Sponge-associated microorganisms: evolution, ecology, and biotechnological potential.
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Journal: 2007/August - Microbiology and Molecular Biology Reviews
ISSN: 1092-2172
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Marine sponges often contain diverse and abundant microbial communities, including bacteria, archaea, microalgae, and fungi. In some cases, these microbial associates comprise as much as 40% of the sponge volume and can contribute significantly to host metabolism (e.g., via photosynthesis or nitrogen fixation). We review in detail the diversity of microbes associated with sponges, including extensive 16S rRNA-based phylogenetic analyses which support the previously suggested existence of a sponge-specific microbiota. These analyses provide a suitable vantage point from which to consider the potential evolutionary and ecological ramifications of these widespread, sponge-specific microorganisms. Subsequently, we examine the ecology of sponge-microbe associations, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution. The ecological and evolutionary importance of sponge-microbe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in at least some cases, the compounds are of microbial rather than sponge origin. We review the status of this important field, outlining the various approaches (e.g., cultivation, cell separation, and metagenomics) which have been employed to access the chemical wealth of sponge-microbe associations.
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Microbiol Mol Biol Rev 71(2): 295-347
PMID: 17554047

Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential<sup><a href="#fn1" rid="fn1" class=" fn">†</a></sup>

Department of Microbial Ecology, University of Vienna, Althanstr. 14, A-1090 Vienna, Austria
Corresponding author. Present address: School of Biological Sciences, Faculty of Science, The University of Auckland, Private Bag 92019, Auckland, New Zealand. Phone: 64 9 373 7599, ext. 82280. Fax: 64 9 373 7416. E-mail: zn.ca.dnalkcua@rolyat.wm
Copyright © 2007, American Society for Microbiology

Abstract

Summary: Marine sponges often contain diverse and abundant microbial communities, including bacteria, archaea, microalgae, and fungi. In some cases, these microbial associates comprise as much as 40% of the sponge volume and can contribute significantly to host metabolism (e.g., via photosynthesis or nitrogen fixation). We review in detail the diversity of microbes associated with sponges, including extensive 16S rRNA-based phylogenetic analyses which support the previously suggested existence of a sponge-specific microbiota. These analyses provide a suitable vantage point from which to consider the potential evolutionary and ecological ramifications of these widespread, sponge-specific microorganisms. Subsequently, we examine the ecology of sponge-microbe associations, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution. The ecological and evolutionary importance of sponge-microbe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in at least some cases, the compounds are of microbial rather than sponge origin. We review the status of this important field, outlining the various approaches (e.g., cultivation, cell separation, and metagenomics) which have been employed to access the chemical wealth of sponge-microbe associations.

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Acknowledgments

We gratefully acknowledge the constructive comments on various sections of the manuscript provided by Rocky de Nys, Friederike Hoffmann, Peter Schupp, Bob Thacker, and Torsten Thomas. The ideas expressed in this article also benefitted from discussions and/or collaborations with Rocky de Nys, Piers Ettinger-Epstein, Ute Hentschel, Matthias Horn, Staffan Kjelleberg, Peter Schupp, Peter Steinberg, and Steve Whalan. We thank Ute Hentschel for providing samples of Plakortis sp. and Agelas dilatata and Megan Huggett and Sharon Longford for collection of Antho chartacea. Ivica Letunic and Peer Bork are thanked for their help with the phylogenetic tree displayed in Fig. ​Fig.4,4, while we are indebted to Rocky de Nys for his compilation of the chemical structures comprising Fig. ​Fig.2121 to ​to23.23. Jörg Ott kindly facilitated access to some of the sponge photographs in Fig. ​Fig.3.3. We thank Kayley Usher, Russell Hill, and Nicole Webster for their permission to reproduce published figures.

The research of M.W.T. was funded in part by a grant from the German Federal Ministry for Education and Research (Biolog II) to M.W. D.S. received a DOC-FORTE stipend from the Austrian Academy of Sciences. M.W. thanks the University of Vienna for financial support in the framework of the faculty focus “Symbiosis” and the university research focus “Symbiosis Research and Molecular Principles of Recognition.”

Acknowledgments

Footnotes

Supplemental material for this article may be found at http://mmbr.asm.org/.

Footnotes

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