Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments

Authors

  • Caroline Ruehland,

    1. Symbiosis Group, Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany.
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    • Authors contributed in equal parts to this publication.

  • Anna Blazejak,

    1. Symbiosis Group, Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany.
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    • Authors contributed in equal parts to this publication.

  • Christian Lott,

    1. Symbiosis Group, Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany.
    2. HYDRA Institute for Marine Sciences, Elba Field Station, Via del Forno 80, I-57034 Campo nell'Elba (LI), Italy.
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  • Alexander Loy,

    1. Department of Microbial Ecology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.
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  • Christer Erséus,

    1. Department of Zoology, University of Gothenburg, Box 463, SE-40530, Göteborg, Sweden.
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  • Nicole Dubilier

    Corresponding author
    1. Symbiosis Group, Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany.
      *E-mail ndubilie@mpi-bremen.de; Tel. (+49) 4212028 932; Fax (+49) 4212028 580.
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*E-mail ndubilie@mpi-bremen.de; Tel. (+49) 4212028 932; Fax (+49) 4212028 580.

Summary

Gutless oligochaete worms are found worldwide in the pore waters of marine sediments and live in symbiosis with chemoautotrophic sulfur-oxidizing bacteria. In the Mediterranean, two species of gutless oligochaete worms, Olavius algarvensis and O. ilvae, co-occur in sediments around sea grass beds. These sediments have extremely low sulfide concentrations (< 1 μM), raising the question if O. ilvae, as shown previously for O. algarvensis, also harbours sulfate-reducing symbionts that provide its sulfur-oxidizing symbionts with reduced sulfur compounds. In this study, we used fluorescence in situ hybridization (FISH) and comparative sequence analysis of genes for 16S rRNA, sulfur metabolism (aprA and dsrAB), and autotrophic carbon fixation (cbbL) to examine the microbial community of O. ilvae and re-examine the O. algarvensis symbiosis. In addition to the four previously described symbionts of O. algarvensis, in this study a fifth symbiont belonging to the Spirochaetes was found in these hosts. The symbiotic community of O. ilvae was similar to that of O. algarvensis and also included two gammaproteobacterial sulfur oxidizers and two deltaproteobacterial sulfate reducers, but not a spirochete. The phylogenetic and metabolic similarity of the symbiotic communities in these two co-occurring host species that are not closely related to each other indicates that syntrophic sulfur cycling provides a strong selective advantage to these worms in their sulfide-poor environment.

Ancillary