Biotic and Environmental Drivers of Plant Microbiomes Across a Permafrost Thaw Gradient

Abstract

Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partiallyand fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance-and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling

High peatland methane emissions following permafrost thaw: enhanced acetoclastic methanogenesis during early successional stages

“…Using a redundancy analysis (RDA, Figure 6) we found that 27.6% of variation in the methanogenic community was explained by two variables: thaw stage (ANOVA, P < 0.05) and depth from the water table (ANOVA, P < 0.05). This percentage is in accordance with other studies conducted in permafrost impacted regions using similar methods, where the percentage of explained variation falls between 6% (low) to 43% (high) (Comte et al, 2015;Hough et al, 2020). Next, we used variance partitioning to assess the extent to which thaw stage and depth from the water table (i.e.…”

Peatland microbial community responses to plant functional group and drought are depth‐dependent

“…Second, inconsistent with our hypothesis, sedges had a limited effect on microbial communities. Oxygenation and substrates from sedge roots are important shapers of microbially driven processes in sedge‐dominated minerotrophic fens (Chanton et al, 2008; Rupp et al, 2019), and of diverse microbial communities associated with sedge rhizospheres (Hough et al, 2020). The modest sedge effect in PEATcosm might be due to their relatively low biomass in the ombrotrophic habitat we focused on, which became more variable through the course of the experiment (Potvin et al, 2015).…”

Recent Developments in the Study of Plant Microbiomes

“…These shifts in activity are associated with increased activity of ABC transporter genes [ 74 ]. (iv) The extremes of temperature that occur as a consequence of climate change have been demonstrated to affect the phyllosphere and rhizosphere microbiomes of several plants [ 36 ]. (v) Low nitrogen and carbon levels, while not typically thought of as abiotic stresses, (nevertheless they may be considered to be nutrient stress) impact the soil microbiome.…”