Leveraging microbiome rediversification for the ecological rescue of soil function

Abstract

Background: Global biodiversity losses threaten ecosystem services and can impact important functional insurance in a changing world. Microbial diversity and function can become depleted in agricultural systems and attempts to rediversify agricultural soils rely on either targeted microbial introductions or retaining natural lands as biodiversity reservoirs. As many soil functions are provided by a combination of microbial taxa, rather than outsized impacts by single taxa, such functions may benefit more from diverse microbiome additions than additions of individual commercial strains. In this study, we measured the impact of soil microbial diversity loss and rediversification (i.e. rescue) on nitrification by quantifying ammonium and nitrate pools. We manipulated microbial assemblages in two distinct soil types, an agricultural and a forest soil, with a dilution-to-extinction approach and performed a microbiome rediversification experiment by re-introducing microorganisms lost from the dilution. A microbiome water control was included to act as a reference point. We assessed disruption and potential restoration of (1) nitrification, (2) bacterial and fungal composition through 16S rRNA gene and fungal ITS amplicon sequencing and (3) functional genes through shotgun metagenomic sequencing on a subset of samples.

Results: Disruption of nitrification corresponded with diversity loss, but nitrification was successfully rescued in the rediversification experiment when high diversity inocula were introduced. Bacterial composition clustered into groups based on high and low diversity inocula. Metagenomic data showed that genes responsible for the conversion of nitrite to nitrate and taxa associated with nitrogen metabolism were absent in the low diversity inocula microcosms but were rescued with high diversity introductions.

Conclusions: In contrast to some previous work, our data suggest that soil functions can be rescued by diverse microbiome additions, but that the concentration of the microbial inoculum is important. By understanding how microbial rediversification impacts soil microbiome performance, we can further our toolkit for microbial management in human-controlled systems in order to restore depleted microbial functions.

Keywords: Biodiversity; Community inoculum; Microbial establishment; Microbial function; Nitrification.

Fig. 1

Experimental design schematic. *10⁻⁶ was chosen as the foundational microcosms to correspond to the N-cycling functional loss observed in Calderón et al. [31]. FZ and WC represent the frozen soil and water control, respectively (see Microbiome rediversification to restore nitrification)

Fig. 2

Loss and recovery of nitrification. Stacked bars of ammonium (red bars) and nitrate (blue bars) for sentinel (A, B) and rediversification (C, D) microcosms. Data are mean ± standard error. Note the differences in y-axis between the different soils and different microcosm experiments. See Additional file 1: Fig. S1 for non-stacked data

Fig. 3

Principal Coordinate Analysis (PCoA) ordinations of bacterial compositions (16S rRNA gene). Panels A and B are the farm and forest soils, respectively. Bacterial compositions from the microbiome rediversification experiment (circle shapes) cluster according to nitrification status (see Fig. 2; i.e. with large and minor nitrate pools) into high (restored) and low (disrupted) concentration rediversification microcosms. PCoA ordinations of fungal compositions are displayed as Additional file 1: Fig. S2.

Fig. 4

Summed relative abundance of taxa associated with nitrification. Panels A and B are the farm and forest soils, respectively. Additional taxa plots are shown as Additional file 1: Figs. S3 and S4.

Fig. 5

Linear trend between bacterial species richness and Bray dissimilarity to water control for bacterial composition. The gradient in bacterial species richness was generated by our microbiome rediversification concentration manipulations (color coded). Panels A and B are the farm and forest soils, respectively

Fig. 6

Nitrogen metabolism functional profile determined with shotgun metagenomic sequencing data and the DRAM functional profiler. Restored (Rec-0) and disrupted (Rec-6) microcosms from the Forest soil are shown. A complete functional profile is shown in Additional file 1: Figs. S8 and S9. The absence of nitrite-oxidation (red box) is observed in the disrupted microcosms