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Title: Genomic expansion of Domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling

Abstract

Domain Archaea is currently represented by one phylum (Euryarchaeota) and two superphyla (TACK and DPANN). However, gene surveys indicate the existence of a vast diversity of uncultivated archaea for which metabolic information is lacking. We sequenced DNA from complex sediment- and groundwater-associated microbial communities sampled prior to and during an acetate biostimulation field experiment to investigate the diversity and physiology of uncultivated subsurface archaea. We sampled 15 genomes that improve resolution of a new phylum within the TACK superphylum and 119 DPANN genomes that highlight a major subdivision within the archaeal domain that separates DPANN from TACK/Euryarchaeota lineages. Within the DPANN superphylum, which lacks any isolated representatives, we defined two new phyla using sequences from 100 newly sampled genomes. The first new phylum, for which we propose the name Woesearchaeota, was defined using 54 new sequences. We reconstructed a complete (finished) genome for an archaeon from this phylum that is only 0.8 Mb in length and lacks almost all core biosynthetic pathways, but has genes encoding enzymes predicted to interact with bacterial cell walls, consistent with a symbiotic lifestyle. The second new phylum, for which we propose the name Pacearchaeota, was defined based on 46 newly sampled archaeal genomes. Thismore » phylum includes the first non-methanogen with an intermediate Type II/III RuBisCO. We also reconstructed a complete (1.24 Mb) genome for another DPANN archaeon, a member of the Diapherotrites phylum. Metabolic prediction and transcriptomic data indicate that this organism has a fermentation-based lifestyle. In fact, genomic analyses consistently indicate lack of recognizable pathways for sulfur, nitrogen, methane, oxygen, and metal cycling, and suggest that symbiotic and fermentation-based lifestyles are widespread across the DPANN superphylum. Thus, as for a recently identified superphylum of bacteria with small genomes and no cultivated representatives, the biogeochemical impacts of this major radiation of archaea are primarily through anaerobic carbon and hydrogen cycling.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1184900
Report Number(s):
PNNL-SA-104949
44717; KP1704020
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Current Biology, 25(6):690-701
Additional Journal Information:
Journal Name: Current Biology, 25(6):690-701
Country of Publication:
United States
Language:
English
Subject:
Genomic; Domain Archaea; phyla; subsurface; anaerobic; carbon; cycling; Environmental Molecular Sciences Laboratory

Citation Formats

Castelle, Cindy, Wrighton, Kelly C., Thomas, Brian C., Hug, Laura A., Brown, Christopher T., Wilkins, Michael J., Frischkorn, Kyle R., Tringe, Susannah G., Singh, Andrea, Markillie, Lye Meng, Taylor, Ronald C., Williams, Kenneth H., and Banfield, Jillian F. Genomic expansion of Domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. United States: N. p., 2015. Web. doi:10.1016/j.cub.2015.01.014.
Castelle, Cindy, Wrighton, Kelly C., Thomas, Brian C., Hug, Laura A., Brown, Christopher T., Wilkins, Michael J., Frischkorn, Kyle R., Tringe, Susannah G., Singh, Andrea, Markillie, Lye Meng, Taylor, Ronald C., Williams, Kenneth H., & Banfield, Jillian F. Genomic expansion of Domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. United States. doi:10.1016/j.cub.2015.01.014.
Castelle, Cindy, Wrighton, Kelly C., Thomas, Brian C., Hug, Laura A., Brown, Christopher T., Wilkins, Michael J., Frischkorn, Kyle R., Tringe, Susannah G., Singh, Andrea, Markillie, Lye Meng, Taylor, Ronald C., Williams, Kenneth H., and Banfield, Jillian F. Sun . "Genomic expansion of Domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling". United States. doi:10.1016/j.cub.2015.01.014.
@article{osti_1184900,
title = {Genomic expansion of Domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling},
author = {Castelle, Cindy and Wrighton, Kelly C. and Thomas, Brian C. and Hug, Laura A. and Brown, Christopher T. and Wilkins, Michael J. and Frischkorn, Kyle R. and Tringe, Susannah G. and Singh, Andrea and Markillie, Lye Meng and Taylor, Ronald C. and Williams, Kenneth H. and Banfield, Jillian F.},
abstractNote = {Domain Archaea is currently represented by one phylum (Euryarchaeota) and two superphyla (TACK and DPANN). However, gene surveys indicate the existence of a vast diversity of uncultivated archaea for which metabolic information is lacking. We sequenced DNA from complex sediment- and groundwater-associated microbial communities sampled prior to and during an acetate biostimulation field experiment to investigate the diversity and physiology of uncultivated subsurface archaea. We sampled 15 genomes that improve resolution of a new phylum within the TACK superphylum and 119 DPANN genomes that highlight a major subdivision within the archaeal domain that separates DPANN from TACK/Euryarchaeota lineages. Within the DPANN superphylum, which lacks any isolated representatives, we defined two new phyla using sequences from 100 newly sampled genomes. The first new phylum, for which we propose the name Woesearchaeota, was defined using 54 new sequences. We reconstructed a complete (finished) genome for an archaeon from this phylum that is only 0.8 Mb in length and lacks almost all core biosynthetic pathways, but has genes encoding enzymes predicted to interact with bacterial cell walls, consistent with a symbiotic lifestyle. The second new phylum, for which we propose the name Pacearchaeota, was defined based on 46 newly sampled archaeal genomes. This phylum includes the first non-methanogen with an intermediate Type II/III RuBisCO. We also reconstructed a complete (1.24 Mb) genome for another DPANN archaeon, a member of the Diapherotrites phylum. Metabolic prediction and transcriptomic data indicate that this organism has a fermentation-based lifestyle. In fact, genomic analyses consistently indicate lack of recognizable pathways for sulfur, nitrogen, methane, oxygen, and metal cycling, and suggest that symbiotic and fermentation-based lifestyles are widespread across the DPANN superphylum. Thus, as for a recently identified superphylum of bacteria with small genomes and no cultivated representatives, the biogeochemical impacts of this major radiation of archaea are primarily through anaerobic carbon and hydrogen cycling.},
doi = {10.1016/j.cub.2015.01.014},
journal = {Current Biology, 25(6):690-701},
number = ,
volume = ,
place = {United States},
year = {2015},
month = {3}
}