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Front. Microbiol. | doi: 10.3389/fmicb.2018.03159

"Candidatus Thermonerobacter thiotrophicus," a non-phototrophic, sulfate-reducing member of the Bacteroidetes/Chlorobi inhabiting hot spring environments

 Vera Thiel1, 2*, Amaya Garcia-Costas2, 3,  Nathaniel W. Fortney4,  Joval N. Martinez1, 5,  Marcus Tank1, 2,  Eric Roden4, Eric S. Boyd6,  David M. Ward6 and  Donald A. Bryant2, 6*
  • 1Biochemistry and Molecular Biology, Tokyo Metropolitan University, Japan
  • 2Pennsylvania State University, United States
  • 3Colorado State University Pueblo, United States
  • 4University of Wisconsin-Madison, United States
  • 5University of St. La Salle, Philippines
  • 6Montana State University, United States

In this study we present evidence for a novel, thermophilic sulfate-reducing bacterium, tentatively named ‘Candidatus Thermonerobacter thiotrophicus’, which is affiliated with the Bacteroides/Ignavibacteria/Chlorobi superphylum. 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 upon 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, USA, 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 suggest 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.

Keywords: hot spring, microbial mat, Sulfate reducing bacteria, Bacteroidetes/Chlorobi, metatranscriptome, Metagenome, dsrAB

Received: 16 Oct 2018; Accepted: 05 Dec 2018.

Edited by:

Marc Mussmann, Universität Wien, Austria

Reviewed by:

Michael Pester, German Collection of Microorganisms and Cell Cultures GmbH (DSMZ), Germany
Geng Wu, China University of Geosciences Wuhan, China  

Copyright: © 2018 Thiel, Garcia-Costas, Fortney, Martinez, Tank, Roden, Boyd, Ward and Bryant. 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) and the copyright owner(s) 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.

* Correspondence:
Prof. Vera Thiel, Tokyo Metropolitan University, Biochemistry and Molecular Biology, Hachioji, 16802, Pennsylvania, Japan, vthiel@tmu.ac.jp
Prof. Donald A. Bryant, Pennsylvania State University, University Park, 16802, Pennsylvania, United States, dab14@psu.edu