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Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms

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Abstract

Deep-sea vestimentiferan tubeworms, which live in symbiosis with bacteria, exhibit different life strategies according to their habitat. At unstable and relatively short-lived hydrothermal vents, they grow extremely fast, whereas their close relatives at stable and long-persisting cold seeps grow slowly and live up to 300 years. Growth and age differences are thought to occur because of ecological and physiological adaptations. However, the underlying mechanisms of cell proliferation and death, which are closely linked to homeostasis, growth, and longevity, are unknown. Here, we show by immunohistochemical and ultrastructural cell cycle analyses that cell proliferation activities of the two species studied are higher than in any other characterized invertebrate, being only comparable with tumor and wound-healing processes. The slow growth in Lamellibrachia luymesi from cold seeps results from balanced activities of proliferation and apoptosis in the epidermis. In contrast, Riftia pachyptila from hydrothermal vents grows fast because apoptosis is down-regulated in this tissue. The symbiont-housing organ, the trophosome, exhibits a complex cell cycle and terminal differentiation pattern in both species, and growth is regulated by proliferation. These mechanisms have similarities to the up- and down-regulation of proliferation or apoptosis in various types of tumor, although they occur in healthy animals in this study, thus providing significant insights into the underlying mechanisms of growth and longevity.

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Acknowledgements

We thank the captains and crews of the R/V Atlantis and DSV Alvin and of the R/V Johnson Seward and DSV Johnson Sea Link II for their continuous support. Technical assistance from S. Adam, U. Hörmann, and D. Gruber, TEM support from W. Klepal (Department of Cell Imaging and Ultrastructure Research, University of Vienna, Austria), and help from E. Cordes and S. Dattagupta are gratefully acknowledged. We are also grateful to C.R. Fisher and S. Katz for critically reading an earlier draft of this manuscript and for their valuable input.

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

    Bettina Pflugfelder & Monika Bright

  2. College of Marine and Earth Studies, University of Delaware, 700 Pilottown Road, Lewes, DE 19958, USA

    S. Craig Cary

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  2. S. Craig Cary
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  3. Monika Bright
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Correspondence to Bettina Pflugfelder.

Additional information

Financial support was provided by the Austrian Science Foundation (FWF; grants to M.B.), a DOC scholarship from the Austrian Academy of Science (to B.P.), and grants from the US National Science Foundation (to C.R. Fisher).

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Pflugfelder, B., Cary, S.C. & Bright, M. Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms. Cell Tissue Res 337, 149–165 (2009). https://doi.org/10.1007/s00441-009-0811-0

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  • DOI: https://doi.org/10.1007/s00441-009-0811-0

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