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Horizontal endosymbiont transmission in hydrothermal vent tubeworms

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.

References

  1. Cary, S. C., Warren, W., Anderson, E. & Giovannoni, S. Identification and localization of bacterial endosymbionts in hydrothermal vent taxa with symbiont-specific polymerase chain reaction amplification and in situ hybridization techniques. Mol. Mar. Biol. Biotechnol. 2, 51–62 (1993)

    CAS  PubMed  Google Scholar 

  2. Di Meo, C. A. et al. Genetic variation among endosymbionts of widely distributed vestimentiferan tubeworms. Appl. Environ. Microbiol. 66, 651–658 (2000)

    CAS  Article  Google Scholar 

  3. van Rhijn, P. & Vanderleyden, J. The Rhizobium–plant symbiosis. Microbiol. Rev. 59, 124–142 (1995)

    CAS  PubMed  PubMed Central  Google Scholar 

  4. McFall-Ngai, M. J. & Ruby, E. G. Developmental biology in marine invertebrate symbioses. Curr. Opin. Microbiol. 3, 603–607 (2000)

    CAS  Article  Google Scholar 

  5. Trench, R. K. Microalgal–invertebrate symbioses: a review. Endocytobiosis Cell Res. 9, 135–175 (1993)

    Google Scholar 

  6. Jones, M. L. & Gardiner, S. L. Evidence for a transient digestive tract in Vestimentifera. Proc. Biol. Soc. Wash. 101, 423–433 (1988)

    Google Scholar 

  7. Southward, E. C. Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): Implications for relationship between Vestimentifera and Pogonophora. J. Mar. Biol. Ass. UK 68, 465–487 (1988)

    Article  Google Scholar 

  8. Callsen-Cencic, P. & Flügel, H. J. Larval development and the formation of the gut Siboglinum poseidoni Flügel & Langhof (Pogonophora, Perviata), evidence of protostomian affinity. Sarsia 80, 73–89 (1995)

    Article  Google Scholar 

  9. Feldman, R. A., Black, M. B., Cary, C. S., Lutz, R. A. & Vrijenhoek, R. C. Molecular phylogenetics of bacterial endosymbionts and their vestimentiferan hosts. Mol. Mar. Biol. Biotechnol. 6, 268–277 (1997)

    CAS  PubMed  Google Scholar 

  10. Shank, T. M. et al. Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9°50′N, East Pacific Rise). Deep-sea Res. II 45, 465–515 (1998)

    ADS  Article  Google Scholar 

  11. Cordes, E. E., Arthur, M. A., Shea, K., Arvidson, R. S. & Fisher, C. R. Modeling the mutualistic interactions between tubeworms and microbial consortia. PLoS Biol. 3, e77 (2005)

    Article  Google Scholar 

  12. Rouse, G. W., Goffredi, S. K. & Vrijenhoek, R. C. Osedax: bone-eating marine worms with dwarf males. Science 305, 668–671 (2004)

    ADS  CAS  Article  Google Scholar 

  13. Southward, E. C., Schulze, A. & Gardiner, S. L. Pogonophora (Annelida): form and function. Hydrobiologia 535/536, 227–251 (2005)

    Article  Google Scholar 

  14. Bright, M. & Sorgo, A. Ultrastructural reinvestigation of the trophosome in adults of Riftia pachyptila (Annelida, Siboglinidae). Invertebr. Biol. 122, 345–366 (2003)

    Google Scholar 

  15. Heimler, H. Larvae. Microfauna Marina 4, 353–371 (1988)

    Google Scholar 

  16. Young, C. M., Vázquez, E., Metaxas, A. & Tyler, P. A. Embryology of vestimentiferan tube worms from deep-sea methane/sulphide seeps. Nature 381, 514–516 (1996)

    ADS  CAS  Article  Google Scholar 

  17. Marsh, A. G., Mullineaux, L. S., Young, C. M. & Manahan, D. T. Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents. Nature 411, 77–80 (2001)

    ADS  CAS  Article  Google Scholar 

  18. Vaux, D. Toward an understanding of the molecular mechanisms of physiological cell death. Proc. Natl Acad. Sci. USA 90, 786–789 (1993)

    ADS  CAS  Article  Google Scholar 

  19. Clarke, P. G. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.) 181, 195–213 (1990)

    CAS  Article  Google Scholar 

  20. Twomey, C. & McCarthy, J. V. Pathways of apoptosis and importance in development. J. Cell. Mol. Med. 9, 345–359 (2005)

    CAS  Article  Google Scholar 

  21. Zychlinsky, A. & Sansonetti, P. Apoptosis in bacterial pathogenesis. J. Clin. Invest. 100, 493–495 (1997)

    CAS  Article  Google Scholar 

  22. Molloy, A., Laochumroonvorapong, P. & Kaplan, G. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J. Exp. Med. 180, 1499–1509 (1994)

    CAS  Article  Google Scholar 

  23. Foster, J. S. & McFall-Ngai, M. J. Induction of apoptosis by cooperative bacteria in the morphogenesis of host epithelial tissues. Dev. Genes Evol. 208, 295–303 (1998)

    CAS  Article  Google Scholar 

  24. Mullineaux, L. S., Fisher, C. R., Peterson, C. H. & Schaeffer, S. W. Tubeworm succession at hydrothermal vents: use of biogenic cues to reduce habitat selection error? Oecologia 123, 275–284 (2000)

    ADS  CAS  Article  Google Scholar 

  25. Dubilier, N., Giere, O., Distel, D. L. & Cavanaugh, C. M. Characterization of chemoautotrophic symbionts in a gutless marine worm (Oligochaeta, Annelida) by phylogenetic 16S rRNA sequence analysis and in situ hybridization. Appl. Environ. Microbiol. 61, 2346–2350 (1995)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004)

    CAS  Article  Google Scholar 

  27. Cole, J. R. et al. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 33, D294–D296 (2005)

    CAS  Article  Google Scholar 

  28. Benson, D. A. et al. GenBank. Nucleic Acids Res. 27, 12–17 (1999)

    CAS  Article  Google Scholar 

  29. Daims, H., Brühl, A., Amann, R., Schleifer, K.-H. & Wagner, M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: Development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434–444 (1999)

    CAS  Article  Google Scholar 

  30. Manz, W., Amann, R., Ludwig, W., Wagner, M. & Schleifer, K. H. Phylogenetic oligonucleotide probes for the major subclasses of Proteobacteria: Problems and solutions. Syst. Appl. Microbiol. 15, 593–600 (1992)

    Article  Google Scholar 

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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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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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