Genome analysis reveals diverse novel psychrotolerant Mucilaginibacter species in Arctic tundra soils

Abstract

As Arctic soil ecosystems warm due to climate change, enhanced microbial activity is projected to increase the rate of soil organic matter degradation. Delineating the diversity and activity of Arctic tundra microbial communities active in decomposition is thus of keen interest. Here, we describe novel cold-adapted bacteria in the genus Mucilaginibacter (Bacteroidota) isolated from Artic tundra soils in Finland. These isolates are aerobic chemoorganotrophs and appear well adapted to the low-temperature environment, where they are also exposed to desiccation and a wide regime of annual temperature variation. Initial 16S ribosomal RNA (rRNA)-based phylogenetic analysis suggested that five isolated strains represent new species of the genus Mucilaginibacter, confirmed by whole genome-based phylogenomic and average nucleotide identity. Five novel species are described: Mucilaginibacter geliditolerans sp. nov., Mucilaginibacter tundrae sp. nov., Mucilaginibacter empetricola sp. nov., Mucilaginibacter saanensis sp. nov., and Mucilaginibacter cryoferens sp. nov. Genome and phenotype analysis showed their potential in complex carbon degradation, nitrogen assimilation, polyphenol degradation, and adaptation to their tundra heath habitat. A pangenome analysis of the newly identified species alongside known members of the Mucilaginibacter genus sourced from various environments revealed the distinctive characteristics of the tundra strains. These strains possess unique genes related to energy production, nitrogen uptake, adaptation, and the synthesis of secondary metabolites that aid in their growth, potentially accounting for their prevalence in tundra soil. By uncovering novel species and strains within the Mucilaginibacter, we enhance our understanding of this genus and elucidate how environmental fluctuations shape the microbial functionality and interactions in Arctic tundra ecosystems.

Keywords: Mucilaginibacter; cold-adapted; novel species; tundra soil isolates.

Graphical Abstract

Figure 1

Phylogenomics tree of eight tundra soil isolates and other members of the Mucilaginibacter genus. The tree was prepared with the UBCG v3 tool employing RAxML. The value at the branch point represents the gene support index (GSI, indicating the number of genes out of 92 conserved genes supporting the branch point) and the bootstrap value, respectively. 1000 bootstrap replications were used for phylogenomics tree preparation. Sphingobacterium spiritivorum FDAARGOS_1144 and Pedobacter heparinus DSM 2366 were used as outgroups.

Figure 2

Carbohydrate degradation ability of the members of the genus Mucilaginibacter predicted by the CAZy database. The Mucilaginibacter strains were able to utilise cellulose, xylose, arabinose, and mixed glycans. The carbohydrate degradation ability is present in all the Mucilaginibacter strains irrespective of the isolation source.

Figure 3

Polyphenol degradation enzymes (A), antiphage defence systems (B), and secondary metabolite synthesis (C) gene clusters present in Mucilaginibacter strains. The novel Mucilaginibacter strains show the presence of genes related to polyphenol degradation. Antiphage-related genes were also found in the novel strains, implying the presence of phages in the tundra ecosystem. Additionally, novel tundra isolates contain secondary metabolite gene clusters having antimicrobial properties.

Figure 4

Pangenome analysis of tundra Mucilaginibacter strains with other members of the genus isolated from diverse habitats. The heatmap represents the ANI between the strains. The analysis shows that the tundra isolates are separated into two groups based on gene cluster presence and absence. This implies that tundra strains are different from strains isolated from other habitats.

Figure 5

Relative abundance of detected Mucilaginibacter species in soils of windswept and snow-accumulating tundra heath plots of Mt. Pikku-Malla. rRNA operon reads from the Bacteroidota represented ~1.7% and Mucilaginibacter spp. ~0.25%–0.32% of the total bacterial reads. Data present the combined reads of four replicate soil samples, each from the windswept and snow-accumulating plots.