Discovery and ecogenomic context of a global Caldiserica-related phylum active in thawing permafrost, Candidatus Cryosericota phylum nov., Ca. Cryosericia class nov., Ca. Cryosericales ord. nov., Ca. Cryosericaceae fam. nov., comprising the four species Cryosericum septentrionale gen. nov. sp. nov., Ca. C. hinesii sp. nov., Ca. C. odellii sp. nov., Ca. C. terrychapinii sp. nov.

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 characterize 7 Caldiserica metagenome-assembled genomes (MAGs) from a thawing permafrost site in Stordalen Mire, Arctic Sweden. By 16S rRNA and marker gene phylogenies, and average nucleotide and amino acid identities, these Stordalen Mire Caldiserica (SMC) MAGs form part of a divergent clade from C. exile. Genome and meta-transcriptome and proteome analyses suggest that unlike Caldisericum, the SMCs (i) are carbohydrate- and possibly amino acid fermenters that can use labile plant compounds and peptides, and (ii) encode adaptations to low temperature. The SMC clade rose to community dominance within permafrost, with a peak metagenome-based relative abundance of ∼60%. It was also physiologically active in the upper seasonally-thawed soil. Beyond Stordalen Mire, analysis of 16S rRNA gene surveys indicated a global distribution of this clade, predominantly in anaerobic, carbon-rich and cold environments. These findings establish the SMCs as four novel phenotypically and ecologically distinct species within a single novel genus, distinct from C. exile clade at the phylum level. The SMCs are thus part of a novel cold-habitat phylum for an understudied, globally-distributed superphylum encompassing the Caldiserica. We propose the names Candidatus Cryosericota phylum nov., Ca. Cryosericia class nov., Ca. Cryosericales ord. nov., Ca. Cryosericaceae fam. nov., Ca. Cryosericum gen. nov., Ca. Cryosericum septentrionale sp. nov., Ca. C. hinesii sp. nov., Ca. C. odellii sp. nov., and Ca. C. terrychapinii sp. nov.

Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments.

T4-like myoviruses are ubiquitous, and their genes are among the most abundant documented in ocean systems. Here we compare 26 T4-like genomes, including 10 from non-cyanobacterial myoviruses, and 16 from marine cyanobacterial myoviruses (cyanophages) isolated on diverse Prochlorococcus or Synechococcus hosts. A core genome of 38 virion construction and DNA replication genes was observed in all 26 genomes, with 32 and 25 additional genes shared among the non-cyanophage and cyanophage subsets, respectively. These hierarchical cores are highly syntenic across the genomes, and sampled to saturation. The 25 cyanophage core genes include six previously described genes with putative functions (psbA, mazG, phoH, hsp20, hli03, cobS), a hypothetical protein with a potential phytanoyl-CoA dioxygenase domain, two virion structural genes, and 16 hypothetical genes. Beyond previously described cyanophage-encoded photosynthesis and phosphate stress genes, we observed core genes that may play a role in nitrogen metabolism during infection through modulation of 2-oxoglutarate. Patterns among non-core genes that may drive niche diversification revealed that phosphorus-related gene content reflects source waters rather than host strain used for isolation, and that carbon metabolism genes appear associated with putative mobile elements. As well, phages isolated on Synechococcus had higher genome-wide %G+C and often contained different gene subsets (e.g. petE, zwf, gnd, prnA, cpeT) than those isolated on Prochlorococcus. However, no clear diagnostic genes emerged to distinguish these phage groups, suggesting blurred boundaries possibly due to cross-infection. Finally, genome-wide comparisons of both diverse and closely related, co-isolated genomes provide a locus-to-locus variability metric that will prove valuable for interpreting metagenomic data sets.