Volume 11, Issue 5 p. 1150-1167

Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels

Frank U. Zielinski

Frank U. Zielinski

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

Helmholtz Centre for Environmental Research – UFZ, Department of Environmental Microbiology, Permoser Str. 15, 04318 Leipzig, Germany.

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Annelie Pernthaler

Annelie Pernthaler

California Institute of Technology, Division of Geological and Planetary Sciences, 1200 E California Blvd, Pasadena, CA 91125, USA.

Present address: Helmholtz Centre for Environmental Research – UFZ, Department of Environmental Microbiology, Permoser Str. 15, 04318 Leipzig, Germany.

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Sébastien Duperron

Sébastien Duperron

Université Pierre et Marie Curie, Équipe Adaptation aux Milieux Extrêmes, 7 Quai St Bernard, 75005 Paris, France.

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Luciana Raggi

Luciana Raggi

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

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Olav Giere

Olav Giere

University of Hamburg, Biozentrum Grindel und Zoologisches Museum, Martin-Luther-King Platz 3, 20146 Hamburg, Germany.

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Christian Borowski

Christian Borowski

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

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Nicole Dubilier

Corresponding Author

Nicole Dubilier

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

*E-mail [email protected]; Tel. (+49) 421 2028 932; Fax (+49) 421 2028 580.Search for more papers by this author
First published: 24 April 2009
Citations: 61

Summary

Many parasitic bacteria live in the cytoplasm of multicellular animals, but only a few are known to regularly invade their nuclei. In this study, we describe the novel bacterial parasite “Candidatus Endonucleobacter bathymodioli” that invades the nuclei of deep-sea bathymodiolin mussels from hydrothermal vents and cold seeps. Bathymodiolin mussels are well known for their symbiotic associations with sulfur- and methane-oxidizing bacteria. In contrast, the parasitic bacteria of vent and seep animals have received little attention despite their potential importance for deep-sea ecosystems. We first discovered the intranuclear parasite “Ca. E. bathymodioli” in Bathymodiolus puteoserpentis from the Logatchev hydrothermal vent field on the Mid-Atlantic Ridge. Using primers and probes specific to “Ca. E. bathymodioli” we found this intranuclear parasite in at least six other bathymodiolin species from vents and seeps around the world. Fluorescence in situ hybridization and transmission electron microscopy analyses of the developmental cycle of “Ca. E. bathymodioli” showed that the infection of a nucleus begins with a single rod-shaped bacterium which grows to an unseptated filament of up to 20 μm length and then divides repeatedly until the nucleus is filled with up to 80 000 bacteria. The greatly swollen nucleus destroys its host cell and the bacteria are released after the nuclear membrane bursts. Intriguingly, the only nuclei that were never infected by “Ca. E. bathymodioli” were those of the gill bacteriocytes. These cells contain the symbiotic sulfur- and methane-oxidizing bacteria, suggesting that the mussel symbionts can protect their host nuclei against the parasite. Phylogenetic analyses showed that the “Ca. E. bathymodioli” belongs to a monophyletic clade of Gammaproteobacteria associated with marine metazoans as diverse as sponges, corals, bivalves, gastropods, echinoderms, ascidians and fish. We hypothesize that many of the sequences from this clade originated from intranuclear bacteria, and that these are widespread in marine invertebrates.