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

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. (2018) Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea. Frontiers in Microbiology, 9 . Art. No. 2917. ISSN 1664-302X. PMCID PMC6286981. doi:10.3389/fmicb.2018.02917.

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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. 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 F_(420)-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.

Item Type:Article
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URLURL TypeDescription CentralArticle
Yu, Hang0000-0002-7600-1582
McGlynn, Shawn E.0000-0002-8199-7011
Skennerton, Connor T.0000-0003-1320-4873
Scheller, Silvan0000-0002-0667-9224
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2018 Yu, Susanti, McGlynn, Skennerton, Chourey, Iyer, Scheller, Tavormina, Hettich, Mukhopadhyay and Orphan. 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. Received: 01 September 2018; Accepted: 13 November 2018; Published: 03 December 2018. We thank the Environmental Analysis Center at Caltech and its director Nathan Delaskas for the help and support with chemical sample analysis. We thank Roland Hatzenpichler, Danielle Goudeau, Rex R. Malmstrom, Tanja Woyke for their help with activity-based cell sorting and genome sequencing. Special thanks to Katherine Dawson, Grayson Chadwick and two reviewers for constructive comments on the manuscript. Data Availability: The ANME genomes generated for this study have been deposited at NCBI GenBank database under the Whole Genome Shotgun project accession numbers QENH00000000, MZXQ00000000, and PYCL00000000 for ANME-1b (ANME sp. CONS3730B06UFb1), ANME-2b (ANME sp. HR1), and ANME-2c (ANME sp. S7142MS2) respectively. Protein sequences and alignments analyzed for this study can be found on FigShare: 10.6084/m9.figshare.7035917, 10.6084/m9.figshare.7036289, and 10.6084/m9.figshare.7037228. Author Contributions: HY, RH, BM, and VO designed research. HY, DS, SM, CS, KC, RI, SS, and PT performed research and data analysis. HY and VO wrote the paper with contribution from all authors. This research and HY, SM, CS, SS, KC, RI, RH, and VO were supported by funding from the United States Department of Energy, Office of Science, Biological and Environmental Research Program under award number DE-SC0016469 and by a DOE Office of Science User Facility grant through the Joint Genome Institute and Environmental Molecular Science Laboratory (FICUS Grant 49001). HY, PT, and VO were additionally supported by the Gordon and Betty Moore Foundation through grant GBMF3780. This is Center for Dark Energy and Biosphere Investigations (C-DEBI) Contribution 449. SEM and VO was additionally supported by funding from the National Aeronautics and Space Administration Exobiology Grant NNX14AO48G. DS and BM were supported by the National Aeronautics and Space Administration Exobiology and Evolutionary Biology Grant NNX13AI05G. BM was also supported by Virginia Tech Agricultural Experiment Station Hatch Program (CRIS project VA-160021). The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Funding AgencyGrant Number
Department of Energy (DOE)DE-SC0016469
Genome Institute and Environmental Molecular Science Laboratory49001
Gordon and Betty Moore FoundationGBMF3780
Virginia TechVA-160021
Subject Keywords:sulfur pathway, sulfate reduction, anaerobic oxidation of methane, ANME, syntrophy, sulfate adenylyltransferase, APS/PAPS Reductase, sulfite reductase
PubMed Central ID:PMC6286981
Record Number:CaltechAUTHORS:20181212-151637497
Persistent URL:
Official Citation:Yu H, Susanti D, McGlynn SE, Skennerton CT, Chourey K, Iyer R, Scheller S, Tavormina PL, Hettich RL, Mukhopadhyay B and Orphan VJ (2018) Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea. Front. Microbiol. 9:2917. doi: 10.3389/fmicb.2018.02917
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:91741
Deposited By: Tony Diaz
Deposited On:12 Dec 2018 23:32
Last Modified:16 Nov 2021 03:44

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