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Symbiosis insights through metagenomic analysis of a microbial consortium

Nature volume 443, pages 950–955 (2006)Cite this article

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Abstract

Symbioses between bacteria and eukaryotes are ubiquitous, yet our understanding of the interactions driving these associations is hampered by our inability to cultivate most host-associated microbes. Here we use a metagenomic approach to describe four co-occurring symbionts from the marine oligochaete Olavius algarvensis, a worm lacking a mouth, gut and nephridia. Shotgun sequencing and metabolic pathway reconstruction revealed that the symbionts are sulphur-oxidizing and sulphate-reducing bacteria, all of which are capable of carbon fixation, thus providing the host with multiple sources of nutrition. Molecular evidence for the uptake and recycling of worm waste products by the symbionts suggests how the worm could eliminate its excretory system, an adaptation unique among annelid worms. We propose a model that describes how the versatile metabolism within this symbiotic consortium provides the host with an optimal energy supply as it shuttles between the upper oxic and lower anoxic coastal sediments that it inhabits.

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Figure 1: Clustering of the O. algarvensis symbiont scaffolds.
Figure 2: Reconstruction of the symbionts’ physiology.
Figure 3: Reconstruction of symbiont–host interactions.
Figure 4: Model for energy metabolism in the symbiosis.

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Change history

  • 26 October 2006

    In the advance online publication version of this Article, author Marcel Huntemann’s surname was misspelled as ‘Hunteman’. This was corrected on 26 October 2006.

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Acknowledgements

This work was performed under the auspices of the US Department of Energy’s Office of Science, Biological and Environmental Research Program, and supported by the University of California Lawrence Livermore National Laboratory, Lawrence Berkeley National Laboratory, and Los Alamos National Laboratory, and the Max Planck Society. We thank members of the Rubin, J. Bristow and P. Hugenholtz laboratories, as well as members of the Joint Genome Institute, for their contributions. We thank V. Markowitz, E. Dalin, N. Putnam, R. Sorek, T. Glavina del Rio, A. Salamov, A. Kobayashi and K. Kellaris for their assistance. At the Max Planck Institute for Marine Microbiology we thank S. Wetzel for technical assistance. We are grateful to C. Lott and the staff of the HYDRA field station at Elba for their generous support and help in sampling the worms.

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Authors and Affiliations

  1. DOE Joint Genome Institute, Walnut Creek, California, 94598, USA

    Tanja Woyke, Natalia N. Ivanova, Dario Boffelli, Iain J. Anderson, Kerrie W. Barry, Harris J. Shapiro, Ernest Szeto, Nikos C. Kyrpides & Edward M. Rubin

  2. Lawrence Berkeley National Laboratory, Genomics Division, Berkeley, California, 94720, USA

    Tanja Woyke, Dario Boffelli & Edward M. Rubin

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

    Hanno Teeling, Marcel Huntemann, Michael Richter, Frank Oliver Gloeckner, Marc Mussmann, Rudolf Amann, Claudia Bergin, Caroline Ruehland & Nicole Dubilier

  4. International University Bremen, 28759, Bremen, Germany

    Frank Oliver Gloeckner

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Correspondence to Edward M. Rubin or Nicole Dubilier.

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Competing interests

The assembled sequences from the Olavius symbionts’ metagenome have been deposited into the NCBI database under the project accession number AASZ00000000. The annotated Olavius symbionts’ bins were incorporated into the metagenomics version of the US Department of Energy Joint Genome Institute Integrated Microbial Genomes/M (IMG/M; http://img.jgi.doe.gov/m). Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Methods, Supplementary Figures 1–4, Supplementary Tables 1–6, Supplementary Discussion and additional references. In the original Supplementary Information posted on 17 September 2006, an incorrect weblink was given. The web link for the Java TreeView was posted as http://genetics.stanford.edu/~alok/TreeView/. The correct link is http://jtreeview.sourceforge.net/ (page 6, 2nd paragraph in the section “Binning”) This note was updated on 26 October 2006. (PDF 655 kb)

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Woyke, T., Teeling, H., Ivanova, N. et al. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950–955 (2006). https://doi.org/10.1038/nature05192

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