Soil warming and fertilization altered rates of nitrogen transformation processes and selected for adapted ammonia-oxidizing archaea in sub-arctic grassland soil

Anne Daebeler, Paul L.E. Bodelier, Mariet M. Hefting, Tobias Rütting, Zhongjun Jia, Hendrikus J. Laanbroek

Netherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, Wageningen, The Netherlands.

Abstract

The balance of microbial nitrogen (N) transformation processes in sub-arctic terrestrial ecosystems is most likely affected by global change, with potential feedbacks to greenhouse gas emissions and eutrophication. Soil temperature and N availability – their global increases being two of the most pressing global change features - will be prime drivers of N dynamics and microbial community structure, but little is known about their interactive effects in these ecosystems. We utilized geothermally warmed soils from Iceland as a natural experiment for assessing fertilization and warming effects on gross soil N transformation processes. Experimental incubations of these soils at different temperatures coupled with a dual ¹⁵N-labelling/-tracing approach and pyrotag transcript-sequencing allowed for the analysis of independent and combined impacts of N fertilization and temperature shifts on gross N mineralisation, nitrification, and ammonium and nitrate immobilisation rates and archaeal ammonia-oxidizing (AOA) communities, being the key ammonia oxidizers in this soil. Gross nitrification in warmed soil was increased in relation to ambient temperature soil and exhibited a higher temperature optimum. Concomitantly, our results revealed a selection of AOA populations adapted to in situ soil temperatures. Phylogenetically distinct populations of actively ammonia-oxidizing archaea exhibited conserved temperature optima.

N mineralization and nitrification showed higher sensitivities in response to short-term temperature changes if the soils had been warmed. In part, the influence of short-term temperature changes could however be neutralized by the effects of N fertilization. Long-term N fertilization alone affected only gross N mineralization. However, all gross N transformation rates were significantly altered by the interactive effects of N fertilization and soil warming. We conclude that in order to reliably predict effects of global change on sub-arctic soil N transformation processes we need to consider multiple interactions among global change factors and to take into account the capacity of soil microbial populations to adapt to global change conditions.

Keywords: ¹⁵N-tracing; ¹⁵N-pool-dilution; Nitrogen cycle; Climate change; Ammonia-oxidizing archaea; Warming; N enrichment.