was passed through a 5 mm

Competition at a population level: plant species' response to the level of N amendment

At a high level of N amendment, D. indica had greater total plant biomass (Table 1) and similar root mass as compared with F. vesca (Fig. 1). At low N, both species did not differ significantly in total mass, whereas the root mass was significantly higher for F. vesca. Thus, both plants decreased shoot mass at low versus high N treatment (Fig. 1). However, F. vesca increased root mass to overcome N limitation, while the root biomass of D. indica was not changed significantly at low versus high

Root-mediated functioning of microbial communities under competition for N

We showed that D. indica had a smaller root biomass, a lower N content in roots, a faster N uptake, and a greater shoot-to-root ratio compared to F. vesca. Accordingly, at the population level (competition between plant species), D. indica is stronger competitor for N than F. vesca, especially in N-rich environments [33]. At the community level (plant–microbial competition), however, the high competitive abilities of D. indica for N affected the soil microorganisms only at N limitation. This

Conclusions

Our study revealed that strategies of plant species to mitigate N deficit by root–microbial interactions depend on plant traits regulating N capture. Plants can actively control microbial metabolism by changing root mass, rhizodeposition and/or N uptake rate. This results in plant-specific rhizosphere microbial communities [23].

The root mass of the native species (F. vesca) increased under N limitation to compensate for the lack of nutrients, maintaining the fast-growing microorganisms (Fig. 5

Acknowledgements

The study was supported by European Commission (Marie Curie IIF program, project MICROSOM), by DAAD (German Academic Exchange Service) and by Russian Academy of Sciences (Leading Scientific School Program-No 6123.2014.4).

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