Novel, Deep-Branching Heterotrophic Bacterial Populations Recovered from Thermal Spring Metagenomes

Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea, and harbor deeply-branching lineages that provide insight regarding the nature of early microbial life. We characterized bacterial populations in two circumneutral (pH ~8) Yellowstone...

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Published inFrontiers in microbiology Vol. 7; p. 304
Main Authors Colman, Daniel R, Jay, Zackary J, Inskeep, William P, Jennings, Ryan deM, Maas, Kendra R, Rusch, Douglas B, Takacs-Vesbach, Cristina D
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Research Foundation 15.03.2016
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Abstract Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea, and harbor deeply-branching lineages that provide insight regarding the nature of early microbial life. We characterized bacterial populations in two circumneutral (pH ~8) Yellowstone National Park thermal (T ~80°C) spring filamentous "streamer" communities using random metagenomic DNA sequence to investigate the metabolic potential of these novel populations. Four de novo assemblies representing three abundant, deeply-branching bacterial phylotypes were recovered. Analysis of conserved phylogenetic marker genes indicated that two of the phylotypes represent separate groups of an uncharacterized phylum (for which we propose the candidate phylum name "Pyropristinus"). The third new phylotype falls within the proposed Calescamantes phylum. Metabolic reconstructions of the "Pyropristinus" and Calescamantes populations showed that these organisms appear to be chemoorganoheterotrophs and have the genomic potential for aerobic respiration and oxidative phosphorylation via archaeal-like V-type, and bacterial F-type ATPases, respectively. A survey of similar phylotypes (>97% nt identity) within 16S rRNA gene datasets suggest that the newly described organisms are restricted to terrestrial thermal springs ranging from 70 to 90°C and pH values of ~7-9. The characterization of these lineages is important for understanding the diversity of deeply-branching bacterial phyla, and their functional role in high-temperature circumneutral "streamer" communities.
AbstractList Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea, and harbor deeply-branching lineages that provide insight regarding the nature of early microbial life. We characterized bacterial populations in two circumneutral (pH ~8) Yellowstone National Park thermal (T ~80°C) spring filamentous "streamer" communities using random metagenomic DNA sequence to investigate the metabolic potential of these novel populations. Four de novo assemblies representing three abundant, deeply-branching bacterial phylotypes were recovered. Analysis of conserved phylogenetic marker genes indicated that two of the phylotypes represent separate groups of an uncharacterized phylum (for which we propose the candidate phylum name "Pyropristinus"). The third new phylotype falls within the proposed Calescamantes phylum. Metabolic reconstructions of the "Pyropristinus" and Calescamantes populations showed that these organisms appear to be chemoorganoheterotrophs and have the genomic potential for aerobic respiration and oxidative phosphorylation via archaeal-like V-type, and bacterial F-type ATPases, respectively. A survey of similar phylotypes (>97% nt identity) within 16S rRNA gene datasets suggest that the newly described organisms are restricted to terrestrial thermal springs ranging from 70 to 90°C and pH values of ~7-9. The characterization of these lineages is important for understanding the diversity of deeply-branching bacterial phyla, and their functional role in high-temperature circumneutral "streamer" communities.
Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea, and harbor deeply-branching lineages that provide insight regarding the nature of early microbial life. We characterized bacterial populations in two circumneutral (pH ~ 8) Yellowstone National Park thermal (T ~ 80 oC) spring filamentous ‘streamer’ communities using random metagenomic DNA sequence to investigate the metabolic potential of these novel populations. Four de novo assemblies representing three abundant, deeply-branching bacterial phylotypes were recovered. Analysis of conserved phylogenetic marker genes indicated that two of the phylotypes represent separate groups of an uncharacterized phylum (for which we propose the candidate phylum name ‘Pyropristinus’). The third new phylotype falls within the proposed Calescamantes phylum. Metabolic reconstructions of the 'Pyropristinus' and Calescamantes populations showed that these organisms appear to be chemoorganoheterotrophs, and have the genomic potential for aerobic respiration and oxidative phosphorylation via archaeal-like V-type, and bacterial F-type ATPases, respectively. A survey of similar phylotypes (> 97% nt identity) within 16S rRNA gene datasets suggest that the newly described organisms are restricted to terrestrial thermal springs ranging from 70 - 90 oC and pH values of ~ 7 - 9. The characterization of these lineages is important for understanding the diversity of deeply-branching bacterial phyla, and their functional role in high-temperature circumneutral ‘streamer’ communities.
Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea , and harbor deeply-branching lineages that provide insight regarding the nature of early microbial life. We characterized bacterial populations in two circumneutral (pH ~8) Yellowstone National Park thermal ( T ~80°C) spring filamentous “streamer” communities using random metagenomic DNA sequence to investigate the metabolic potential of these novel populations. Four de novo assemblies representing three abundant, deeply-branching bacterial phylotypes were recovered. Analysis of conserved phylogenetic marker genes indicated that two of the phylotypes represent separate groups of an uncharacterized phylum (for which we propose the candidate phylum name “Pyropristinus”). The third new phylotype falls within the proposed Calescamantes phylum. Metabolic reconstructions of the “Pyropristinus” and Calescamantes populations showed that these organisms appear to be chemoorganoheterotrophs and have the genomic potential for aerobic respiration and oxidative phosphorylation via archaeal-like V-type, and bacterial F-type ATPases, respectively. A survey of similar phylotypes (>97% nt identity) within 16S rRNA gene datasets suggest that the newly described organisms are restricted to terrestrial thermal springs ranging from 70 to 90°C and pH values of ~7–9. The characterization of these lineages is important for understanding the diversity of deeply-branching bacterial phyla, and their functional role in high-temperature circumneutral “streamer” communities.
Author Jennings, Ryan deM
Inskeep, William P
Maas, Kendra R
Colman, Daniel R
Rusch, Douglas B
Jay, Zackary J
Takacs-Vesbach, Cristina D
AuthorAffiliation 1 Department of Biology, University of New Mexico Albuquerque, NM, USA
2 Thermal Biology Institute and Department of Land Resources and Environmental Sciences, Montana State University Bozeman, MT, USA
3 Center for Genomics and Bioinformatics, Indiana University Bloomington, IN, USA
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Keywords Yellowstone National Park
Aquificales
Thermotogae
hot springs
Calescamantes
Pyropristinus
hyperthermophiles
Language English
License This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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This article was submitted to Extreme Microbiology, a section of the journal Frontiers in Microbiology
Reviewed by: Tim Magnuson, Idaho State University, USA; Yiran Dong, University of Illinois, Urbana-Champaign, USA
Edited by: Jesse G. Dillon, California State University, Long Beach, USA
Ryan deM. Jennings, Mercer University, Macon, GA, USA
Present Address: Daniel R. Colman, Thermal Biology Institute and Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA
Kendra R. Maas, Biotechnology-Bioservices Center, University of Connecticut, Storrs, CT, USA
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Snippet Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea, and harbor deeply-branching lineages that...
Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea , and harbor deeply-branching lineages that...
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StartPage 304
SubjectTerms Aquificales
BASIC BIOLOGICAL SCIENCES
Calescamantes
Hot Springs
hyperthermophiles
Microbiology
Pyropristinus
Thermotogae
Yellowstone National Park
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Title Novel, Deep-Branching Heterotrophic Bacterial Populations Recovered from Thermal Spring Metagenomes
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