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Title: Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea

Abstract

Here, we report that sulfate is the predominant electron acceptor for anaerobic oxidation of methane (AOM) in marine sediments. This process is carried out by a syntrophic consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria (SRB) through an energy conservation mechanism that is still poorly understood. It was previously hypothesized that ANME alone could couple methane oxidation to dissimilatory sulfate reduction, but a genetic and biochemical basis for this proposal has not been identified. Using comparative genomic and phylogenetic analyses, we found the genetic capacity in ANME and related methanogenic archaea for sulfate reduction, including sulfate adenylyltransferase, APS kinase, APS/PAPS reductase and two different sulfite reductases. Additionally, based on characterized homologs and the lack of associated energy conserving complexes, the sulfate reduction pathways in ANME are likely used for assimilation but not dissimilation of sulfate. Environmental metaproteomic analysis confirmed the expression of 6 proteins in the sulfate assimilation pathway of ANME. The highest expressed proteins related to sulfate assimilation were two sulfite reductases, namely assimilatory-type low-molecular-weight sulfite reductase (alSir) and a divergent group of coenzyme F420-dependent sulfite reductase (Group II Fsr). In methane seep sediment microcosm experiments, however, sulfite and zero-valent sulfur amendments were inhibitory to ANME-2a/2c whilemore » growth in their syntrophic SRB partner was not observed. Combined with our genomic and metaproteomic results, the passage of sulfur species by ANME as metabolic intermediates for their SRB partners is unlikely. Instead, our findings point to a possible niche for ANME to assimilate inorganic sulfur compounds more oxidized than sulfide in anoxic marine environments.« less

Authors:
; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1484309
Alternate Identifier(s):
OSTI ID: 1528712
Grant/Contract Number:  
SC0016469; AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Yu, Hang, Susanti, Dwi, McGlynn, Shawn E., Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Scheller, Silvan, Tavormina, Patricia L., Hettich, Robert L., Mukhopadhyay, Biswarup, and Orphan, Victoria J. Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea. Switzerland: N. p., 2018. Web. doi:10.3389/fmicb.2018.02917.
Yu, Hang, Susanti, Dwi, McGlynn, Shawn E., Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Scheller, Silvan, Tavormina, Patricia L., Hettich, Robert L., Mukhopadhyay, Biswarup, & Orphan, Victoria J. Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea. Switzerland. doi:10.3389/fmicb.2018.02917.
Yu, Hang, Susanti, Dwi, McGlynn, Shawn E., Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Scheller, Silvan, Tavormina, Patricia L., Hettich, Robert L., Mukhopadhyay, Biswarup, and Orphan, Victoria J. Mon . "Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea". Switzerland. doi:10.3389/fmicb.2018.02917.
@article{osti_1484309,
title = {Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea},
author = {Yu, Hang and Susanti, Dwi and McGlynn, Shawn E. and Skennerton, Connor T. and Chourey, Karuna and Iyer, Ramsunder and Scheller, Silvan and Tavormina, Patricia L. and Hettich, Robert L. and Mukhopadhyay, Biswarup and Orphan, Victoria J.},
abstractNote = {Here, we report that sulfate is the predominant electron acceptor for anaerobic oxidation of methane (AOM) in marine sediments. This process is carried out by a syntrophic consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria (SRB) through an energy conservation mechanism that is still poorly understood. It was previously hypothesized that ANME alone could couple methane oxidation to dissimilatory sulfate reduction, but a genetic and biochemical basis for this proposal has not been identified. Using comparative genomic and phylogenetic analyses, we found the genetic capacity in ANME and related methanogenic archaea for sulfate reduction, including sulfate adenylyltransferase, APS kinase, APS/PAPS reductase and two different sulfite reductases. Additionally, based on characterized homologs and the lack of associated energy conserving complexes, the sulfate reduction pathways in ANME are likely used for assimilation but not dissimilation of sulfate. Environmental metaproteomic analysis confirmed the expression of 6 proteins in the sulfate assimilation pathway of ANME. The highest expressed proteins related to sulfate assimilation were two sulfite reductases, namely assimilatory-type low-molecular-weight sulfite reductase (alSir) and a divergent group of coenzyme F420-dependent sulfite reductase (Group II Fsr). In methane seep sediment microcosm experiments, however, sulfite and zero-valent sulfur amendments were inhibitory to ANME-2a/2c while growth in their syntrophic SRB partner was not observed. Combined with our genomic and metaproteomic results, the passage of sulfur species by ANME as metabolic intermediates for their SRB partners is unlikely. Instead, our findings point to a possible niche for ANME to assimilate inorganic sulfur compounds more oxidized than sulfide in anoxic marine environments.},
doi = {10.3389/fmicb.2018.02917},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {Switzerland},
year = {2018},
month = {12}
}

Journal Article:
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DOI: 10.3389/fmicb.2018.02917

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