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Title: “Candidatus Thermonerobacter thiotrophicus,” A Non-phototrophic Member of the Bacteroidetes/Chlorobi With Dissimilatory Sulfur Metabolism in Hot Spring Mat Communities

Abstract

In this study we present evidence for a novel, thermophilic bacterium with dissimilatory sulfur metabolism, tentatively named “Candidatus Thermonerobacter thiotrophicus,” which is affiliated with the Bacteroides/Ignavibacteria/Chlorobi and which we predict to be a sulfate reducer. Dissimilatory sulfate reduction (DSR) is an important and ancient metabolic process for energy conservation with global importance for geochemical sulfur and carbon cycling. Characterized sulfate-reducing microorganisms (SRM) are found in a limited number of bacterial and archaeal phyla. However, based on highly diverse environmental dsrAB sequences, a variety of uncultivated and unidentified SRM must exist. The recent development of high-throughput sequencing methods allows the phylogenetic identification of some of these uncultured SRM. In this study, we identified a novel putative SRM inhabiting hot spring microbial mats that is a member of the OPB56 clade (“Ca. Kapabacteria”) within the Bacteroidetes/Chlorobi superphylum. Partial genomes for this new organism were retrieved from metagenomes from three different hot springs in Yellowstone National Park, United States, and Japan. Supporting the prediction of a sulfate-reducing metabolism for this organism during period of anoxia, diel metatranscriptomic analyses indicate highest relative transcript levels in situ for all DSR-related genes at night. The presence of terminal oxidases, which are transcribed during the day, furthermore » suggests that these organisms might also perform aerobic respiration. The relative phylogenetic proximity to the sulfur-oxidizing, chlorophototrophic Chlorobi further raises new questions about the evolution of dissimilatory sulfur metabolism.« less

Authors:
 [1];  [2];  [3];  [4];  [1];  [3];  [5];  [5];  [6];  [7]
  1. Tokyo Metropolitan Univ. (Japan); Pennsylvania State Univ., University Park, PA (United States)
  2. Pennsylvania State Univ., University Park, PA (United States); Univ. of Colorado, Pueblo, CO (United States)
  3. Univ. of Wisconsin, Madison, WI (United States)
  4. Tokyo Metropolitan Univ. (Japan); Univ. of St. La Salle, Bacolod (Philippines)
  5. Montana State Univ., Bozeman, MT (United States)
  6. Tokyo Metropolitan Univ. (Japan)
  7. Pennsylvania State Univ., University Park, PA (United States); Montana State Univ., Bozeman, MT (United States)
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1610260
Grant/Contract Number:  
FG02-94ER20137; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; hot spring; microbial mat; sulfate reducing bacteria; Bacteroidetes/Chlorobi; metatranscriptome; metagenome; dsrAB

Citation Formats

Thiel, Vera, Garcia Costas, Amaya M., Fortney, Nathaniel W., Martinez, Joval N., Tank, Marcus, Roden, Eric E., Boyd, Eric S., Ward, David M., Hanada, Satoshi, and Bryant, Donald A. “Candidatus Thermonerobacter thiotrophicus,” A Non-phototrophic Member of the Bacteroidetes/Chlorobi With Dissimilatory Sulfur Metabolism in Hot Spring Mat Communities. United States: N. p., 2019. Web. doi:10.3389/fmicb.2018.03159.
Thiel, Vera, Garcia Costas, Amaya M., Fortney, Nathaniel W., Martinez, Joval N., Tank, Marcus, Roden, Eric E., Boyd, Eric S., Ward, David M., Hanada, Satoshi, & Bryant, Donald A. “Candidatus Thermonerobacter thiotrophicus,” A Non-phototrophic Member of the Bacteroidetes/Chlorobi With Dissimilatory Sulfur Metabolism in Hot Spring Mat Communities. United States. https://doi.org/10.3389/fmicb.2018.03159
Thiel, Vera, Garcia Costas, Amaya M., Fortney, Nathaniel W., Martinez, Joval N., Tank, Marcus, Roden, Eric E., Boyd, Eric S., Ward, David M., Hanada, Satoshi, and Bryant, Donald A. Wed . "“Candidatus Thermonerobacter thiotrophicus,” A Non-phototrophic Member of the Bacteroidetes/Chlorobi With Dissimilatory Sulfur Metabolism in Hot Spring Mat Communities". United States. https://doi.org/10.3389/fmicb.2018.03159. https://www.osti.gov/servlets/purl/1610260.
@article{osti_1610260,
title = {“Candidatus Thermonerobacter thiotrophicus,” A Non-phototrophic Member of the Bacteroidetes/Chlorobi With Dissimilatory Sulfur Metabolism in Hot Spring Mat Communities},
author = {Thiel, Vera and Garcia Costas, Amaya M. and Fortney, Nathaniel W. and Martinez, Joval N. and Tank, Marcus and Roden, Eric E. and Boyd, Eric S. and Ward, David M. and Hanada, Satoshi and Bryant, Donald A.},
abstractNote = {In this study we present evidence for a novel, thermophilic bacterium with dissimilatory sulfur metabolism, tentatively named “Candidatus Thermonerobacter thiotrophicus,” which is affiliated with the Bacteroides/Ignavibacteria/Chlorobi and which we predict to be a sulfate reducer. Dissimilatory sulfate reduction (DSR) is an important and ancient metabolic process for energy conservation with global importance for geochemical sulfur and carbon cycling. Characterized sulfate-reducing microorganisms (SRM) are found in a limited number of bacterial and archaeal phyla. However, based on highly diverse environmental dsrAB sequences, a variety of uncultivated and unidentified SRM must exist. The recent development of high-throughput sequencing methods allows the phylogenetic identification of some of these uncultured SRM. In this study, we identified a novel putative SRM inhabiting hot spring microbial mats that is a member of the OPB56 clade (“Ca. Kapabacteria”) within the Bacteroidetes/Chlorobi superphylum. Partial genomes for this new organism were retrieved from metagenomes from three different hot springs in Yellowstone National Park, United States, and Japan. Supporting the prediction of a sulfate-reducing metabolism for this organism during period of anoxia, diel metatranscriptomic analyses indicate highest relative transcript levels in situ for all DSR-related genes at night. The presence of terminal oxidases, which are transcribed during the day, further suggests that these organisms might also perform aerobic respiration. The relative phylogenetic proximity to the sulfur-oxidizing, chlorophototrophic Chlorobi further raises new questions about the evolution of dissimilatory sulfur metabolism.},
doi = {10.3389/fmicb.2018.03159},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {United States},
year = {Wed Jan 09 00:00:00 EST 2019},
month = {Wed Jan 09 00:00:00 EST 2019}
}

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