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Horizontal endosymbiont transmission in hydrothermal vent tubeworms

Nature volume 441, pages 345–348 (2006)Cite this article

Abstract

Transmission of obligate bacterial symbionts between generations is vital for the survival of the host. Although the larvae of certain hydrothermal vent tubeworms (Vestimentifera, Siboglinidae) are symbiont-free and possess a transient digestive system, these structures are lost during development, resulting in adult animals that are nutritionally dependent on their bacterial symbionts. Thus, each generation of tubeworms must be newly colonized with its specific symbiont1,2. Here we present a model for tubeworm symbiont acquisition and the development of the symbiont-housing organ, the trophosome. Our data indicate that the bacterial symbionts colonize the developing tube of the settled larvae and enter the host through the skin, a process that continues through the early juvenile stages during which the trophosome is established from mesodermal tissue. In later juvenile stages we observed massive apoptosis of host epidermis, muscles and undifferentiated mesodermal tissue, which was coincident with the cessation of the colonization process. Characterizing the symbiont transmission process in this finely tuned mutualistic symbiosis provides another model of symbiont acquisition and additional insights into underlying mechanisms common to both pathogenic infections and beneficial host–symbiont interactions.

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Figure 1: Tubeworm artificial settlement cubes (TASCs).
Figure 2: Symbiont acquisition and early development of recently settled vestimentiferans.
Figure 3: Infection and trophosome development in vestimentiferans.

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Acknowledgements

We thank the captain and crew of the RV Atlantis and the crew of the DSV Alvin for their continuous support; H. Grillitsch for the schematic illustrations; P. Gahleitner for sectioning; W. Klepal for the EM support; S. C. Cary, C. M. Cavanaugh (grants from NOAA and NSF), J. J. Childress and L. S. Mullineaux for their hospitality on cruises; and C. M. Cavanaugh and M. Horn for their comments on the manuscript. This work was supported by grants from the Austrian Science Foundation and the Austrian Academy of Science to M.B., by a grant from the Faculty of Life Sciences, University of Vienna to A.D.N., and a grant from the US National Science Foundation to C.R.F. Author Contributions M.B. was the project leader, designed the TASCs and performed the t.e.m. work; A.D.N. performed the molecular work and was responsible for the data collection; and A.D.N., C.R.F. and M.B. performed the field work and wrote the paper.

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Authors and Affiliations

  1. Department of Marine Biology, University of Vienna, Vienna, Althanstrasse 14, A-1090, Austria

    Andrea D. Nussbaumer & Monika Bright

  2. Department of Biology, Pennsylvania State University, 208 Mueller Laboratory, University Park, Pennsylvania, 16802, USA

    Charles R. Fisher

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  1. Andrea D. Nussbaumer
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Correspondence to Monika Bright.

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Nussbaumer, A., Fisher, C. & Bright, M. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441, 345–348 (2006). https://doi.org/10.1038/nature04793

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