Soil minerals affect taxon-specific bacterial growth

Abstract

Secondary minerals (clays and metal oxides) are important components of the soil matrix. Clay minerals affect soil carbon persistence and cycling, and they also select for distinct microbial communities. Here we show that soil mineral assemblages-particularly short-range order minerals-affect both bacterial community composition and taxon-specific growth. Three soils with different parent material and presence of short-range order minerals were collected from ecosystems with similar vegetation and climate. These three soils were provided with ¹⁸O-labeled water and incubated with or without artificial root exudates or pine needle litter. Quantitative stable isotope probing was used to determine taxon-specific growth. We found that the growth of bacteria varied among soils of different mineral assemblages but found the trend of growth suppression in the presence of short-range order minerals. Relative growth of bacteria declined with increasing concentration of short-range order minerals between 25-36% of taxa present in all soils. Carbon addition in the form of plant litter or root exudates weakly affected relative growth of taxa (p = 0.09) compared to the soil type (p < 0.01). However, both exudate and litter carbon stimulated growth for at least 34% of families in the soils with the most and least short-range order minerals. In the intermediate short-range order soil, fresh carbon reduced growth for more bacterial families than were stimulated. These results highlight how bacterial-mineral-substrate interactions are critical to soil organic carbon processing, and how growth variation in bacterial taxa in these interactions may contribute to soil carbon persistence and loss.

Fig. 1. Variation in bacterial community composition of the three soils studied.

A Venn diagram of the number of shared and unique bacterial amplicon sequence variances (ASVs) within each soil. B Non-metric multidimensional scaling (NMDS) of soil communities at the ASV level under water-only conditions, as well as under exudate and litter C addition. Distances of points within NMDS are based on relative abundances of ASVs.

Fig. 2. Bacterial community growth responses in soils of varying SRO mineral content under different substrate-additions.

A Grand mean excess atom fraction (EAF) ¹⁸O of all bacterial amplicon sequence variants (ASVs) present within each soil, common taxa shared across all soil types (484 ASVs), as well as taxa unique to each soil type. Error bars represent standard error of the mean. B Non-metric multidimensional scaling (NMDS) plots of EAF ¹⁸O for the 484 common taxa across soils and substrate-addition treatments (stress level = 0.11). Distances of points within NMDS are based on mean EAF ¹⁸O of ASVs.

Fig. 3. Growth responses by family in different soils and substrate additions.

Heatmap of mean relative growth rate (excess atom fraction ¹⁸O) of 70 families present in all soils under water-only (control), exudate-addition and litter-addition with at least two member taxa within each family. Darker colors depict lower growth rates, and lighter (green to yellow) depict higher growth rates. Bars with “+” symbols indicate families that had significantly higher growth rates under exudate or litter addition compared to the water-only treatment of the same soil type, while bars with “−” symbols indicate significantly lower growth rates compared to water-only conditions (CI 95%). Families are grouped by phylum alphabetically. Numbers in parentheses to the right of the heatmap indicate the number of ASVs grouped within each family.

Fig. 4. Phylogenetic tree of bacterial taxa based on 16S rRNA gene sequences and associated growth responses in presence of SRO minerals.

The phylogenetic tree is colored by phylum and labeled by phylogenetic group. The heatmap depicts the direction and magnitude of the slope of excess atom fraction (EAF) ¹⁸O per ASV over short-range order (SRO) mineral proportion within soil. Negative slopes correspond to amplicon sequence variants (ASVs) which grew less in soil with greater SRO minerals (indicating SRO suppression on growth) and positive slopes (red) correspond to ASVs which had positive correlation of relative growth rate and SRO mineral content (SRO stimulation on growth).