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Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling

BACKGROUND: Sediments are massive reservoirs of carbon compounds and host a large fraction of microbial life. Microorganisms within terrestrial aquifer sediments control buried organic carbon turnover, degrade organic contaminants, and impact drinking water quality. Recent 16S rRNA gene profiling in...

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Autores principales: Hug, Laura A, Castelle, Cindy J, Wrighton, Kelly C, Thomas, Brian C, Sharon, Itai, Frischkorn, Kyle R, Williams, Kenneth H, Tringe, Susannah G, Banfield, Jillian F
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971608/
https://www.ncbi.nlm.nih.gov/pubmed/24450983
http://dx.doi.org/10.1186/2049-2618-1-22
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author Hug, Laura A
Castelle, Cindy J
Wrighton, Kelly C
Thomas, Brian C
Sharon, Itai
Frischkorn, Kyle R
Williams, Kenneth H
Tringe, Susannah G
Banfield, Jillian F
author_facet Hug, Laura A
Castelle, Cindy J
Wrighton, Kelly C
Thomas, Brian C
Sharon, Itai
Frischkorn, Kyle R
Williams, Kenneth H
Tringe, Susannah G
Banfield, Jillian F
author_sort Hug, Laura A
collection PubMed
description BACKGROUND: Sediments are massive reservoirs of carbon compounds and host a large fraction of microbial life. Microorganisms within terrestrial aquifer sediments control buried organic carbon turnover, degrade organic contaminants, and impact drinking water quality. Recent 16S rRNA gene profiling indicates that members of the bacterial phylum Chloroflexi are common in sediment. Only the role of the class Dehalococcoidia, which degrade halogenated solvents, is well understood. Genomic sampling is available for only six of the approximate 30 Chloroflexi classes, so little is known about the phylogenetic distribution of reductive dehalogenation or about the broader metabolic characteristics of Chloroflexi in sediment. RESULTS: We used metagenomics to directly evaluate the metabolic potential and diversity of Chloroflexi in aquifer sediments. We sampled genomic sequence from 86 Chloroflexi representing 15 distinct lineages, including members of eight classes previously characterized only by 16S rRNA sequences. Unlike in the Dehalococcoidia, genes for organohalide respiration are rare within the Chloroflexi genomes sampled here. Near-complete genomes were reconstructed for three Chloroflexi. One, a member of an unsequenced lineage in the Anaerolinea, is an aerobe with the potential for respiring diverse carbon compounds. The others represent two genomically unsampled classes sibling to the Dehalococcoidia, and are anaerobes likely involved in sugar and plant-derived-compound degradation to acetate. Both fix CO(2) via the Wood-Ljungdahl pathway, a pathway not previously documented in Chloroflexi. The genomes each encode unique traits apparently acquired from Archaea, including mechanisms of motility and ATP synthesis. CONCLUSIONS: Chloroflexi in the aquifer sediments are abundant and highly diverse. Genomic analyses provide new evolutionary boundaries for obligate organohalide respiration. We expand the potential roles of Chloroflexi in sediment carbon cycling beyond organohalide respiration to include respiration of sugars, fermentation, CO(2) fixation, and acetogenesis with ATP formation by substrate-level phosphorylation.
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spelling pubmed-39716082014-04-02 Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling Hug, Laura A Castelle, Cindy J Wrighton, Kelly C Thomas, Brian C Sharon, Itai Frischkorn, Kyle R Williams, Kenneth H Tringe, Susannah G Banfield, Jillian F Microbiome Research BACKGROUND: Sediments are massive reservoirs of carbon compounds and host a large fraction of microbial life. Microorganisms within terrestrial aquifer sediments control buried organic carbon turnover, degrade organic contaminants, and impact drinking water quality. Recent 16S rRNA gene profiling indicates that members of the bacterial phylum Chloroflexi are common in sediment. Only the role of the class Dehalococcoidia, which degrade halogenated solvents, is well understood. Genomic sampling is available for only six of the approximate 30 Chloroflexi classes, so little is known about the phylogenetic distribution of reductive dehalogenation or about the broader metabolic characteristics of Chloroflexi in sediment. RESULTS: We used metagenomics to directly evaluate the metabolic potential and diversity of Chloroflexi in aquifer sediments. We sampled genomic sequence from 86 Chloroflexi representing 15 distinct lineages, including members of eight classes previously characterized only by 16S rRNA sequences. Unlike in the Dehalococcoidia, genes for organohalide respiration are rare within the Chloroflexi genomes sampled here. Near-complete genomes were reconstructed for three Chloroflexi. One, a member of an unsequenced lineage in the Anaerolinea, is an aerobe with the potential for respiring diverse carbon compounds. The others represent two genomically unsampled classes sibling to the Dehalococcoidia, and are anaerobes likely involved in sugar and plant-derived-compound degradation to acetate. Both fix CO(2) via the Wood-Ljungdahl pathway, a pathway not previously documented in Chloroflexi. The genomes each encode unique traits apparently acquired from Archaea, including mechanisms of motility and ATP synthesis. CONCLUSIONS: Chloroflexi in the aquifer sediments are abundant and highly diverse. Genomic analyses provide new evolutionary boundaries for obligate organohalide respiration. We expand the potential roles of Chloroflexi in sediment carbon cycling beyond organohalide respiration to include respiration of sugars, fermentation, CO(2) fixation, and acetogenesis with ATP formation by substrate-level phosphorylation. BioMed Central 2013-08-05 /pmc/articles/PMC3971608/ /pubmed/24450983 http://dx.doi.org/10.1186/2049-2618-1-22 Text en Copyright © 2013 Hug et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Hug, Laura A
Castelle, Cindy J
Wrighton, Kelly C
Thomas, Brian C
Sharon, Itai
Frischkorn, Kyle R
Williams, Kenneth H
Tringe, Susannah G
Banfield, Jillian F
Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
title Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
title_full Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
title_fullStr Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
title_full_unstemmed Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
title_short Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
title_sort community genomic analyses constrain the distribution of metabolic traits across the chloroflexi phylum and indicate roles in sediment carbon cycling
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971608/
https://www.ncbi.nlm.nih.gov/pubmed/24450983
http://dx.doi.org/10.1186/2049-2618-1-22
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