Soil Microbes Trade-Off Biogeochemical Cycling for Stress Tolerance Traits in Response to Year-Round Climate Change

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.

Exploring Trait Trade-Offs for Fungal Decomposers in a Southern California Grassland

“…Empirical evidence for these trade-offs is strong for some, but limited for others. Several studies document trade-offs between growth yield and stress tolerance ( Sterne and McCarver, 1978 ; Killham and Firestone, 1984 ; Dijksterhuis and de Vries, 2006 ; Gasch, 2007 ; Tiemann and Billings, 2011 ; Crowther et al, 2014 ; Garcia et al, 2020 ; Malik et al, 2020a ). In contrast, trade-offs between resource acquisition and the other traits are less commonly studied.…”

Trait-trait relationships and tradeoffs vary with genome size in prokaryotes

“…This inference however contradicts the often observed and above outlined tradeoff between resistance and resilience in microbial communities (e.g. Ferenci, 2016; Garcia et al ., 2020; Piton et al ., 2021). A resistance-resilience tradeoff would instead imply a negative correlation between resistance associated traits, such as genome size or transcription factors versus resilience associated traits, such as rRNA gene copy numbers or growth rates.…”

“…Such tradeoffs between resistance and resilience have been described not only at the species but also at the community level (e.g. de Vries and Shade, 2013; Garcia et al, 2020; Piton et al, 2021).…”

Soil age and soil organic carbon content shape biochemical responses to multiple freeze–thaw events in soils along a postmining agricultural chronosequence

“…Accordingly, a longer history of soil freezing (i.e. older soils) may select for frost-tolerant microbial traits and communities that are physiologically better adapted to FT cycles (Walker et al 2006;Garcia et al 2020). Indeed, a recent metagenomic study by Schmidt et al (2020) showed highly distinct clusters of bacterial communities with soil age in restored loess soils of a comparable soil chronosequence in Inden.…”

“…Soil age was recently identified as an important local-scale driver of ecosystem properties such as soil pH, soil N:P and C:P ratios and total soil C stocks (Delgado-Baquerizo et al 2020). Moreover, a history of soil freezing selects for more frost-tolerant and physiologically adapted microbial communities (Walker et al 2006;Garcia et al 2020), suggesting that soil age might be important too. Accordingly, we used four different soils of varying SOC contents (from 0.39 to 1.04% C) and time after soil restoration (from 4 to 23 years; from now on referred to as 'soil age') and exposed these to three severe FT cycles.…”