PNNL

Abstract

The phylum Caldiserica was identified from the hot spring 16S rRNA gene lineage ‘OP5’ and named for the sole isolate Caldisericum exile, a hot spring sulfur-reducing chemoheterotroph. Here we roughly double the genomic representation of the phylum with 7 Caldiserica metagenome-assembled genomes (MAGs) from a thawing permafrost site in the Stordalen Mire peatland of Arctic Sweden. By 16S rRNA and marker gene phylogenies, and average nucleotide and amino acid identities, these MAGs represent four species withina single novel genus (Candidatus Cryosericum), within a novel family (Ca. Cryosericaceae) and order (Ca. Cryosericales). Genome and metatranscriptome and -proteome analyses suggest that unlike Caldisericum, Ca. Cryosericum (i) is a carbohydrate- and possibly amino acid fermenter that can use labile plant compounds and peptides, generating acetate, carbon dioxideand hydrogen (which have the potential to fuel methanogenesis in these important methanogenic habitats), and (ii) has likely adaptations to low temperature including osmoprotection, detoxification mechanisms and DNA repair systems. Ca. Cryosericum was highly abundant (up to 70%) within the permafrost layer, and abundant through the deeper, thawed fens, where it was also physiologically active based on metatranscriptome and metaproteome analyses. Beyond Stordalen Mire, analysis of 16S rRNA gene sequence surveys indicated a global distribution of this order predominantly in anaerobic, carbon rich and cold environments like permafrost and aquifers, and absent from terrestrial hot springs and hydrothermal vents where Caldisericum dominates. Together these findings help establish an novel, ecologically-relevant cold-habitat order for an understudied, globally-distributed phylum previously best characterized by its thermophilic isolate.