Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota

St. John, Emily; Flores, Gilberto E.; Meneghin, Jennifer; Reysenbach, Anna‐Louise

doi:10.1111/1758-2229.12740

Title: Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota

Abstract

Summary Ectosymbiotic Nanoarchaeota live on the surface of diverse archaeal hosts. Despite being broadly distributed in global geothermal systems, only three Nanoarchaeota have been successfully co‐cultivated with their hosts, and until now no nanoarchaeotal cultures or genomes have been described from deep‐sea hydrothermal vents. We recovered three nanoarchaeotal metagenome‐assembled genomes (MAGs) from deep‐sea hydrothermal vent sites at the Eastern Lau Spreading Center (M10‐121), Guaymas Basin (Gua‐46) and the Mid‐Cayman Rise (MC‐1). Based on average amino acid identity analysis, M10‐121 is a novel species in the candidate genus Nanoclepta, while the other two MAGs represent novel genera in the Nanoarchaeota . Like previously sequenced Nanoarchaeota, each MAG encodes at least one split protein‐coding gene. The MAGs also contain a mosaic of key nanoarchaeotal features, including CRISPR repeat regions and marker genes for gluconeogenesis and archaeal flagella. MC‐1 also encodes the pentose bisphosphate pathway, which may allow the nanoarchaeote to bypass several steps in glycolysis and produce ATP.

Authors:

St. John, Emily ^[1]; Flores, Gilberto E. ^[2]; Meneghin, Jennifer ^[1];

^[1]

Department of Biology Portland State University Portland OR 97201 USA
Department of Biology California State University Northridge CA 91330 USA

Publication Date:: Mon Mar 18 00:00:00 EDT 2019

Sponsoring Org.:: USDOE

OSTI Identifier:: 1501747

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: Environmental Microbiology Reports

Additional Journal Information:: Journal Name: Environmental Microbiology Reports Journal Volume: 11 Journal Issue: 2; Journal ID: ISSN 1758-2229

Publisher:: Wiley-Blackwell

Country of Publication:: United States

Language:: English

Citation Formats


                    St. John, Emily, Flores, Gilberto E., Meneghin, Jennifer, and Reysenbach, Anna‐Louise. Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota.  United States: N. p., 2019. 
Web.  doi:10.1111/1758-2229.12740.

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                    St. John, Emily, Flores, Gilberto E., Meneghin, Jennifer, & Reysenbach, Anna‐Louise. Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota.  United States.  https://doi.org/10.1111/1758-2229.12740

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                    St. John, Emily, Flores, Gilberto E., Meneghin, Jennifer, and Reysenbach, Anna‐Louise. Mon .  
"Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota".  United States.  https://doi.org/10.1111/1758-2229.12740.

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@article{osti_1501747,

  title        = {Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota},

  author       = {St. John, Emily and Flores, Gilberto E. and Meneghin, Jennifer and Reysenbach, Anna‐Louise},

  abstractNote = {Summary Ectosymbiotic Nanoarchaeota live on the surface of diverse archaeal hosts. Despite being broadly distributed in global geothermal systems, only three Nanoarchaeota have been successfully co‐cultivated with their hosts, and until now no nanoarchaeotal cultures or genomes have been described from deep‐sea hydrothermal vents. We recovered three nanoarchaeotal metagenome‐assembled genomes (MAGs) from deep‐sea hydrothermal vent sites at the Eastern Lau Spreading Center (M10‐121), Guaymas Basin (Gua‐46) and the Mid‐Cayman Rise (MC‐1). Based on average amino acid identity analysis, M10‐121 is a novel species in the candidate genus Nanoclepta, while the other two MAGs represent novel genera in the Nanoarchaeota . Like previously sequenced Nanoarchaeota, each MAG encodes at least one split protein‐coding gene. The MAGs also contain a mosaic of key nanoarchaeotal features, including CRISPR repeat regions and marker genes for gluconeogenesis and archaeal flagella. MC‐1 also encodes the pentose bisphosphate pathway, which may allow the nanoarchaeote to bypass several steps in glycolysis and produce ATP.},

  doi          = {10.1111/1758-2229.12740},

  journal      = {Environmental Microbiology Reports},

  number       = 2,

  volume       = 11,

  place        = {United States},

  year         = {Mon Mar 18 00:00:00 EDT 2019},

  month        = {Mon Mar 18 00:00:00 EDT 2019}

}

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Title: Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota

Abstract

Citation Formats

Uncultivated microbes in need of their own taxonomy journal, July 2017

Life without RNase P journal, May 2008

An updated evolutionary classification of CRISPR–Cas systems journal, September 2015

Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments journal, June 2008

Anvi’o: an advanced analysis and visualization platform for ‘omics data journal, January 2015

RNase P: interface of the RNA and protein worlds journal, June 2006

Enzymatic Characterization of AMP Phosphorylase and Ribose-1,5-Bisphosphate Isomerase Functioning in an Archaeal AMP Metabolic Pathway journal, October 2012

Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin: Microbial communities of hydrothermal deposits journal, March 2012

Purification and characterization of two reversible and ADP-dependent acetyl coenzyme A synthetases from the hyperthermophilic archaeon Pyrococcus furiosus. journal, October 1996

Extreme genome reduction in symbiotic bacteria journal, November 2011

Transfer RNA genes in pieces journal, June 2008

Linking pangenomes and metagenomes: the Prochlorococcus metapangenome journal, January 2018

Genetic Diversity of Archaea in Deep-Sea Hydrothermal Vent Environments journal, August 1999

The archaellum: how archaea swim journal, January 2015

High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality journal, August 2005

Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment journal, July 2016

Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5′- and 3′-halves journal, February 2005

Multi-omics analysis provides insight to the Ignicoccus hospitalis-Nanoarchaeum equitans association journal, September 2017

Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge: Microbial communities of hydrothermal vent deposits journal, March 2011

The phosphofructokinase-B (MJ0406) from Methanocaldococcus jannaschii represents a nucleoside kinase with a broad substrate specificity journal, October 2006

Microbial life in Bourlyashchy, the hottest thermal pool of Uzon Caldera, Kamchatka journal, September 2015

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A pentose bisphosphate pathway for nucleoside degradation in Archaea journal, March 2015

Yellowstone Lake Nanoarchaeota journal, January 2013

The cytochrome bd respiratory oxygen reductases journal, November 2011

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The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism journal, October 2003

Structural Basis for a Unique ATP Synthase Core Complex from Nanoarcheaum equitans journal, September 2015

Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden-Meyerhof pathway in Thermococcus kodakarensis journal, August 2006

Colonization of nascent, deep-sea hydrothermal vents by a novel Archaeal and Nanoarchaeal assemblage journal, January 2006

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal, May 2015

Reductive genome evolution in Buchnera aphidicola journal, January 2003

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations journal, September 2018

Detection of 16S rDNA Sequences Representing the Novel Phylum “Nanoarchaeota”: Indication for a Wide Distribution in High Temperature Biotopes journal, January 2002

A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont journal, May 2002

Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park journal, April 2013

Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents journal, October 2017

Uncultivated microbes in need of their own taxonomy
journal, July 2017

Life without RNase P
journal, May 2008

An updated evolutionary classification of CRISPR–Cas systems
journal, September 2015

Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments
journal, June 2008

Anvi’o: an advanced analysis and visualization platform for ‘omics data
journal, January 2015

RNase P: interface of the RNA and protein worlds
journal, June 2006

Enzymatic Characterization of AMP Phosphorylase and Ribose-1,5-Bisphosphate Isomerase Functioning in an Archaeal AMP Metabolic Pathway
journal, October 2012

Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin: Microbial communities of hydrothermal deposits
journal, March 2012

Purification and characterization of two reversible and ADP-dependent acetyl coenzyme A synthetases from the hyperthermophilic archaeon Pyrococcus furiosus.
journal, October 1996

Extreme genome reduction in symbiotic bacteria
journal, November 2011

Transfer RNA genes in pieces
journal, June 2008

Linking pangenomes and metagenomes: the Prochlorococcus metapangenome
journal, January 2018

Genetic Diversity of Archaea in Deep-Sea Hydrothermal Vent Environments
journal, August 1999

The archaellum: how archaea swim
journal, January 2015

High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality
journal, August 2005

Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment
journal, July 2016

Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5′- and 3′-halves
journal, February 2005

Multi-omics analysis provides insight to the Ignicoccus hospitalis-Nanoarchaeum equitans association
journal, September 2017

Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge: Microbial communities of hydrothermal vent deposits
journal, March 2011

The phosphofructokinase-B (MJ0406) from Methanocaldococcus jannaschii represents a nucleoside kinase with a broad substrate specificity
journal, October 2006

Microbial life in Bourlyashchy, the hottest thermal pool of Uzon Caldera, Kamchatka
journal, September 2015

Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis
journal, September 2018

A new symbiotic nanoarchaeote (Candidatus Nanoclepta minutus) and its host (Zestosphaera tikiterensis gen. nov., sp. nov.) from a New Zealand hot spring
journal, January 2019

A pentose bisphosphate pathway for nucleoside degradation in Archaea
journal, March 2015

Yellowstone Lake Nanoarchaeota
journal, January 2013

The cytochrome bd respiratory oxygen reductases
journal, November 2011

Nanoarchaeota, Their Sulfolobales Host, and Nanoarchaeota Virus Distribution across Yellowstone National Park Hot Springs
journal, September 2015

The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism
journal, October 2003

Structural Basis for a Unique ATP Synthase Core Complex from Nanoarcheaum equitans
journal, September 2015

Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden-Meyerhof pathway in Thermococcus kodakarensis
journal, August 2006

Colonization of nascent, deep-sea hydrothermal vents by a novel Archaeal and Nanoarchaeal assemblage
journal, January 2006

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

Reductive genome evolution in Buchnera aphidicola
journal, January 2003

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
journal, September 2018

Detection of 16S rDNA Sequences Representing the Novel Phylum “Nanoarchaeota”: Indication for a Wide Distribution in High Temperature Biotopes
journal, January 2002

A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
journal, May 2002

Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park
journal, April 2013

Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents
journal, October 2017