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Title: 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.

Abstract

Here, 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,more » 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.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [4];  [2];  [2];  [4];  [5];  [6];  [7];  [8];  [8];  [9];  [4];  [8];  [2];  [10]
  1. The Ohio State Univ., Columbus, OH (United States); Ensenada Center for Scientific Research and Higher Education, CICESE, Ensenada (Mexico)
  2. Univ. of Queensland (Australia)
  3. The Ohio State Univ., Columbus, OH (United States); Univ. of Southern California, Los Angeles, CA (United States)
  4. The Ohio State Univ., Columbus, OH (United States)
  5. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  6. Ronin Institute, Montclair, NJ (United States)
  7. The Ohio State Univ., Columbus, OH (United States); Florida State Univ., Tallahassee, FL (United States)
  8. Univ. of Arizona, Tucson, AZ (United States)
  9. Univ. of Exeter, Exeter (United Kingdom)
  10. The Ohio State Univ., Columbus, OH (United States); Univ. of Arizona, Tucson, AZ (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1491258
Report Number(s):
PNNL-SA-135223
Journal ID: ISSN 0723-2020; PII: S072320201830184X
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Systematic and Applied Microbiology
Additional Journal Information:
Journal Volume: 42; Journal Issue: 1; Journal ID: ISSN 0723-2020
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Metagenome-assembled genome; Caldiserica; Ca. Cryosericota; Ca. Cryosericum; Permafrost; Stordalen Mire

Citation Formats

Martinez, Miguel A., Woodcroft, Ben J., Ignacio Espinoza, Julio C., Zayed, Ahmed A., Singleton, Caitlin M., Boyd, Joel A., Li, Yueh -Fen, Purvine, Samuel, Maughan, Heather, Hodgkins, Suzanne B., Anderson, Darya, Sederholm, Maya, Temperton, Ben, Bolduc, Benjamin, Saleska, Scott R., Tyson, Gene W., and Rich, Virginia I. 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.. United States: N. p., 2018. Web. doi:10.1016/J.SYAPM.2018.12.003.
Martinez, Miguel A., Woodcroft, Ben J., Ignacio Espinoza, Julio C., Zayed, Ahmed A., Singleton, Caitlin M., Boyd, Joel A., Li, Yueh -Fen, Purvine, Samuel, Maughan, Heather, Hodgkins, Suzanne B., Anderson, Darya, Sederholm, Maya, Temperton, Ben, Bolduc, Benjamin, Saleska, Scott R., Tyson, Gene W., & Rich, Virginia I. 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.. United States. doi:10.1016/J.SYAPM.2018.12.003.
Martinez, Miguel A., Woodcroft, Ben J., Ignacio Espinoza, Julio C., Zayed, Ahmed A., Singleton, Caitlin M., Boyd, Joel A., Li, Yueh -Fen, Purvine, Samuel, Maughan, Heather, Hodgkins, Suzanne B., Anderson, Darya, Sederholm, Maya, Temperton, Ben, Bolduc, Benjamin, Saleska, Scott R., Tyson, Gene W., and Rich, Virginia I. Fri . "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.". United States. doi:10.1016/J.SYAPM.2018.12.003. https://www.osti.gov/servlets/purl/1491258.
@article{osti_1491258,
title = {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.},
author = {Martinez, Miguel A. and Woodcroft, Ben J. and Ignacio Espinoza, Julio C. and Zayed, Ahmed A. and Singleton, Caitlin M. and Boyd, Joel A. and Li, Yueh -Fen and Purvine, Samuel and Maughan, Heather and Hodgkins, Suzanne B. and Anderson, Darya and Sederholm, Maya and Temperton, Ben and Bolduc, Benjamin and Saleska, Scott R. and Tyson, Gene W. and Rich, Virginia I.},
abstractNote = {Here, 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.},
doi = {10.1016/J.SYAPM.2018.12.003},
journal = {Systematic and Applied Microbiology},
number = 1,
volume = 42,
place = {United States},
year = {2018},
month = {12}
}

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Figures / Tables:

Fig. 1. Fig. 1.: Ecogenomic context of SMC MAGs. (A) Maximum likelihood phylogenetic tree containing Caldiserica sequences from other 16S rRNA environmental surveys (blue text), and those from genomes (red text; isolate, single cell or metagenome-assembled genomes; the latter, bolded, is SMC1 from this survey). Overall Caldiserica topology was re-rooted to matchmore » that presented in Rinke et al. [61]. Current unofficial family-level designations from the SILVA database [57] are indicated to the right. Bootstrap values are shown for nodes with >50% support (100 replicates; black circles = >95, gray = >75, and white = >50). 16S rRNA gene amplicon sequences from this study were then aligned and inserted in this reference tree, and placement of their phylogenetic groups is denoted by dashed lines. The habitat distributions (brown for the palsa rim of the collapse feature, purple for the adjacent hole) of the amplicon phylogenetic groups are shown by the inset pie charts, with the normalized number of sequences and 97% OTUs comprising each phylogenetic group indicated adjacent. To the right of the tree are markers characterizing the origin habitat of the reference tree sequences; columns describe basic habitat types, circle colors denote temperature (orange = thermic, >40 °C; green = mesic, 10–40 °C; blue = cryic, <10 °C; white = N/A), and black triangles indicate hydrocarbon-associated habitats. (B) Pairwise 16S rRNA gene identities (y-axis) within and between each unofficial family in (A). Intra-clade identity bars are colored according to the arbitrary family colors used« less

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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.