Abstract

Winter air temperatures are rising faster than summer air temperatures in high-latitude forests, increasing the frequency of soil freeze/thaw events in winter. To determine how climate warming and soil freeze/thaw cycles affect soil microbial communities and the ecosystem processes they drive, we leveraged the Climate Change across Seasons Experiment (CCASE) at the Hubbard Brook Experimental Forest in the northeastern United States, where replicate field plots receive one of three climate treatments: warming (+5°C above ambient in the growing season), warming in the growing season + winter freeze/thaw cycles (+5°C above ambient +4 freeze/thaw cycles during winter), and no treatment. Soil samples were taken from plots at six time points throughout the growing season and subjected to amplicon (rDNA) and metagenome sequencing. We found that soil fungal and bacterial community composition were affected by changes in soil temperature, where the taxonomic composition of microbial communities shifted more with the combination of growing-season warming and increased frequency of soil freeze/thaw cycles in winter than with warming alone. Warming increased the relative abundance of brown rot fungi and plant pathogens but decreased that of arbuscular mycorrhizal fungi, all of which recovered under combined growing-season warming and soil freeze/thaw cycles in winter. The abundance of animal parasites increased significantly under combined warming and freeze/thaw cycles. We also found that warming and soil freeze/thaw cycles suppressed bacterial taxa with the genetic potential for carbon (i.e., cellulose) decomposition and soil nitrogen cycling, such as N fixation and the final steps of denitrification. These new soil communities had higher genetic capacity for stress tolerance and lower genetic capacity to grow or reproduce, relative to the communities exposed to warming in the growing season alone. Our observations suggest that initial suppression of biogeochemical cycling with year-round climate change may be linked to the emergence of taxa that trade-off growth for stress tolerance traits.

Highlights

  • High-latitude biomes such as boreal and temperate forests have experienced the fastest rates of climate warming of any ecosystem since the industrial revolution (Stocker et al, 2013) and future greenhouse gas emissions are expected to increase mean annual air temperatures at these locations in the coming century (HoeghGuldberg et al, 2018)

  • While the composition of microbial communities changed across Change across Seasons Experiment (CCASE) treatments, the richness of bacterial and fungal taxa in soils did not differ between any of the treatments (Supplementary Figure 1)

  • Our results indicate that winter climate change reshapes the soil microbial community beyond the impact of growing-season warming alone, promoting the emergence of stress-tolerant taxa that could have long-term impacts on C and N cycling in forest soils

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Summary

Introduction

High-latitude biomes such as boreal and temperate forests have experienced the fastest rates of climate warming of any ecosystem since the industrial revolution (Stocker et al, 2013) and future greenhouse gas emissions are expected to increase mean annual air temperatures at these locations in the coming century (HoeghGuldberg et al, 2018). Additional storage or loss of soil C and nutrients over the longer term will be determined by how the biogeochemical cycling activities of soil microorganisms (“effect traits”) are linked to traits that allow microbial species to persist under environmental stressors (“response traits”) (Allison and Martiny, 2008; Shade et al, 2012; Koide et al, 2014) Both warming and reduced winter snow cover can affect the species composition of soil microbial communities (Lipson and Schmidt, 2004; Allison and Treseder, 2008; Castro et al, 2010; Aanderud et al, 2013; Buckeridge et al, 2013; Luo et al, 2014; DeAngelis et al, 2015; Pold et al, 2015; Fernandez et al, 2016). If we could link shifts in the taxonomic composition of soil microbial communities due to climate change in these regions with community-level physiology of the soil microbiome, we might be able to better anticipate future changes in forest C and nutrient cycling on regional or global scales

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