Metagenomic reconstruction of nitrogen and carbon cycling pathways in forest soil: Influence of different hardwood tree species

Abstract

The soil microbiome plays an essential role in processing and storage of nitrogen (N) and carbon (C) and is influenced by vegetation above-ground through imparted differences in chemistry, structure, mass of plant litter, root physiology, and dominant mycorrhizal associations. We used shotgun metagenomic sequencing to quantify the abundance and distribution of gene families involved in soil microbial N and C cycling beneath three deciduous hardwood tree species: ectomycorrhizal (ECM)-associated Quercus rubra (red oak), ECM-associated Castanea dentata (American chestnut), and arbuscular mycorrhizal (AM)-associated Prunus serotina (black cherry). Chestnut exhibited the most distinct soil microbiome of the three species, both functionally and taxonomically, with a general suppression of functional genes in the nitrification, denitrification, and nitrate reduction pathways. These changes were related to low inorganic N availability in chestnut stands as soil was modified by poor, low-N litter quality relative to red oak and black cherry soils. Previous studies have used field biogeochemical process rates, isotopic tracing, and targeted gene abundance measurements to study the influence of tree species on ecosystem N and C dynamics. However, these approaches do not enable a comprehensive systems-level understanding of the relationship between microbial diversity and dynamics of N and C below-ground. We analyzed microbial metagenomes from soils beneath red oak, American chestnut, and black cherry stands and showed that tree species can mediate the abundance of key microbial genes involved in N and (to a lesser extent) C metabolism pathways in soil. We compare gene abundance values to measures of N and C flux from incubated soil. Our results highlight the genetic framework underlying tree species’ control over soil microbial communities, and below-ground C and N metabolism, and may enable land managers to select tree species to maximize C and N storage in soils.