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

Abstract

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 inmore » sugar and plant-derived-compound degradation to acetate. Both fix CO2 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, CO2 fixation, and acetogenesis with ATP formation by substrate-level phosphorylation.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [1]
  1. Univ. of California, Berkeley, CA (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1511367
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Microbiome
Additional Journal Information:
Journal Volume: 1; Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Hug, Laura A., Castelle, Cindy J., Wrighton, Kelly C., Thomas, Brian C., Sharon, Itai, Frischkorn, Kyle R., Williams, Kenneth H., Tringe, Susannah G., and Banfield, Jillian F. Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. United States: N. p., 2013. Web. doi:10.1186/2049-2618-1-22.
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. United States. doi:10.1186/2049-2618-1-22.
Hug, Laura A., Castelle, Cindy J., Wrighton, Kelly C., Thomas, Brian C., Sharon, Itai, Frischkorn, Kyle R., Williams, Kenneth H., Tringe, Susannah G., and Banfield, Jillian F. Mon . "Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling". United States. doi:10.1186/2049-2618-1-22. https://www.osti.gov/servlets/purl/1511367.
@article{osti_1511367,
title = {Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling},
author = {Hug, Laura A. and Castelle, Cindy J. and Wrighton, Kelly C. and Thomas, Brian C. and Sharon, Itai and Frischkorn, Kyle R. and Williams, Kenneth H. and Tringe, Susannah G. and Banfield, Jillian F.},
abstractNote = {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 CO2 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, CO2 fixation, and acetogenesis with ATP formation by substrate-level phosphorylation.},
doi = {10.1186/2049-2618-1-22},
journal = {Microbiome},
number = 1,
volume = 1,
place = {United States},
year = {2013},
month = {8}
}

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Figures / Tables:

Figure 1 Figure 1: Rank abundance curve of the 161 most abundant organisms from the 5 m metagenome assembly for which at least eight of the 16 selected ribosomal proteins were recovered. Bars correspond to summed abundances for major taxonomic divisions (domains and phyla), with individual organism abundances denoted by stacked boxes.more » Taxonomic affiliation for each organism was determined based on placement on the concatenated ribosomal protein tree. Abundance metrics were calculated utilizing total dataset size, coverage of ribosomal protein-containing scaffolds, and predicted genome sizes (3 Mbp in general, 1.5 Mbp for OD-1 and OP-11). Ribosomal proteins utilized were RpL2, 3, 4, 5, 6, 14, 15, 16, 18, 22, 24 and RpS3, 8, 10, 17, 19.« less

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