Variations in the structure and function of the soil fungal communities in the traditional cropping systems from Madeira Island

Abstract

Agricultural soils are responsible for ecological functions and services that include primary production of food, fiber and fuel, nutrient cycling, carbon cycling and storage, water infiltration and purification, among others. Fungi are important drivers of most of those ecosystem services. Given the importance of fungi in agricultural soils, in this study, we aimed to characterize and analyse the changes of the soil fungal communities of three cropping systems from Madeira Island, where family farming is predominant, and investigate the response of fungi and its functional groups to soil physicochemical properties. To achieve that, we sequenced amplicons targeting the internal transcribed spacer 1 (ITS1) of the rRNA region, to analyse soil samples from 18 agrosystems: 6 vineyards (V), 6 banana plantations (B) and 6 vegetable plantations (H). Our results showed that alpha diversity indices of fungal communities are similar in the three cropping systems, but fungal composition and functional aspects varied among them, with more pronounced differences in B. Ascomycota, Basidiomycota, and Mortierellomycota were the main phyla found in the three cropping systems. Agaricomycetes and Sordariomycetes are the predominant classes in B, representing 23.8 and 22.4%, respectively, while Sordariomycetes (27.9%) followed by Eurotiomycetes (12.3%) were the predominant classes in V and Sordariomycetes (39.2%) followed by Tremellomycetes (8.9%) in the H. Saprotrophs are the fungal group showing higher relative abundance in the three cropping systems, followed by plant pathogens. Regarding symbionts, endophytes were highly observed in B, while mycorrhizal fungi was predominant in V and H. The structure of fungal communities was mainly correlated with soil content of P, K, N, Fe, and Cu. In addition, we identified bioindicators for each cropping system, which means that cultivated crops are also drivers of functional groups and the composition of communities. Overall, the three cropping systems favored diversity and growth of taxa that play important roles in soil, which highlights the importance of conservative management practices to maintain a healthy and resilient agrosystem.

Keywords: functional communities; microbial communities; soil biodiversity; soil mycobiota; sustainable agriculture.

Figure 1

Location of agrosystems under study along Madeira Island. B1–B6 is for banana plantations, V1–V6 is for vineyards and H1–H6 is for vegetable plantations.

Figure 2

Comparison of the soil fungal communities in the cropping systems (B, V, and H). (A) NMDS ordination plot based on unweighted UniFrac distance metric for the 18 sampling sites (in duplicates) and pairwise ANOSIM R test results. (B) NMDS based on weighted UniFrac distance metric for the 18 sampling sites (in duplicates) and pairwise ANOSIM R test results. (C) Venn diagram showing the number of unique and shared ASVs among and between cropping systems.

Figure 3

Relative abundance of fungal taxa in each cropping system from phylum to family (A–D). For class, order and family only the 10 most abundant taxa are discriminated in the graphics.

Figure 4

Differences found in fungal community composition of different cropping systems. (A) Heatmap of top 35 most abundant genera with the abundance increasing from blue to red, after Z-score normalization. Z values, depicted by colors, indicate the content of fungal species among groups at the genus level. (B) Cladogram indicating the polygenetic distribution of fungi. The color of the nodes in the diagram represents the groups that play significant roles in the matching cropping system, while yellow nodes indicate unimportant fungal groups. (C) The LDA value distribution histogram shows the taxonomic levels with higher significant differences in abundance in the different cropping systems. Higher scores of LDA represent higher influence of the taxa.

Figure 5

Variation of relative abundance of fungal functional groups in each cropping system. (A–E) Saprotrophs; (F–I) Symbiotrophs; (J–L) Pathotrophs. Boxes with different letters indicate a significant difference among them (Kruskal-Wallis, p < 0.05).

Figure 6

Principal coordinate analysis (PCA) based on soil physicochemical properties in cropping systems B, V, and H.

Figure 7

Observed Spearman significant correlations between soil physicochemical properties and (A) diversity indices, (B) key fungal genus identified as bioindicators in LefSe, (C) functional groups. Symbol * for p < 0.05; ** for p < 0.01. OM, Organic Matter; CEC, Cation Exchange Capacity; SD, Saturation Degree; Obs.ASV, Richness; E, Pielou Evenness; H′, Shannon–Wiener diversity index; Endoph, Endophytes; Ectomyc., Ectomycorrhizal; Und., Undefined.