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Genomic analysis of methanogenic archaea reveals a shift towards energy conservation

BACKGROUND: The metabolism of archaeal methanogens drives methane release into the environment and is critical to understanding global carbon cycling. Methanogenesis operates at a very low reducing potential compared to other forms of respiration and is therefore critical to many anaerobic environme...

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Autores principales: Gilmore, Sean P., Henske, John K., Sexton, Jessica A., Solomon, Kevin V., Seppälä, Susanna, Yoo, Justin I, Huyett, Lauren M., Pressman, Abe, Cogan, James Z., Kivenson, Veronika, Peng, Xuefeng, Tan, YerPeng, Valentine, David L., O’Malley, Michelle A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5563889/
https://www.ncbi.nlm.nih.gov/pubmed/28826405
http://dx.doi.org/10.1186/s12864-017-4036-4
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author Gilmore, Sean P.
Henske, John K.
Sexton, Jessica A.
Solomon, Kevin V.
Seppälä, Susanna
Yoo, Justin I
Huyett, Lauren M.
Pressman, Abe
Cogan, James Z.
Kivenson, Veronika
Peng, Xuefeng
Tan, YerPeng
Valentine, David L.
O’Malley, Michelle A.
author_facet Gilmore, Sean P.
Henske, John K.
Sexton, Jessica A.
Solomon, Kevin V.
Seppälä, Susanna
Yoo, Justin I
Huyett, Lauren M.
Pressman, Abe
Cogan, James Z.
Kivenson, Veronika
Peng, Xuefeng
Tan, YerPeng
Valentine, David L.
O’Malley, Michelle A.
author_sort Gilmore, Sean P.
collection PubMed
description BACKGROUND: The metabolism of archaeal methanogens drives methane release into the environment and is critical to understanding global carbon cycling. Methanogenesis operates at a very low reducing potential compared to other forms of respiration and is therefore critical to many anaerobic environments. Harnessing or altering methanogen metabolism has the potential to mitigate global warming and even be utilized for energy applications. RESULTS: Here, we report draft genome sequences for the isolated methanogens Methanobacterium bryantii, Methanosarcina spelaei, Methanosphaera cuniculi, and Methanocorpusculum parvum. These anaerobic, methane-producing archaea represent a diverse set of isolates, capable of methylotrophic, acetoclastic, and hydrogenotrophic methanogenesis. Assembly and analysis of the genomes allowed for simple and rapid reconstruction of metabolism in the four methanogens. Comparison of the distribution of Clusters of Orthologous Groups (COG) proteins to a sample of genomes from the RefSeq database revealed a trend towards energy conservation in genome composition of all methanogens sequenced. Further analysis of the predicted membrane proteins and transporters distinguished differing energy conservation methods utilized during methanogenesis, such as chemiosmotic coupling in Msar. spelaei and electron bifurcation linked to chemiosmotic coupling in Mbac. bryantii and Msph. cuniculi. CONCLUSIONS: Methanogens occupy a unique ecological niche, acting as the terminal electron acceptors in anaerobic environments, and their genomes display a significant shift towards energy conservation. The genome-enabled reconstructed metabolisms reported here have significance to diverse anaerobic communities and have led to proposed substrate utilization not previously reported in isolation, such as formate and methanol metabolism in Mbac. bryantii and CO(2) metabolism in Msph. cuniculi. The newly proposed substrates establish an important foundation with which to decipher how methanogens behave in native communities, as CO(2) and formate are common electron carriers in microbial communities. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-4036-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-55638892017-08-23 Genomic analysis of methanogenic archaea reveals a shift towards energy conservation Gilmore, Sean P. Henske, John K. Sexton, Jessica A. Solomon, Kevin V. Seppälä, Susanna Yoo, Justin I Huyett, Lauren M. Pressman, Abe Cogan, James Z. Kivenson, Veronika Peng, Xuefeng Tan, YerPeng Valentine, David L. O’Malley, Michelle A. BMC Genomics Research Article BACKGROUND: The metabolism of archaeal methanogens drives methane release into the environment and is critical to understanding global carbon cycling. Methanogenesis operates at a very low reducing potential compared to other forms of respiration and is therefore critical to many anaerobic environments. Harnessing or altering methanogen metabolism has the potential to mitigate global warming and even be utilized for energy applications. RESULTS: Here, we report draft genome sequences for the isolated methanogens Methanobacterium bryantii, Methanosarcina spelaei, Methanosphaera cuniculi, and Methanocorpusculum parvum. These anaerobic, methane-producing archaea represent a diverse set of isolates, capable of methylotrophic, acetoclastic, and hydrogenotrophic methanogenesis. Assembly and analysis of the genomes allowed for simple and rapid reconstruction of metabolism in the four methanogens. Comparison of the distribution of Clusters of Orthologous Groups (COG) proteins to a sample of genomes from the RefSeq database revealed a trend towards energy conservation in genome composition of all methanogens sequenced. Further analysis of the predicted membrane proteins and transporters distinguished differing energy conservation methods utilized during methanogenesis, such as chemiosmotic coupling in Msar. spelaei and electron bifurcation linked to chemiosmotic coupling in Mbac. bryantii and Msph. cuniculi. CONCLUSIONS: Methanogens occupy a unique ecological niche, acting as the terminal electron acceptors in anaerobic environments, and their genomes display a significant shift towards energy conservation. The genome-enabled reconstructed metabolisms reported here have significance to diverse anaerobic communities and have led to proposed substrate utilization not previously reported in isolation, such as formate and methanol metabolism in Mbac. bryantii and CO(2) metabolism in Msph. cuniculi. The newly proposed substrates establish an important foundation with which to decipher how methanogens behave in native communities, as CO(2) and formate are common electron carriers in microbial communities. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-4036-4) contains supplementary material, which is available to authorized users. BioMed Central 2017-08-21 /pmc/articles/PMC5563889/ /pubmed/28826405 http://dx.doi.org/10.1186/s12864-017-4036-4 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Gilmore, Sean P.
Henske, John K.
Sexton, Jessica A.
Solomon, Kevin V.
Seppälä, Susanna
Yoo, Justin I
Huyett, Lauren M.
Pressman, Abe
Cogan, James Z.
Kivenson, Veronika
Peng, Xuefeng
Tan, YerPeng
Valentine, David L.
O’Malley, Michelle A.
Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
title Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
title_full Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
title_fullStr Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
title_full_unstemmed Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
title_short Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
title_sort genomic analysis of methanogenic archaea reveals a shift towards energy conservation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5563889/
https://www.ncbi.nlm.nih.gov/pubmed/28826405
http://dx.doi.org/10.1186/s12864-017-4036-4
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