Volume 10, Issue 12 p. 3237-3254

Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic Cold Seep (Haakon Mosby Mud Volcano, Barents Sea)

Tina Lösekann

Tina Lösekann

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

Present addresses: Stanford University School of Medicine, 299 Campus Drive, Stanford, CA 94305, USA;

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Alberto Robador

Alberto Robador

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

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Helge Niemann

Helge Niemann

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

Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, Bremerhaven 27515, Germany.

Institute for Environmental Geoscience, University of Basel, Bernoullistrasse 30, 4056 Basel, Switzerland.

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Katrin Knittel

Katrin Knittel

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

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Antje Boetius

Antje Boetius

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

Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, Bremerhaven 27515, Germany.

Jacobs University Bremen, Research II, Campus Ring 1, Bremen 28759, Germany.

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Nicole Dubilier

Corresponding Author

Nicole Dubilier

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

*E-mail [email protected]; Tel. (+49) 421 2028 932; Fax (+49) 421 2028 580. Search for more papers by this author
First published: 07 November 2008
Citations: 101

Summary

Siboglinid tubeworms do not have a mouth or gut and live in obligate associations with bacterial endosymbionts. Little is currently known about the phylogeny of frenulate and moniliferan siboglinids and their symbionts. In this study, we investigated the symbioses of two co-occurring siboglinid species from a methane emitting mud volcano in the Arctic Ocean (Haakon Mosby Mud Volcano, HMMV): Oligobrachia haakonmosbiensis (Frenulata) and Sclerolinum contortum (Monilifera). Comparative sequence analysis of the host-specific 18S and the symbiont-specific 16S rRNA genes of S. contortum showed that the close phylogenetic relationship of this host to vestimentiferan siboglinids was mirrored in the close relationship of its symbionts to the sulfur-oxidizing gammaproteobacterial symbionts of vestimentiferans. A similar congruence between host and symbiont phylogeny was observed in O. haakonmosbiensis: both this host and its symbionts were most closely related to the frenulate siboglinid O. mashikoi and its gammaproteobacterial symbiont. The symbiont sequences from O. haakonmosbiensis and O. mashikoi formed a clade unaffiliated with known methane- or sulfur-oxidizing bacteria. Fluorescence in situ hybridization indicated that the dominant bacterial phylotypes originated from endosymbionts residing inside the host trophosome. In both S. contortum and O. haakonmosbiensis, characteristic genes for autotrophy (cbbLM) and sulfur oxidation (aprA) were present, while genes diagnostic for methanotrophy were not detected. The molecular data suggest that both HMMV tubeworm species harbour chemoautotrophic sulfur-oxidizing symbionts. In S. contortum, average stable carbon isotope values of fatty acids and cholesterol of −43‰ were highly negative for a sulfur oxidizing symbiosis, but can be explained by a 13C-depleted CO2 source at HMMV. In O. haakonmosbiensis, stable carbon isotope values of fatty acids and cholesterol of −70‰ are difficult to reconcile with our current knowledge of isotope signatures for chemoautotrophic processes.