Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture

Abstract

Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with ¹³CO₂. The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived ¹³C was taken up by bacteria but that in long-term abandoned fields most of the root-derived ¹³C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.

Figure 1

The share of functional groups of fungi incorporating recently photosynthesized carbon by vegetation on soil cores of three land abandonment categories. The total amount of carbon from plants to fungi is calculated as an average of three soils for each of the three time categories using the excess ¹³C labeling information of the PLFA marker 18:2ω6c and set to 1 for the long-term soils. For assignment of ITS sequences to functional groups, see text.

Figure 2

Effect of the time since abandonment from agriculture on fungal classes in the samples calculated from the percentage of data. For significant differences between treatments, see Supplementary Figure S5.

Figure 3

Fungal functional groups using recently photosynthesized carbon from plants affected by the time since agricultural abandonment. The recently abandoned fields are represented by red bars, mid-term abandoned fields by blue and long-term abandoned fields by green. The bars represent averages and error bars represent s.e. The significant trends in time are shown in the figure; for significance between treatments, see text. The groups are ordered based on their abundances in samples starting from the most abundant group. The full colour version of this figure is available at ISME Journal online.

Figure 4

The AMF/pathogen ratio changing in time since agricultural abandonment. The recently abandoned fields are marked as red bars, mid-term abandoned fields as blue and long-term abandoned fields with green. The bars represent averages and error bars represent s.e. The full colour version of this figure is available at ISME Journal online.

Figure 5

Development of network topology abandonment time. Only significant (P<0.05) positive correlations are visualized. The node size is proportional to the percentage of abundance of the organism and edge darkness is scaled to the strength of the correlation (Pearson’s rho). OTUs presented in the figure are grouped to functional groups (see text) and colored based on function. Network parameters such as clustering coefficient, number of nodes, density and number of neighbors are presented in the figure. The full colour version of this figure is available at ISME Journal online.

Figure 6

Trends in mineralization rates, network topology and F:B ratio (a) and changes in soil food web and fungal functional groups (b) as a function of time since agriculture. B, bacterial channel; F, fungal channel.