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Title: Comparative Genomic Analysis of the Class Epsilonproteobacteria and Proposed Reclassification to Epsilonbacteraeota (phyl. nov.)

Abstract

The Epsilonproteobacteria is the fifth validly described class of the phylum Proteobacteria, known primarily for clinical relevance and for chemolithotrophy in various terrestrial and marine environments, including deep-sea hydrothermal vents. As 16S rRNA gene repositories have expanded and protein marker analysis become more common, the phylogenetic placement of this class has become less certain. A number of recent analyses of the bacterial tree of life using both 16S rRNA and concatenated marker gene analyses have failed to recover the Epsilonproteobacteria as monophyletic with all other classes of Proteobacteria. In order to address this issue, we investigated the phylogenetic placement of this class in the bacterial domain using 16S and 23S rRNA genes, as well as 120 single-copy marker proteins. Singleand concatenated-marker trees were created using a data set of 4,170 bacterial representatives, including 98 Epsilonproteobacteria. Phylogenies were inferred under a variety of tree building methods, with sequential jackknifing of outgroup phyla to ensure robustness of phylogenetic affiliations under differing combinations of bacterial genomes. Based on the assessment of nearly 300 phylogenetic tree topologies, we conclude that the continued inclusion of Epsilonproteobacteria within the Proteobacteria is not warranted, and that this group should be reassigned to a novel phylum for whichmore » we propose the name Epsilonbacteraeota (phyl. nov.). We further recommend the reclassification of the order Desulfurellales (Deltaproteobacteria) to a novel class within this phylum and a number of subordinate changes to ensure consistency with the genome-based phylogeny. Phylogenomic analysis of 658 genomes belonging to the newly proposed Epsilonbacteraeota suggests that the ancestor of this phylum was an autotrophic, motile, thermophilic chemolithotroph that likely assimilated nitrogen from ammonium taken up from the environment or generated from environmental nitrate and nitrite by employing a variety of functional redox modules. The emergence of chemoorganoheterotrophic lifestyles in several Epsilonbacteraeota families is the result of multiple independent losses of various ancestral chemolithoautotrophic pathways. Our proposed reclassification of this group resolves an important anomaly in bacterial systematics and ensures that the taxonomy of Proteobacteria remains robust, specifically as genome-based taxonomies become more common.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [1]
+ Show Author Affiliations
  1. Univ. of Queensland, St Lucia, QLD (Australia). School of Chemistry and Molecular Biosciences. Australian Centre for Ecogenomics
  2. Univ. of Rhode Island, Kingston, RI (United States). College of the Environment and Life Sciences. Dept. of Cell and Molecular Biology
  3. Japan Agency for Marine-Earth Science and Technology, Yokosuka (Japan). Dept. of Subsurface Geobiological Analysis and Research
  4. Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Dept. of Biology
  5. Technische Univ. Darmstadt (Germany). Dept. of Biology. Microbial Energy Conversion and Biotechnology
  6. Clemson Univ., SC (United States). Life Sciences Facility. Dept. of Biological Sciences
  7. Univ. of Delaware, Newark, DE (United States). Delaware Biotechnology Inst. College of Earth, Ocean, and Environment. School of Marine Science and Policy.
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  9. Queens College of the City of Univ. of New York (United States). School of Earth and Environmental Sciences. Dept. of Biology; Xiamen Univ. (China). College of Ocean and Earth Sciences. Inst. of Marine Microbes and Ecospheres. State Key Lab. of Marine Environmental Science
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1628154
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; Epsilonproteobacteria; taxonomy; classification; genome; phylogenomics; Epsilonbacteraeota; evolution

Citation Formats

Waite, David W., Vanwonterghem, Inka, Rinke, Christian, Parks, Donovan H., Zhang, Ying, Takai, Ken, Sievert, Stefan M., Simon, Jörg, Campbell, Barbara J., Hanson, Thomas E., Woyke, Tanja, Klotz, Martin G., and Hugenholtz, Philip. Comparative Genomic Analysis of the Class Epsilonproteobacteria and Proposed Reclassification to Epsilonbacteraeota (phyl. nov.). United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.00682.
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Waite, David W., Vanwonterghem, Inka, Rinke, Christian, Parks, Donovan H., Zhang, Ying, Takai, Ken, Sievert, Stefan M., Simon, Jörg, Campbell, Barbara J., Hanson, Thomas E., Woyke, Tanja, Klotz, Martin G., & Hugenholtz, Philip. Comparative Genomic Analysis of the Class Epsilonproteobacteria and Proposed Reclassification to Epsilonbacteraeota (phyl. nov.). United States. https://doi.org/10.3389/fmicb.2017.00682
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Waite, David W., Vanwonterghem, Inka, Rinke, Christian, Parks, Donovan H., Zhang, Ying, Takai, Ken, Sievert, Stefan M., Simon, Jörg, Campbell, Barbara J., Hanson, Thomas E., Woyke, Tanja, Klotz, Martin G., and Hugenholtz, Philip. Mon . "Comparative Genomic Analysis of the Class Epsilonproteobacteria and Proposed Reclassification to Epsilonbacteraeota (phyl. nov.)". United States. https://doi.org/10.3389/fmicb.2017.00682. https://www.osti.gov/servlets/purl/1628154.
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@article{osti_1628154,
title = {Comparative Genomic Analysis of the Class Epsilonproteobacteria and Proposed Reclassification to Epsilonbacteraeota (phyl. nov.)},
author = {Waite, David W. and Vanwonterghem, Inka and Rinke, Christian and Parks, Donovan H. and Zhang, Ying and Takai, Ken and Sievert, Stefan M. and Simon, Jörg and Campbell, Barbara J. and Hanson, Thomas E. and Woyke, Tanja and Klotz, Martin G. and Hugenholtz, Philip},
abstractNote = {The Epsilonproteobacteria is the fifth validly described class of the phylum Proteobacteria, known primarily for clinical relevance and for chemolithotrophy in various terrestrial and marine environments, including deep-sea hydrothermal vents. As 16S rRNA gene repositories have expanded and protein marker analysis become more common, the phylogenetic placement of this class has become less certain. A number of recent analyses of the bacterial tree of life using both 16S rRNA and concatenated marker gene analyses have failed to recover the Epsilonproteobacteria as monophyletic with all other classes of Proteobacteria. In order to address this issue, we investigated the phylogenetic placement of this class in the bacterial domain using 16S and 23S rRNA genes, as well as 120 single-copy marker proteins. Singleand concatenated-marker trees were created using a data set of 4,170 bacterial representatives, including 98 Epsilonproteobacteria. Phylogenies were inferred under a variety of tree building methods, with sequential jackknifing of outgroup phyla to ensure robustness of phylogenetic affiliations under differing combinations of bacterial genomes. Based on the assessment of nearly 300 phylogenetic tree topologies, we conclude that the continued inclusion of Epsilonproteobacteria within the Proteobacteria is not warranted, and that this group should be reassigned to a novel phylum for which we propose the name Epsilonbacteraeota (phyl. nov.). We further recommend the reclassification of the order Desulfurellales (Deltaproteobacteria) to a novel class within this phylum and a number of subordinate changes to ensure consistency with the genome-based phylogeny. Phylogenomic analysis of 658 genomes belonging to the newly proposed Epsilonbacteraeota suggests that the ancestor of this phylum was an autotrophic, motile, thermophilic chemolithotroph that likely assimilated nitrogen from ammonium taken up from the environment or generated from environmental nitrate and nitrite by employing a variety of functional redox modules. The emergence of chemoorganoheterotrophic lifestyles in several Epsilonbacteraeota families is the result of multiple independent losses of various ancestral chemolithoautotrophic pathways. Our proposed reclassification of this group resolves an important anomaly in bacterial systematics and ensures that the taxonomy of Proteobacteria remains robust, specifically as genome-based taxonomies become more common.},
doi = {10.3389/fmicb.2017.00682},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Mon Apr 24 00:00:00 EDT 2017},
month = {Mon Apr 24 00:00:00 EDT 2017}
}
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    Prokaryotic Hydrocarbon Degraders
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