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Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink

Nature volume 443, pages 854–858 (2006)Cite this article

Abstract

Mud volcanism is an important natural source of the greenhouse gas methane to the hydrosphere and atmosphere1,2. Recent investigations show that the number of active submarine mud volcanoes might be much higher than anticipated (for example, see refs 3–5), and that gas emitted from deep-sea seeps might reach the upper mixed ocean6,7,8. Unfortunately, global methane emission from active submarine mud volcanoes cannot be quantified because their number and gas release are unknown9. It is also unclear how efficiently methane-oxidizing microorganisms remove methane. Here we investigate the methane-emitting Haakon Mosby Mud Volcano (HMMV, Barents Sea, 72° N, 14° 44′ E; 1,250 m water depth) to provide quantitative estimates of the in situ composition, distribution and activity of methanotrophs in relation to gas emission. The HMMV hosts three key communities: aerobic methanotrophic bacteria (Methylococcales), anaerobic methanotrophic archaea (ANME-2) thriving below siboglinid tubeworms, and a previously undescribed clade of archaea (ANME-3) associated with bacterial mats. We found that the upward flow of sulphate- and oxygen-free mud volcano fluids restricts the availability of these electron acceptors for methane oxidation, and hence the habitat range of methanotrophs. This mechanism limits the capacity of the microbial methane filter at active marine mud volcanoes to <40% of the total flux.

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Figure 1: The Haakon Mosby Mud Volcano.
Figure 2: A schematic diagram of the different microbial habitats at the HMMV.
Figure 3: Vertical distribution of methanotrophs in relation to environmental factors.

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Acknowledgements

The expeditions ‘AWI’ on RV L’Atalante in 2001 and ‘ARK XIX3b’ on RV Polarstern in 2003, both with ROV Victor 6000, were jointly planned, coordinated and carried out by the Alfred Wegener Institute for Polar and Marine Research in Bremerhaven, Germany, and the French Research Institute for Exploitation of the Sea (IFREMER) in Brest, France. We thank the captain and crew, the team of the ROV Victor 6000 and the shipboard scientific community of the RV Polarstern and L’Atalante for their help at sea. We thank S. Lüdeling, L. Baumann, V. Beier, I. Busse, F. Heinrich, G. Eickert, A. Nordhausen, J. Rogenhagen and R. Usbeck for technical assistance, C. Edy for help with georeferencing, U. Witte for providing the benthic lander technology, and S. Joye for comments on the manuscript. This is publication no. GEOTECH-235 of the R&D-Programme GEOTECHNOLOGIEN, Project MUMM, funded by the German Ministry of Education and Research (BMBF) and German Research Foundation (DFG). Author Contributions T.L., T.N., K.K. and R.A. carried out the 16S-rRNA-based analyses and microscopy, H.N. and M.E. the lipid biomarker work, A.B. and H.N. the rate measurements, D.B., E.S. and M.S. the microsensor and geochemical measurements, and M.K., M.S., A.B., H.N. and J.P.F. the geo- and video-graphical survey and experimental strategy. A.B., H.N. and D.B. wrote the manuscript text, and H.N., T.L. and K.K. wrote the supplements. All authors discussed the results and commented on the manuscript.

Author information

Author notes

  1. Marcus Elvert

    Present address: DFG Research Center Ocean Margins, University of Bremen, 28334, Bremen, Germany

  2. Thierry Nadalig

    Present address: UMR 7156 Université Louis-Pasteur/CNRS, Département Microorganismes, Génomes, Environnement, 67083, Strasbourg Cedex, France

  3. Helge Niemann and Tina Lösekann: These authors contributed equally to this work.

Authors and Affiliations

  1. Max Planck Institute for Marine Microbiology, 28359, Bremen, Germany

    Helge Niemann, Tina Lösekann, Dirk de Beer, Marcus Elvert, Katrin Knittel, Rudolf Amann & Antje Boetius

  2. Alfred Wegener Institute for Polar and Marine Research, 27515, Bremerhaven, Germany

    Helge Niemann, Eberhard J. Sauter, Michael Schlüter, Michael Klages & Antje Boetius

  3. Centre Ifremer de Brest, BP70, 29280, Plouzane, France

    Thierry Nadalig & Jean Paul Foucher

  4. International University Bremen, 28759, Bremen, Germany

    Antje Boetius

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Corresponding author

Correspondence to Antje Boetius.

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Competing interests

The nucleotide sequence data have been deposited in EMBL, GenBank and the DDBJ nucleotide sequence database under accession numbers AJ704650–AJ704653, AJ704631 and AM287206–AM287207. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file includes a section about the methane budget, the identity of the different methanotrophic communities as determined by 16S rDNA analysis, fluorescence in situ hybridisation (FISH) and lipid biomarker patterns. This file also contains Supplementary Methods and Supplementary Figure Legends. (DOC 60 kb)

Supplementary Figure 1

This file contains the phylogenetic tree of archaeal 16S rDNA sequences of Haakon Mosby mud volcano. (PDF 155 kb)

Supplementary Figure 2

This file contains the phylogenetic tree of bacterial 16S rDNA sequences of Haakon Mosby mud volcano. (PDF 164 kb)

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Niemann, H., Lösekann, T., de Beer, D. et al. Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature 443, 854–858 (2006). https://doi.org/10.1038/nature05227

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