Response of Oxidative Enzyme Activities to Nitrogen Deposition Affects Soil Concentrations of Dissolved Organic Carbon

Abstract

Recent evidence suggests that atmospheric nitrate (NO ⁻₃ ) deposition can alter soil carbon (C) storage by directly affecting the activity of lignin-degrading soil fungi. In a laboratory experiment, we studied the direct influence of increasing soil NO ⁻₃ concentration on microbial C cycling in three different ecosystems: black oak–white oak (BOWO), sugar maple–red oak (SMRO), and sugar maple–basswood (SMBW). These ecosystems span a broad range of litter biochemistry and recalcitrance; the BOWO ecosystem contains the highest litter lignin content, SMRO had intermediate lignin content, and SMBW leaf litter has the lowest lignin content. We hypothesized that increasing soil solution NO ⁻₃ would reduce lignolytic activity in the BOWO ecosystem, due to a high abundance of white-rot fungi and lignin-rich leaf litter. Due to the low lignin content of litter in the SMBW, we further reasoned that the NO ⁻₃ repression of lignolytic activity would be less dramatic due to a lower relative abundance of white-rot basidiomycetes; the response in the SMRO ecosystem should be intermediate. We increased soil solution NO ⁻₃ concentrations in a 73-day laboratory incubation and measured microbial respiration and soil solution dissolved organic carbon (DOC) and phenolics concentrations. At the end of the incubation, we measured the activity of β-glucosidase, N-acetyl-glucosaminidase, phenol oxidase, and peroxidase, which are extracellular enzymes involved with cellulose and lignin degradation. We quantified the fungal biomass, and we also used fungal ribosomal intergenic spacer analysis (RISA) to gain insight into fungal community composition. In the BOWO ecosystem, increasing NO ⁻₃ significantly decreased oxidative enzyme activities (−30% to −54%) and increased DOC (+32% upper limit) and phenolic (+77% upper limit) concentrations. In the SMRO ecosystem, we observed a significant decrease in phenol oxidase activity (−73% lower limit) and an increase in soluble phenolic concentrations (+57% upper limit) in response to increasing NO ⁻₃ in soil solution, but there was no significant change in DOC concentration. In contrast to these patterns, increasing soil solution NO ⁻₃ in the SMBW soil resulted in significantly greater phenol oxidase activity (+700% upper limit) and a trend toward lower DOC production (−52% lower limit). Nitrate concentration had no effect on microbial respiration or β-glucosidase or N-acetyl-glucosaminidase activities. Fungal abundance and basidiomycete diversity tended to be highest in the BOWO soil and lowest in the SMBW, but neither displayed a consistent response to NO ⁻₃ additions. Taken together, our results demonstrate that oxidative enzyme production by microbial communities responds directly to NO ⁻₃ deposition, controlling extracellular enzyme activity and DOC flux. The regulation of oxidative enzymes by different microbial communities in response to NO ⁻₃ deposition highlights the fact that the composition and function of soil microbial communities directly control ecosystem-level responses to environmental change.