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Sulfate differentially stimulates but is not respired by diverse anaerobic methanotrophic archaea

Yu, Hang and Skennerton, Connor T. and Chadwick, Grayson L. and Leu, Andy O. and Aoki, Masataka and Tyson, Gene W. and Orphan, Victoria J. (2022) Sulfate differentially stimulates but is not respired by diverse anaerobic methanotrophic archaea. ISME Journal, 16 (1). pp. 168-177. ISSN 1751-7362. doi:10.1038/s41396-021-01047-0.

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Sulfate-coupled anaerobic oxidation of methane (AOM) is a major methane sink in marine sediments. Multiple lineages of anaerobic methanotrophic archaea (ANME) often coexist in sediments and catalyze this process syntrophically with sulfate-reducing bacteria (SRB), but the potential differences in ANME ecophysiology and mechanisms of syntrophy remain unresolved. A humic acid analog, anthraquinone 2,6-disulfonate (AQDS), could decouple archaeal methanotrophy from bacterial sulfate reduction and serve as the terminal electron acceptor for AOM (AQDS-coupled AOM). Here in sediment microcosm experiments, we examined variations in physiological response between two co-occurring ANME-2 families (ANME-2a and ANME-2c) and tested the hypothesis of sulfate respiration by ANME-2. Sulfate concentrations as low as 100 µM increased AQDS-coupled AOM nearly 2-fold matching the rates of sulfate-coupled AOM. However, the SRB partners remained inactive in microcosms with sulfate and AQDS and neither ANME-2 families respired sulfate, as shown by their cellular sulfur contents and anabolic activities measured using nanoscale secondary ion mass spectrometry. ANME-2a anabolic activity was significantly higher than ANME-2c, suggesting that ANME-2a was primarily responsible for the observed sulfate stimulation of AQDS-coupled AOM. Comparative transcriptomics showed significant upregulation of ANME-2a transcripts linked to multiple ABC transporters and downregulation of central carbon metabolism during AQDS-coupled AOM compared to sulfate-coupled AOM. Surprisingly, genes involved in sulfur anabolism were not differentially expressed during AQDS-coupled AOM with and without sulfate amendment. Collectively, this data indicates that ANME-2 archaea are incapable of respiring sulfate, but sulfate availability differentially stimulates the growth and AOM activity of different ANME lineages.

Item Type:Article
Related URLs:
URLURL TypeDescription ReadCube access
Yu, Hang0000-0002-7600-1582
Skennerton, Connor T.0000-0003-1320-4873
Chadwick, Grayson L.0000-0003-0700-9350
Leu, Andy O.0000-0002-9882-9364
Aoki, Masataka0000-0002-9352-2072
Tyson, Gene W.0000-0001-8559-9427
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© The Author(s), under exclusive licence to International Society for Microbial Ecology 2021. Received 27 January 2021; Revised 21 June 2021; Accepted 22 June 2021. We thank our colleagues, facilities managers, and staff at Caltech: Stephanie Connon for assistance with iTag sample preparation; Ranjani Murali for assistance with sulfate-reducing bacteria phylogeny; Haley Sapers for comments on the manuscript; Nathan Dalleska for assistance with ion chromatography at the Environmental Analysis Center; Yunbin Guan for assistance with nanoSIMS analyses at the Microanalysis Center in the Division of Geological and Planetary Sciences; Fan Gao for valuable discussions on transcriptome analysis at Bioinformatics Resource Center in the Beckman Institute; David Vander Velde for nuclear magnetic resonance analysis at the Liquid NMR Facility in the Division of Chemistry and Chemical Engineering. We also thank Margaret Butler at University of Queensland for assistance with RNA sample preparation and sequencing. We further acknowledge the support from the Monterey Bay Aquarium Research Institute (MBARI) and the pilots and crew of the R/W Western Flyer and ROV Doc Ricketts who supported the field expedition and sample collection. Special thanks to three anonymous reviewers for their constructive comments on the manuscript. This work was supported by the United States Department of Energy’s Office of Science Biological and Environmental Research Program (DE-SC0016469 and DE-SC0020373), Caltech’s Center for Environmental Microbial Interactions (CEMI), and the Simons Foundation Principles of Microbial Ecosystems (PriME). Data availability: The high-coverage metagenomic assembly and metagenome-assembled genomes (MAGs) from this study can be found in Joint Genome Institute Genome Online Database under Study ID Gs0135232. Also, the metagenomic reads, transcriptomic reads and MAGs can be found under National Center for Biotechnology Information BioProject IDs PRJNA431796 and PRJNA576751. Database IDs for each MAG can be found in Supplementary Table 3. Author Contributions: HY, GWT and VJO designed the study. HY performed geochemical analyses. MA developed the ANME-2a FISH probe. HY and GLC performed the FISH-nanoSIMS experiments and analyses. HY, CTS and AOL performed the metagenomic and metatranscriptomic experiments and analyses. HY and VJO wrote the manuscript with contributions from other authors. All authors reviewed, revised, and approved the final manuscript. The authors declare no competing interests.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funding AgencyGrant Number
Department of Energy (DOE)DE-SC0016469
Department of Energy (DOE)DE-SC0020373
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Simons FoundationUNSPECIFIED
Subject Keywords:Archaeal physiology; Microbial ecology; Water microbiology
Issue or Number:1
Record Number:CaltechAUTHORS:20210726-170837328
Persistent URL:
Official Citation:Yu, H., Skennerton, C.T., Chadwick, G.L. et al. Sulfate differentially stimulates but is not respired by diverse anaerobic methanotrophic archaea. ISME J 16, 168–177 (2022).
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:110007
Deposited By: Tony Diaz
Deposited On:26 Jul 2021 17:25
Last Modified:22 Dec 2021 19:07

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