Habitat‐adapted microbial communities mediate Sphagnum peatmoss resilience to warming

Abstract

Summary Sphagnum peatmosses are fundamental members of peatland ecosystems, where they contribute to the uptake and long‐term storage of atmospheric carbon. Warming threatens Sphagnum mosses and is known to alter the composition of their associated microbiome. Here, we use a microbiome transfer approach to test if microbiome thermal origin influences host plant thermotolerance. We leveraged an experimental whole‐ecosystem warming study to collect field‐grown Sphagnum, mechanically separate the associated microbiome and then transfer onto germ‐free laboratory Sphagnum for temperature experiments. Host and microbiome dynamics were assessed with growth analysis, Chla fluorescence imaging, metagenomics, metatranscriptomics and 16S rDNA profiling. Microbiomes originating from warming field conditions imparted enhanced thermotolerance and growth recovery at elevated temperatures. Metagenome and metatranscriptome analyses revealed that warming altered microbial community structure in a manner that induced the plant heat shock response, especially the HSP70 family and jasmonic acid production. The heat shock response was induced even without warming treatment in the laboratory, suggesting that the warm‐microbiome isolated from the field provided the host plant with thermal preconditioning. Our results demonstrate that microbes, which respond rapidly to temperature alterations, can play key roles in host plant growth response to rapidly changing environments.

Impact of global change on the plant microbiome

“…2126–2139). Particularly, the observation that habitat‐adapted microbial communities can transmit thermotolerance to Sphagnum peatmoss and can promote resilience to warming demonstrates that rapid adaptation to stress in the host can occur via the microbiota (Carrell et al ., 2022). Taken together, the results suggest that microbial commensals and symbionts might represent key components promoting host survival and rapid adaptation to environmental perturbations.…”

“…Different strategies have been discussed here, including: (1) iterative root microbiome selection to alleviate salt stress (King et al, 2022(King et al, , in this issue pp. 2101(King et al, -2110; (2) use of habitat-adapted microbiomes to promote host tolerance to warming (Carrell et al, 2022(Carrell et al, , in this issue pp. 2111(Carrell et al, -2125; and (3) utilization of microbes from extreme desert environments (Maldonado et al, 2022(Maldonado et al, , in this issue pp.…”

Viral infections mediate microbial controls on ecosystem responses to global warming

“…1, Box 1). Microbes play diverse functional roles in peatlands (Gilbert et al 1998;Gilbert and Mitchell 2006;Lara et al 2011;Kostka et al 2016;Carrell et al 2022a) (Fig. 3).…”

“…For example, bacterial and fungal decomposers are primarily responsible for breaking down dead organic material stored within peatlands (Gilbert et al 1998;Gilbert and Mitchell 2006), a process being accelerated by warming (Dorrepaal et al 2009). Additionally, Sphagnum's ability to persist in harsh peatland habitats with extremely low mineral nitrogen availability depends on symbiotic interactions with microbial associates (Lindo, Nilsson and Gundale 2013;Kostka et al 2016;Carrell et al 2022a)-including diazotrophs that colonize the cell surface and water-filled hyaline cells in host plants (Kostka et al 2016) (Fig. 3).…”

Keystone Taxa and Predictive Functional Analysis of Sphagnum palustre Tank Microbiomes in Erxianyan Peatland, Central China

“…Within those Sphagnum- associated bacterial communities, some functional groups have begun to be revealed in N 2 fixation, disease suppression, promote growth [ 6 , 7 , 8 ] of Sphagnum mosses and elemental cycling [ 9 , 10 ] in peatland ecosystems. In addition, the Sphagnum microbial biomass and microbial community are impacted by elevated temperatures and respond rapidly to temperature alterations [ 8 , 11 , 12 ]. Generally, Sphagnum -associated microbiomes differ from those of common plants due to the inhospitable acidic environments.…”