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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

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 thismore » 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.« less

Authors:
; ; ; ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1501836
Report Number(s):
PNNL-SA-135223
Journal ID: ISSN 0723-2020
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
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:
metagenome-assembled genome, Caldiserica, Ca. Cryosericales, 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., Rich, Virginia I., 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., 2019. 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., 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., Rich, Virginia I., Saleska, Scott R., Tyson, Gene W., and Rich, Virginia I. Tue . "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.
@article{osti_1501836,
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. and Saleska, Scott R. and Tyson, Gene W. and Rich, Virginia I.},
abstractNote = {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.},
doi = {10.1016/j.syapm.2018.12.003},
journal = {Systematic and Applied Microbiology},
issn = {0723-2020},
number = 1,
volume = 42,
place = {United States},
year = {2019},
month = {1}
}