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 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.
| Original language | English |
|---|---|
| Journal | Systematic and Applied Microbiology |
| Volume | 42 |
| Issue number | 1 |
| Pages (from-to) | 54-66 |
| Number of pages | 13 |
| ISSN | 0723-2020 |
| DOIs | |
| Publication status | Published - Jan 2019 |
| Externally published | Yes |
Bibliographical note
Funding Information:This study was funded by the Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research, grants DE-SC0004632, DE-SC0010580, and DE-SC0016440. A portion of the research was performed under the Facilities Integrating Collaborations for User Science (FICUS) initiative, with resources at both the DOE Joint Genome Institute (JGI) and the Environmental Molecular Sciences Laboratory (EMSL), under EMSL Proposal ID 49521. A portion was additionally performed through an EMSL Science Theme Award, Proposal ID 48467. JGI and EMSL are DOE Office of Science User Facilities, sponsored by the Office of Biological and Environmental Research and operated under Contract Nos. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). A portion of the computational support was provided by an award from the Ohio Supercomputer Center (OSC; www.osc.edu) to Matthew B. Sullivan. We thank the IsoGenie1 and IsoGenie2 Project Teams for scientific discussions about these results, and the 2010–2012 field teams for sample collection, particularly Tyler Logan, as well as the Abisko Scientific Research Station for sampling infrastructure and support. We thank Eun-Hae Kim and Robert Jones for DNA extraction of the palsa collapse feature samples, Sarah Owens at Argonne National Labs for assistance with amplicon sequencing, and Margretta Murphy for early assistance with the amplicon data. We gratefully acknowledge the reviews of Dr. Ramon Rossello-Mora and two anonymous reviewers, whose thorough and thoughtful feedback improved the manuscript.
Funding Information:
This study was funded by the Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research, grants DE-SC0004632, DE-SC0010580, and DE-SC0016440. A portion of the research was performed under the Facilities Integrating Collaborations for User Science (FICUS) initiative, with resources at both the DOE Joint Genome Institute (JGI) and the Environmental Molecular Sciences Laboratory (EMSL), under EMSL Proposal ID 49521. A portion was additionally performed through an EMSL Science Theme Award, Proposal ID 48467. JGI and EMSL are DOE Office of Science User Facilities, sponsored by the Office of Biological and Environmental Research and operated under Contract Nos. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). A portion of the computational support was provided by an award from the Ohio Supercomputer Center (OSC; www.osc.edu ) to Matthew B. Sullivan. We thank the IsoGenie1 and IsoGenie2 Project Teams for scientific discussions about these results, and the 2010–2012 field teams for sample collection, particularly Tyler Logan, as well as the Abisko Scientific Research Station for sampling infrastructure and support. We thank Eun-Hae Kim and Robert Jones for DNA extraction of the palsa collapse feature samples, Sarah Owens at Argonne National Labs for assistance with amplicon sequencing, and Margretta Murphy for early assistance with the amplicon data. We gratefully acknowledge the reviews of Dr. Ramon Rossello-Mora and two anonymous reviewers, whose thorough and thoughtful feedback improved the manuscript.
Publisher Copyright:
© 2018 The Authors
Keywords
- Ca. Cryosericota
- Ca. Cryosericum
- Caldiserica
- Metagenome-assembled genome
- Permafrost
- Stordalen Mire