Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

This article has been updated

Abstract

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.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Metabolic activities of methane-oxidizing consortia in sediment microcosms incubated with methane and different electron acceptors.
Fig. 2: Sulfate stimulates AQDS-coupled anaerobic oxidation of methane (AOM).
Fig. 3: Schematic showing two hypothetical scenarios of anaerobic oxidation of methane coupled to AQDS as the terminal electron acceptor by ANME-2 and SRB consortia.
Fig. 4: Paired FISH-nanoSIMS photomicrographs showing anabolic activity for two ANME-2 lineages and their syntrophic bacterial partners with different electron acceptors.
Fig. 5: Gene expression variation of two ANME-2 lineages and two syntrophic sulfate-reducing bacterial lineages with different electron acceptors after 9 days of incubation.
Fig. 6: Differential expression of key pathways by two ANME-2 lineages from comparative metatranscriptomics.

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.

Change history

  • 18 August 2021

    All instances of “AQDS + Sulfate” are changed to “AQDS+Sulfate” (without the two extra spaces.) In Figure 6 legend (x-axis) is italiczed.

References

  1. 1.

    Knittel K, Boetius A. Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol. 2009;63:311–34.

    CAS  Google Scholar 

  2. 2.

    Reeburgh WS. Oceanic methane biogeochemistry. Chem Rev. 2007;107:486–513.

    CAS  PubMed  Google Scholar 

  3. 3.

    Hatzenpichler R, Connon SA, Goudeau D, Malmstrom RR, Woyke T, Orphan VJ. Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia. Proc Natl Acad Sci USA. 2016;113:E4069–E4078.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Skennerton CT, Chourey K, Iyer R, Hettich RL, Tyson GW, Orphan VJ. Methane-fueled syntrophy through extracellular electron transfer: uncovering the genomic traits conserved within diverse bacterial partners of anaerobic methanotrophic archaea. mBio. 2017;8:e00530–e00517.

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci USA. 2002;99:7663–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Wegener G, Krukenberg V, Ruff SE, Kellermann MY, Knittel K. Metabolic capabilities of microorganisms involved in and associated with the anaerobic oxidation of methane. Front Microbiol. 2016;7:869.

    Google Scholar 

  7. 7.

    Metcalfe KS, Murali R, Mullin SW, Connon SA, Orphan VJ. Experimentally-validated correlation analysis reveals new anaerobic methane oxidation partnerships with consortium-level heterogeneity in diazotrophy. ISME J. 2020;15:377–96.

  8. 8.

    Krukenberg V, Riedel D, Gruber-Vodicka HR, Buttigieg PL, Tegetmeyer HE, Boetius A, et al. Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia. Environ Microbiol. 2018;20:1651–6.

  9. 9.

    Milucka J, Ferdelman TG, Polerecky L, Franzke D, Wegener G, Schmid M, et al. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature. 2012;491:541–6.

    CAS  PubMed  Google Scholar 

  10. 10.

    Schreiber L, Holler T, Knittel K, Meyerdierks A, Amann R. Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade. Environ Microbiol. 2010;12:2327–40.

    CAS  PubMed  Google Scholar 

  11. 11.

    Yu H, Susanti D, McGlynn SE, Skennerton CT, Chourey K, Iyer R, et al. Comparative genomics and proteomic analysis of assimilatory sulfate reduction pathways in anaerobic methanotrophic archaea. Front Microbiol. 2018;9:2917

  12. 12.

    Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science. 2016;351:703–7.

    CAS  PubMed  Google Scholar 

  13. 13.

    Wegener G, Krukenberg V, Riedel D, Tegetmeyer HE, Boetius A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature. 2015;526:587–90.

    CAS  PubMed  Google Scholar 

  14. 14.

    McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature. 2015;526:531–5.

    CAS  PubMed  Google Scholar 

  15. 15.

    Liu Y, Beer LL, Whitman WB. Sulfur metabolism in archaea reveals novel processes. Environ Microbiol. 2012;14:2632–44.

    CAS  PubMed  Google Scholar 

  16. 16.

    Perona JJ, Rauch BJ, Driggers CM. Sulfur assimilation and trafficking in methanogens. In: Rampelotto PH, editor. Molecular Mechanisms of Microbial Evolution. Cham: Springer International Publishing; 2018. p. 371–408.

  17. 17.

    White RH, Allen KD, Wegener G. Identification of a redox active thioquinoxalinol sulfate compound produced by an anaerobic methane-oxidizing microbial consortium. ACS Omega. 2019;4:22613–22.

  18. 18.

    Cline JD. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr. 1969;14:454–8.

    CAS  Google Scholar 

  19. 19.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.

    CAS  PubMed  Google Scholar 

  21. 21.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Mason OU, Case DH, Naehr TH, Lee RW, Thomas RB, Bailey JV, et al. Comparison of archaeal and bacterial diversity in methane seep carbonate nodules and host sediments, Eel River Basin and Hydrate Ridge, USA. Microb Ecol. 2015;70:766–84.

    CAS  PubMed  Google Scholar 

  23. 23.

    Laczny CC, Sternal T, Plugaru V, Gawron P, Atashpendar A, Margossian HH, et al. VizBin - an application for reference-independent visualization and human-augmented binning of metagenomic data. Microbiome. 2015;3:1.

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.

    Google Scholar 

  26. 26.

    Chen I-MA, Chu K, Palaniappan K, Pillay M, Ratner A, Huang J, et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res. 2019;47:D666–D677.

    CAS  PubMed  Google Scholar 

  27. 27.

    Agarwala R, Barrett T, Beck J, Benson DA, Bollin C, Bolton E, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2018;46:D8–D13.

    Google Scholar 

  28. 28.

    Saier MH, Reddy VS, Tsu BV, Ahmed MS, Li C, Moreno-Hagelsieb G. The Transporter Classification Database (TCDB): recent advances. Nucleic Acids Res. 2016;44:D372–D379.

    CAS  PubMed  Google Scholar 

  29. 29.

    Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009;25:1754–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Knittel K, Losekann T, Boetius A, Kort R, Amann R. Diversity and distribution of methanotrophic archaea at cold seeps. Appl Environ Microbiol. 2005;71:467–79.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Manz W, Eisenbrecher M, Neu TR, Szewzyk U. Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides. FEMS Microbiol Ecol. 1998;25:43–61.

    CAS  Google Scholar 

  32. 32.

    Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM. Look@NanoSIMS – a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. 2012;14:1009–23.

    CAS  PubMed  Google Scholar 

  33. 33.

    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Kopylova E, Noe L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.

    CAS  PubMed  Google Scholar 

  35. 35.

    Bray NL, Pimentel H, Melsted P, Pachter L. Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol. 2016;34:525–7.

    CAS  Google Scholar 

  36. 36.

    Pimentel H, Bray NL, Puente S, Melsted P, Pachter L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nat Methods. 2017;14:687–90.

    CAS  PubMed  Google Scholar 

  37. 37.

    McGee WA, Pimentel H, Pachter L, Wu JY. Compositional Data Analysis is necessary for simulating and analyzing RNA-Seq data. bioRxiv 2019;564955.

  38. 38.

    Rocha DJP, Santos CS, Pacheco LGC. Bacterial reference genes for gene expression studies by RT-qPCR: survey and analysis. Antonie van Leeuwenhoek. 2015;108:685–93.

    CAS  PubMed  Google Scholar 

  39. 39.

    Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.

    CAS  Google Scholar 

  41. 41.

    Rinke C, Chuvochina M, Mussig AJ, Chaumeil P-A, Davín AA, Waite DW, et al. A standardized archaeal taxonomy for the Genome Taxonomy Database. Nat Microbiol. 2021;6:946–59.

  42. 42.

    Orphan VJ, Turk KA, Green AM, House CH. Patterns of 15N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environ Microbiol. 2009;11:1777–91.

    CAS  PubMed  Google Scholar 

  43. 43.

    Girguis PR, Cozen AE, DeLong EF. Growth and population dynamics of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria in a continuous-flow bioreactor. Appl Environ Microbiol. 2005;71:3725–33.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Nauhaus K, Albrecht M, Elvert M, Boetius A, Widdel F. In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate. Environ Microbiol. 2007;9:187–96.

    CAS  PubMed  Google Scholar 

  45. 45.

    Meulepas RJW, Jagersma CG, Khadem AF, Buisman CJN, Stams AJM, Lens PNL. Effect of environmental conditions on sulfate reduction with methane as electron donor by an Eckernförde Bay enrichment. Environ Sci Technol. 2009;43:6553–9.

    CAS  PubMed  Google Scholar 

  46. 46.

    McGlynn SE. Energy metabolism during anaerobic methane oxidation in ANME archaea. Microbes Environ. 2017;32:5–13.

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Wang F-P, Zhang Y, Chen Y, He Y, Qi J, Hinrichs K-U, et al. Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways. ISME J. 2014;8:1069–78.

    CAS  PubMed  Google Scholar 

  48. 48.

    Meyerdierks A, Kube M, Kostadinov I, Teeling H, Glöckner FO, Reinhardt R, et al. Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. Environ Microbiol. 2010;12:422–39.

    CAS  PubMed  Google Scholar 

  49. 49.

    Cai C, Leu AO, Xie G-J, Guo J, Feng Y, Zhao J-X, et al. A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction. ISME J. 2018;1:285.

    Google Scholar 

  50. 50.

    Leu AO, Cai C, McIlroy SJ, Southam G, Orphan VJ, Yuan Z, et al. Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae. ISME J. 2020;14:1030–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Yanagawa K, Sunamura M, Lever MA, Morono Y, Hiruta A, Ishizaki O, et al. Niche separation of methanotrophic archaea (ANME-1 and-2) in methane-seep sediments of the eastern Japan Sea offshore Joetsu. Geomicrobiol J. 2011;28:118–29.

    CAS  Google Scholar 

  52. 52.

    Biddle JF, Cardman Z, Mendlovitz H, Albert DB, Lloyd KG, Boetius A, et al. Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments. ISME J. 2012;6:1018–31.

    CAS  PubMed  Google Scholar 

  53. 53.

    Holler T, Widdel F, Knittel K, Amann R, Kellermann MY, Hinrichs K-U, et al. Thermophilic anaerobic oxidation of methane by marine microbial consortia. ISME J. 2011;5:1946–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Roalkvam I, Jørgensen SL, Chen Y, Stokke R, Dahle H, Hocking WP, et al. New insight into stratification of anaerobic methanotrophs in cold seep sediments. FEMS Microbiol Ecol. 2011;78:233–43.

    CAS  PubMed  Google Scholar 

  55. 55.

    Timmers PHA, Widjaja-Greefkes HCA, Ramiro-Garcia J, Plugge CM, Stams AJM. Growth and activity of ANME clades with different sulfate and sulfide concentrations in the presence of methane. Front Microbiol. 2015;6:988.

  56. 56.

    Nauhaus K, Treude T, Boetius A, Krüger M. Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ Microbiol. 2005;7:98–106.

    CAS  PubMed  Google Scholar 

  57. 57.

    Green-Saxena A, Dekas AE, Dalleska NF, Orphan VJ. Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. ISME J. 2014;8:150–63.

    CAS  PubMed  Google Scholar 

  58. 58.

    Wegener G, Niemann H, Elvert M, Hinrichs K-U, Boetius A. Assimilation of methane and inorganic carbon by microbial communities mediating the anaerobic oxidation of methane. Environ Microbiol. 2008;10:2287–98.

    CAS  PubMed  Google Scholar 

  59. 59.

    Scherer P, Lippert H, Wolff G. Composition of the major elements and trace elements of 10 methanogenic bacteria determined by inductively coupled plasma emission spectrometry. Biol Trace Elem Res. 1983;5:149–63.

    CAS  PubMed  Google Scholar 

  60. 60.

    Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA. 2008;105:3968–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Kotloski NJ, Gralnick JA. Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. mBio 2013;4:e00553-12.

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Mevers E, Su L, Pishchany G, Baruch M, Cornejo J, Hobert E, et al. An elusive electron shuttle from a facultative anaerobe. eLife. 2019;8:e48054.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Weimer PJ, Odom JM, Cooling FB, Anderson AG. Anthraquinones as inhibitors of sulfide production from sulfate-reducing bacteria. US Patent 5385842. 1995.

  64. 64.

    Wang X, Cheng X, Ren Y, Xu G, Tang J. Humic analog AQDS can act as a selective inhibitor to enable anoxygenic photosynthetic bacteria to outcompete sulfate-reducing bacteria under microaerobic conditions. J Chem Technol Biotechnol. 2016;91:2103–10.

    CAS  Google Scholar 

  65. 65.

    Lee YH, Pavlostathis SG. Decolorization and toxicity of reactive anthraquinone textile dyes under methanogenic conditions. Water Res. 2004;38:1838–52.

    CAS  PubMed  Google Scholar 

  66. 66.

    Wu Y-W, Ouyang J, Xiao X-H, Gao W-Y, Liu Y. Antimicrobial properties and toxicity of anthraquinones by microcalorimetric bioassay. Chin J Chem. 2006;24:45–50.

    CAS  Google Scholar 

  67. 67.

    Novotný Č, Dias N, Kapanen A, Malachová K, Vándrovcová M, Itävaara M, et al. Comparative use of bacterial, algal and protozoan tests to study toxicity of azo- and anthraquinone dyes. Chemosphere. 2006;63:1436–42.

    PubMed  Google Scholar 

  68. 68.

    Shyu JBH, Lies DP, Newman DK. Protective role of tolC in efflux of the electron shuttle anthraquinone-2,6-disulfonate. J Bacteriol. 2002;184:1806–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP, Woodward JC. Humic substances as electron acceptors for microbial respiration. Nature. 1996;382:445–8.

    CAS  Google Scholar 

  70. 70.

    Newman DK, Kolter R. A role for excreted quinones in extracellular electron transfer. Nature. 2000;405:94–7.

    CAS  PubMed  Google Scholar 

  71. 71.

    Holmes DE, Ueki T, Tang H-Y, Zhou J, Smith JA, Chaput G, et al. A membrane-bound cytochrome enables Methanosarcina acetivorans to conserve energy from extracellular electron transfer. mBio. 2019;10:e00789–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Neuberger A, Du D, Luisi BF. Structure and mechanism of bacterial tripartite efflux pumps. Res Microbiol. 2018;169:401–13.

    CAS  PubMed  Google Scholar 

  73. 73.

    Crow A, Greene NP, Kaplan E, Koronakis V. Structure and mechanotransmission mechanism of the MacB ABC transporter superfamily. Proc Natl Acad Sci USA. 2017;114:12572–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Jiménez-Otero F, Chan CH, Bond DR. Identification of different putative outer membrane electron conduits necessary for Fe (III) citrate, Fe (III) oxide, Mn (IV) oxide, or electrode reduction by Geobacter sulfurreducens. J Bacteriol. 2018;200:3061.

    Google Scholar 

  75. 75.

    Plugge CM, Scholten JCM, Culley DE, Nie L, Brockman FJ, Zhang W. Global transcriptomics analysis of the Desulfovibrio vulgaris change from syntrophic growth with Methanosarcina barkeri to sulfidogenic metabolism. Microbiology. 2010;156:2746–56.

    CAS  PubMed  Google Scholar 

  76. 76.

    Walker CB, He Z, Yang ZK, Ringbauer JAJ, He Q, Zhou J, et al. The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J Bacteriol. 2009;191:5793–801.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Wenter R, Hütz K, Dibbern D, Li T, Reisinger V, Plöscher M, et al. Expression-based identification of genetic determinants of the bacterial symbiosis ‘Chlorochromatium aggregatum’. Environ Microbiol. 2010;12:2259–76.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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).

Author information

Affiliations

Authors

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.

Corresponding author

Correspondence to Victoria J. Orphan.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yu, H., Skennerton, C.T., Chadwick, G.L. et al. Sulfate differentially stimulates but is not respired by diverse anaerobic methanotrophic archaea. ISME J (2021). https://doi.org/10.1038/s41396-021-01047-0

Download citation

Search

Quick links