Arid Ecosystem Vegetation Canopy-Gap Dichotomy: Influence on Soil Microbial Composition and Nutrient Cycling Functional Potential

ABSTRACT

Increasing temperatures and drought in desert ecosystems are predicted to cause decreased vegetation density combined with barren ground expansion. It remains unclear how nutrient availability, microbial diversity, and the associated functional capacity vary between the vegetated canopy and gap soils. The specific aim of this study was to characterize canopy versus gap microsite effect on soil microbial diversity, the capacity of gap soils to serve as a canopy soil microbial reservoir, nitrogen (N)-mineralization genetic potential (ureC gene abundance) and urease enzyme activity, and microbial-nutrient pool associations in four arid-hyperarid geolocations of the western Sonoran Desert, Arizona, United States. Microsite combined with geolocation explained 57% and 45.8% of the observed variation in bacterial/archaeal and fungal community composition, respectively. A core microbiome of amplicon sequence variants was shared between the canopy and gap soil communities; however, canopy soils included abundant taxa that were not present in associated gap communities, thereby suggesting that these taxa cannot be sourced from the associated gap soils. Linear mixed-effects models showed that canopy soils have significantly higher microbial richness, nutrient content, and organic N-mineralization genetic and functional capacity. Furthermore, ureC gene abundance was detected in all samples, suggesting that ureC is a relevant indicator of N mineralization in deserts. Additionally, novel phylogenetic associations were observed for ureC, with the majority belonging to Actinobacteria and uncharacterized bacteria. Thus, key N-mineralization functional capacity is associated with a dominant desert phylum. Overall, these results suggest that lower microbial diversity and functional capacity in gap soils may impact ecosystem sustainability as aridity drives open-space expansion in deserts.

IMPORTANCE Increasing aridity will drive a shift in desert vegetation and interspace gap (microsite) structure toward gap expansion. To evaluate the impact of gap expansion, we assess microsite effects on soil nutrients, microbiome community composition and functional capacity, and the potential of gap soils to serve as microbial reservoirs for plant root-associated microbiomes in an arid ecosystem. Results indicate that gap soils have significantly lower bioavailable nutrients, microbial richness, and N-mineralization functional capacity. Further, abundance of the bacterial urease gene (ureC) correlates strongly with N availability, and its major phylogenetic association is with Actinobacteria, the dominant phylum found in deserts. This finding is relevant because it identifies an important N-mineralization capacity indicator in the arid soil microbiome. Such indicators are needed to understand the relationships between interplant gap expansion and microbial diversity and functional potential associated with plant sustainability. This will be a critical step in recovery of land degraded by aridity stress.