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Title: Genomic analysis of methanogenic archaea reveals a shift towards energy conservation

Abstract

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. 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. Methanogens occupy a unique ecological niche, acting as the terminal electron acceptors in anaerobic environments, andmore » 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.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Univ. of California, Santa Barbara, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Univ. of California (United States); US Army Research Office (ARO); National Science Foundation (NSF); VILLUM Foundation (Denmark)
OSTI Identifier:
1618559
Alternate Identifier(s):
OSTI ID: 1424613
Grant/Contract Number:  
SC0010352; W911NF-09-0001; OCE-1046144; DGE 1144085; VKR023128
Resource Type:
Published Article
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Name: BMC Genomics Journal Volume: 18 Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 32 ENERGY CONSERVATION, CONSUMPTION, AND UTILIZATION; Methanogenesis; Archaea; Metabolism; Anaerobes; Energy

Citation Formats

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., and O’Malley, Michelle A. Genomic analysis of methanogenic archaea reveals a shift towards energy conservation. United Kingdom: N. p., 2017. Web. doi:10.1186/s12864-017-4036-4.
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. United Kingdom. doi:10.1186/s12864-017-4036-4.
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., and O’Malley, Michelle A. Mon . "Genomic analysis of methanogenic archaea reveals a shift towards energy conservation". United Kingdom. doi:10.1186/s12864-017-4036-4.
@article{osti_1618559,
title = {Genomic analysis of methanogenic archaea reveals a shift towards energy conservation},
author = {Gilmore, Sean P. and Henske, John K. and Sexton, Jessica A. and Solomon, Kevin V. and Seppälä, Susanna and Yoo, Justin I. and Huyett, Lauren M. and Pressman, Abe and Cogan, James Z. and Kivenson, Veronika and Peng, Xuefeng and Tan, YerPeng and Valentine, David L. and O’Malley, Michelle A.},
abstractNote = {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. 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. 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 CO2 metabolism in Msph. cuniculi. The newly proposed substrates establish an important foundation with which to decipher how methanogens behave in native communities, as CO2 and formate are common electron carriers in microbial communities.},
doi = {10.1186/s12864-017-4036-4},
journal = {BMC Genomics},
number = 1,
volume = 18,
place = {United Kingdom},
year = {2017},
month = {8}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1186/s12864-017-4036-4

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Cited by: 5 works
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