Effects of environmental spatial variation in structuring ammonia-oxidizing microbial communities in arid grassland

The enormous biodiversity of soil microbial communities is likely caused, in part, by a similar diversity of soil microhabitats.  Understanding how the environmental properties that create diverse microbial habitats affect microbial community communities is necessary to predict responses of biogeochemistry to environmental perturbations. Nitrifying microbes play a key role in transforming bioavailable nitrogen and ammonia-oxidizing archaea (AOA) often dominate ammonia-oxidizing bacteria (AOB) in soil communities. While diversity studies have characterized the phylogenies of these functional groups, the niche-space and relative importance of nitrifier taxa is not well understood.

We chose a study ecosystem, the Colorado shortgrass steppe, where soil resources and environmental properties are strongly patterned by a plant-interspace spatial structure, creating well-defined soil microhabitats.  We investigated the composition of AOA communities across this structure and related gradients of inorganic nitrogen to determine how small-scale environmental variation affects microbial diversity.   We sampled vegetated soils (grass hummocks) and bare interspace soils, and measured soil properties (pH, moisture) and inorganic nitrogen concentrations (NH₄+ and NO₃-).  We built clone libraries (n=203) of AOA communities using the A subunit of the ammonia mono-oxygenase gene (amoA) and analyzed their compositions phylogenetically and with multivariate statistics.   

The vegetated soils contained 23% higher NH₄+ (p<0.0001) than interspace, while the interspace soils contained 11% higher NO₃- (p<0.001).  Vegetated soils contained greater total inorganic nitrogen (p<0.0001) and 13% greater moisture (p<0.0001) but there was no difference in pH. Insertion of our amoA clone sequences into a recently published phylogeny separated them into seven established Nitrososphaera subclusters.  Differences in diversity were primarily related to variations in NH₄+ concentration found across the plant-interspace patterns. Sequences falling into Nitrososphaera subcluster 3.2 (19% of total sequences), were found to be highly correlated with very low NH₄+ concentrations, while sequences in Nitrososphaera subcluster 3.1 (36% of total sequences) were highly correlated with high NH₄+ soils.  Disaggregation of taxa to specific operational taxonomic units (97% identification) revealed even stronger correlations to microhabitat.  These relationships are also supported by principal components analyses. The robust correlation of the dominant archaeal nitrifiers with NH₄+ levels indicates that these lineages may have niches defined along the primary soil structuring elements of this ecosystem, the plant-interspace structure. 

This work has important implications for our understanding of microbial niches and their potential effects on nutrient cycling.  It shows that archaeal communities can be structured by environmental properties and resource availability at small-scale.