Shotgun metagenomics reveals distinct functional diversity and metabolic capabilities between 12 000-year-old permafrost and active layers on Muot da Barba Peider (Swiss Alps)

Abstract

The warming-induced thawing of permafrost promotes microbial activity, often resulting in enhanced greenhouse gas emissions. The ability of permafrost microorganisms to survive the in situ sub-zero temperatures, their energetic strategies and their metabolic versatility in using soil organic materials determine their growth and functionality upon thawing. Hence, functional characterization of the permafrost microbiome, particularly in the underexplored mid-latitudinal alpine regions, is a crucial first step in predicting its responses to the changing climate, and the consequences for soil–climate feedbacks. In this study, for the first time, the functional potential and metabolic capabilities of a temperate mountain permafrost microbiome from central Europe has been analysed using shotgun metagenomics. Permafrost and active layers from the summit of Muot da Barba Peider (MBP) [Swiss Alps, 2979 m above sea level (a.s.l.)] revealed a strikingly high functional diversity in the permafrost (north-facing soils at a depth of 160 cm). Permafrost metagenomes were enriched in stress-response genes (e.g. cold-shock genes, chaperones), as well as in genes involved in cell defence and competition (e.g. antiviral proteins, antibiotics, motility, nutrient-uptake ABC transporters), compared with active-layer metagenomes. Permafrost also showed a higher potential for the synthesis of carbohydrate-active enzymes, and an overrepresentation of genes involved in fermentation, carbon fixation, denitrification and nitrogen reduction reactions. Collectively, these findings demonstrate the potential capabilities of permafrost microorganisms to thrive in cold and oligotrophic conditions, and highlight their metabolic versatility in carbon and nitrogen cycling. Our study provides a first insight into the high functional gene diversity of the central European mountain permafrost microbiome. Our findings extend our understanding of the microbial ecology of permafrost and represent a baseline for future investigations comparing the functional profiles of permafrost microbial communities at different latitudes.

Shotgun Metagenomics of Deep Forest Soil Layers Show Evidence of Altered Microbial Genetic Potential for Biogeochemical Cycling

“…Among the most overrepresented genes of the carbohydrate and amino acid transport and metabolism categories were ABC-type amino acid transporters, peptidases, synthetases, transferases, kinases, hydrolases, dehydrogenases, lyases, and mannosidases. Such a dominance of overrepresented functional gene categories is surprising but not unusual, as Perez-Mon et al (2021) found a similar pattern when comparing permafrost soils with active-layer soils in a high mountain soil in the Swiss Alps. Likewise, in a comparison of cultivated and uncultivated chernozems in Russia, the majority of the functional gene categories were overrepresented in the virgin soil ( Gorbacheva et al, 2018 ).…”

“…Pre-processing of metagenomic reads, assembly of reads into contigs, contig binning, and functional and phylogenetic annotation of contigs and bins were achieved using a customized pipeline ( Donhauser et al, 2021 ; Perez-Mon et al, 2021 ). Briefly, raw reads were quality checked using FastQC v.0.11.9 1 .…”

RiboTaxa: combined approaches for rRNA genes taxonomic resolution down to the species level from metagenomics data revealing novelties

“…We also applied RiboTaxa on metagenomics data produced from underexplored permafrost mid-latitudinal alpine regions ( 52 ). Our results demonstrated that the richness was highest for the N160 (permafrost) soils ( Supplementary Figure S7 ) with 97 detected species (Figure 9C ) confirming the observed highest alpha diversity of the predicted protein-coding genes in N160 soils.…”

The structure and function of the rhizosphere microbial communities of Carex praeclara and Leymus secalinus in a Zoige alpine grassland

“…Samples of C and L contained a higher abundance of CAZy genes than the N samples (Figure S4b). These genes encode multiple glycosyl hydrolases (GHs), polysaccharide hydrolases and auxiliary enzymes that together participate in the depolymerization and utilization of recalcitrant compounds derived from plants and exudations from the roots, such as cellulose, lignin, starch and other polysaccharides (Perez-Mon et al ., 2021). These findings indicated that microorganisms can obtain and use multiple carbon sources in the rhizosphere.…”