Soil Macroinvertebrate Presence Alters Microbial Community Composition and Activity in the Rhizosphere

Abstract

Despite decades of research, our understanding of the importance of invertebrates for soil biogeochemical processes remains incomplete. This is especially true when considering soil invertebrate effects mediated through their interactions with soil microbes. The aim of this study was to elucidate how soil macroinvertebrates affect soil microbial community composition and function within the root zone of a managed grass system. We conducted a 2-year field mesocosm study in which soil macroinvertebrate communities were manipulated through size-based exclusion and tracked changes in microbial community composition, diversity, biomass and activity to quantify macroinvertebrate-driven effects on microbial communities and their functions within the rhizosphere. The presence of soil macroinvertebrates created distinct microbial communities and altered both microbial biomass and function. Soil macroinvertebrates increased bacterial diversity and fungal biomass, as well as increased phenol oxidase and glucosidase activities, which are important in the degradation of organic matter. Macroinvertebrates also caused distinct shifts in the relative abundance of different bacterial phyla. Our findings indicate that within the rhizosphere, macroinvertebrates have a stimulatory effect on microbial communities and processes, possibly due to low-intensity microbial grazing or through the dispersal of microbial cells and spores by mobile invertebrates. Our results suggest that macroinvertebrate activity can be an important control on microbially-mediated processes in the rhizosphere such as nitrogen mineralization and soil organic matter formation.

Keywords: mesocosms; microbial activity; rhizosphere; soil macroinvertebrates; soil microbial communities.

FIGURE 1

Non-metric multidimensional scaling (NMDS) of bacterial community from 16SrRNA (Bray–Curtis dissimilarities). Macroinvertebrate manipulations resulted in significant shifts in bacterial taxa (PERMANOVA, P < 0.01). Vectors indicate significant correlations (P < 0.05) between invertebrate densities and microbial community ordination scores for ordination axis two. Vectors include total macroinvertebrate density (macroinvertebrates), earthworm (earthworms), total mesofauna density (mesoinvertebrates) and oribatid mite density (oribatid mites). Non-significant vectors are not shown. Black symbols denote microbial communities from soils permitting macroinvertebrates. Gray symbols denote microbial communities from soils excluding macroinvertebrates. Squares indicate communities from year one and circles from year two.

FIGURE 2

Non-metric multidimensional scaling (NMDS) of fungal community from ITS (Bray–Curtis dissimilarities). Macroinvertebrate manipulations resulted in significant shifts in fungal taxa (PERMANOVA, P < 0.01). Vectors indicate significant correlations (P < 0.01) between invertebrate densities and microbial community ordination scores for ordination axis two. Vectors include total macroinvertebrate density (macroinvertebrates) and earthworm density (earthworms). Non-significant vectors are not shown. Black symbols denote microbial communities from soils permitting macroinvertebrates. Gray symbols denote microbial communities from soils excluding macroinvertebrates. Squares indicate communities from year one and circles from year two.

FIGURE 3

Microbial biomass based on phospholipid fatty acids (PLFAs) (nmol g^-1 soil, average ± standard error) in years 1 (y1) and 2 (y2) for total bacteria, total non-AMF fungi (fungi) and AMF. Mesocosms with macroinvertebrates (macro) are represented in dark gray and mesocosms excluding macroinvertebrates (meso) are in light gray. Asterisks denote significant differences between mesocosm treatments within years (P < 0.05).

FIGURE 4

Potential extracellular phenol oxidase (POX) activity (nmol g^-1 soil, average ± standard error) in years 1 and 2. Mesocosms with macroinvertebrates (macro) are represented in dark gray and mesocosms excluding macroinvertebrates (meso) are in light gray. Asterisks denote significant differences between mesocosm treatments within years (P < 0.05).

FIGURE 5

Potential extracellular β-glucosidase (BG) activity (nmol g^-1 soil, average ± standard error) in years 1 and 2. Mesocosms with macroinvertebrates (macro) are represented in dark gray and mesocosms excluding macroinvertebrates (meso) are in light gray. Asterisks denote significant differences between mesocosm treatments within years (P < 0.05).

FIGURE 6

Cumulative CO₂ (μg carbon g^-1 soil) over a 30 day incubation from mesocosm soils recovered following 2 years of burial. Mesocosms with macroinvertebrates (macro) are represented with a solid line and mesocosms excluding macroinvertebrates (meso) are represented with a dashed line. Asterisks denote significant differences between mesocosm treatments (P < 0.05).

FIGURE 7

Ammonium and nitrate mineralization (μg g^-1 soil, average ± standard error) following 30 days of incubation of mesocosm soils collected after 2 years of burial. Mesocosms with macroinvertebrates (macro) are represented in dark gray and mesocosms excluding macroinvertebrates (meso) are in light gray. Asterisks denote significant differences between mesocosm treatments (P < 0.05).