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Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System

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Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System

Daniel C Schlatter et al. Front Microbiol.

Abstract

Earthworms play important roles in no-till cropping systems by redistributing crop residue to lower soil horizons, providing macropores for root growth, increasing water infiltration, enhancing soil quality and organic matter, and stimulating nitrogen cycling. The soil impacted by earthworm activity, including burrows, casts, and middens, is termed the drilosphere. The objective of this study was to determine the effect of earthworms on soil microbial community composition in the drilosphere at different landscape slope positions. Soil cores (50 cm depth) were extracted from three landscape locations (top, middle, and bottom slope positions) on a sloping aspect of a no-till wheat farm. Soil was sampled at the bottom of the soil core from inside multiple earthworm (Lumbricus terrestris) channels (drilosphere) and from adjacent bulk soil. Bacterial communities were characterized for 16S rRNA gene diversity using high-throughput sequencing and functional denitrifier gene abundance (nirK, nirS, and nosZ) by quantitative PCR. Bacterial communities were structured primarily by the landscape slope position of the soil core followed by source (bulk versus drilosphere soil), with a significant interaction between core position and source. The families AKIW874, Chitinophagaceae, and Comamonadaceae and the genera Amycolatopsis, Caulobacter, Nocardioides, and Variovorax were more abundant in the drilosphere compared to the bulk soil. Most of the individual bacterial taxa enriched in the drilosphere versus bulk soil were members of Actinobacteria, including Micrococcales, Gaiellaceae, Solirubrobacterales, and Mycobacterium. In general, the greatest differences in communities were observed in comparisons of the top and bottom slope positions in which the bottom slope communities had significantly greater richness, diversity, and denitrifier abundance than the top slope position. Populations of denitrifiers (i.e., ratio of nirK+nirS to 16S rRNA) were more abundant in earthworm-impacted soils and there was a significant impact of L. terrestris on soil community composition which was observed only in the top landscape position. There were significant correlations between the abundance of nirK and nirS and taxa within Proteobacteria, Acidobacteria, Actinobacteria, Verrucomicrobia, and Chloroflexi, suggesting a broad diversity of denitrifying bacteria. Earthworms influence the soil microbial communities, but the impact depends on the slope location in a variable landscape, which likely reflects different soil characteristics.

Keywords: Pacific Northwest; direct seed; earthworms; microbiome; next-generation sequencing; soil.

Figures

FIGURE 1
FIGURE 1
(A) Map showing the locations of the top-slope (circle), mid-slope (triangle), and bottom-slope (plus sign) core positions within the Cook Agronomy Farm. Contour intervals are 1 m. (B) Example of earthworm burrows found in the 25 cm (10 inch) diameter extracted soil cores (viewed from the bottom at a depth of 50 cm).
FIGURE 2
FIGURE 2
Relative abundance [Log2(1+x)-transformed rarefied sequence counts] of bacterial phyla among slope positions (top-, mid-, bottom-slope) and soil sources (bulk, channel). Top, mid, and bottom refer to slope positions.
FIGURE 3
FIGURE 3
Non-metric multidimensional scaling plots of bacterial communities among (left; Stress = 0.044), and within individual soil cores (right; Stress = 0.09, 0.02, and 0.06 for bottom-, mid-, and top-slope samples, respectively). Top, mid, and bottom refer to slope positions.
FIGURE 4
FIGURE 4
Heatmap of bacterial family abundances [Log2(1+x)-transformed rarefied sequence counts] in different soil cores and drilosphere samples. Top, mid, and bottom refer to slope positions. Triangles indicate families that differ significantly among slope positions (Kruskal–Wallis test, FDR-adjusted p-value <0.1). Circles indicate families that differ significantly between bulk versus earthworm channel soil (Kruskal–Wallis test, FDR-adjusted p-value <0.1).
FIGURE 5
FIGURE 5
Heatmap of bacterial genera abundances [Log2(1+x)-transformed rarefied sequence counts] in different soil cores and drilosphere samples. Triangles indicate genera that differ significantly among slope positions (Kruskal–Wallis test, FDR-adjusted p-value <0.1). Circles indicate genera that differ significantly between bulk versus earthworm channel soil (Kruskal–Wallis test, FDR-adjusted p-value <0.1).
FIGURE 6
FIGURE 6
Differentially abundant OTUs between bulk and earthworm channel soil. The x-axis represents the DESeq2 estimated log2-fold difference in abundances between bulk and earthworm channel soil. Points are colored by the phylum to which they were classified and the size of the points indicates the mean abundance of that OTU among all samples.
FIGURE 7
FIGURE 7
Abundances of 16S rRNA, nirK and nirS gene copy numbers from bulk soil and earthworm channels among landscape slope positions. Different letters above bars indicate statistically significant differences (Tukey’s HSD, p < 0.05). A statistical evaluation of differences is also presented in Supplementary Table 5.

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