Abstract
The North American prairie covered about 3.6 million-km2 of the continent prior to European contact. Only 1–2% of the original prairie remains, but the soils that developed under these prairies are some of the most productive and fertile in the world, containing over 35% of the soil carbon in the continental United States. Cultivation may alter microbial diversity and composition, influencing the metabolism of carbon, nitrogen, and other elements. Here, we explored the structure and functional potential of the soil microbiome in paired cultivated-corn (at the time of sampling) and never-cultivated native prairie soils across a three-states transect (Wisconsin, Iowa, and Kansas) using metagenomic and 16S rRNA gene sequencing and lipid analysis. At the Wisconsin site, we also sampled adjacent restored prairie and switchgrass plots. We found that agricultural practices drove differences in community composition and diversity across the transect. Microbial biomass in prairie samples was twice that of cultivated soils, but alpha diversity was higher with cultivation. Metagenome analyses revealed denitrification and starch degradation genes were abundant across all soils, as were core genes involved in response to osmotic stress, resource transport, and environmental sensing. Together, these data indicate that cultivation shifted the microbiome in consistent ways across different regions of the prairie, but also suggest that many functions are resilient to changes caused by land management practices – perhaps reflecting adaptations to conditions common to tallgrass prairie soils in the region (e.g., soil type, parent material, development under grasses, temperature and rainfall patterns, and annual freeze-thaw cycles). These findings are important for understanding the long-term consequences of land management practices to prairie soil microbial communities and their genetic potential to carry out key functions.
Highlights
The original North American prairie was a 3.6 million-km2 expanse of fertile soil (Mollisols)
Alpha diversity was significantly higher overall in cultivated soils compared to native prairie soils (P = 0.006) and in switchgrass compared to native prairie soils (P < 0.04), within-state alpha diversity metrics were not significantly different between management practices (e.g., Iowa CC versus Iowa native tallgrass prairie (NP))
The primary hemicelluloses found in grass cell walls contain L-arabinose side chains (Scheller and Ulvskov, 2010), which may explain the high abundance of α-L-arabinofuranosidases (GH51, GH54, and GH62: 12.9–16.8%) in all of the samples examined. The former tallgrass prairie region of the Midwestern United States is an area of economic and ecological importance for food security, biofuel production, nutrient retention, and is a major terrestrial carbon store, that could be jeopardized with climate change (Boody and DeVore, 2006; Jordan and Warner, 2010; Jokela et al, 2011; Paustian et al, 2016)
Summary
The original North American prairie was a 3.6 million-km expanse of fertile soil (Mollisols). This region is highly productive agriculturally and the majority of the original prairie has been cultivated (Samson and Knopf, 1994). Besides replacing a speciesrich plant community with monoculture, land management induces changes in soil physicochemical characteristics. In 2016, agriculture was the source of 8.6% of total greenhouse gas emissions in the United States (USEPA, 2018). Thirty one to 39% of the total soil organic carbon (SOC) stocks of the conterminous United States are stored in prairie soils (Guo et al, 2006). Fertilizer application and other agricultural management practices induce N2O production, making croplands responsible for 76.7% of United States N2O emissions into the atmosphere (USEPA, 2018)
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