Regulation of polyp-to-jellyfish transition in Aurelia aurita

Björn Fuchs; Wei Wang; Simon Graspeuntner; Yizhu Li; Santiago Insua; Eva Maria Herbst; Philipp Dirksen; Anna Marei Böhm; Georg Hemmrich; Felix Sommer; Tomislav Domazet-Lošo; Ulrich C. Klostermeier; Friederike Anton-Erxleben; Philip Rosenstiel; Thomas C G Bosch; Konstantin Khalturin

doi:10.1016/j.cub.2013.12.003

Regulation of polyp-to-jellyfish transition in Aurelia aurita

Björn Fuchs, Wei Wang, Simon Graspeuntner, Yizhu Li, Santiago Insua, Eva Maria Herbst, Philipp Dirksen, Anna Marei Böhm, Georg Hemmrich, Felix Sommer, Tomislav Domazet-Lošo, Ulrich C. Klostermeier, Friederike Anton-Erxleben, Philip Rosenstiel, Thomas C G Bosch, Konstantin Khalturin^*

^*Corresponding author for this work

Clinic of Infectious Diseases and Microbiology

167 Citations (Scopus)

Abstract

Background The life cycle of scyphozoan cnidarians alternates between sessile asexual polyps and pelagic medusa. Transition from one life form to another is triggered by environmental signals, but the molecular cascades involved in the drastic morphological and physiological changes remain unknown. Results We show in the moon jelly Aurelia aurita that the molecular machinery controlling transition of the sessile polyp into a free-swimming jellyfish consists of two parts. One is conserved and relies on retinoic acid signaling. The second, novel part is based on secreted proteins that are strongly upregulated prior to metamorphosis in response to the seasonal temperature changes. One of these proteins functions as a temperature-sensitive "timer" and encodes the precursor of the strobilation hormone of Aurelia. Conclusions Our findings uncover the molecule framework controlling the polyp-to-jellyfish transition in a basal metazoan and provide insights into the evolution of complex life cycles in the animal kingdom.

Original language	English
Journal	Current Biology
Volume	24
Issue number	3
Pages (from-to)	263-273
Number of pages	11
ISSN	0960-9822
DOIs	https://doi.org/10.1016/j.cub.2013.12.003
Publication status	Published - 03.02.2014

Funding

We thank Antje Thomas for the help with microscopy, Thomas Walter for constructing jellyfish facility, and Elke Blohm-Sievers for the help with microarrays. Tatiana Shaposhnikova and Gerhard Jarms provided the animal lines. Ivan Gluzdikov, Ludmila Kuznetzova, and Rainer Herges gave important advice in organic chemistry. Ulrich Technau, Johanna Kraus, and David Fredman shared with us highly valuable nonpublished Clytia and Aurelia data. We are grateful to Diethard Tautz for the opportunity to use research facilities at MPI for Evolutionary Biology in Plön. K.K. thanks Oleg Chaga, Ivan Tikhomirov, and Ivan Rudsky for inspiring discussions. Our work was financially supported by DFG Clusters “Future Ocean” and “Inflammation at Interfaces.” K.K. is supported by RFBR (РФФИ) grant 13-04-01795. W.W. was supported by China Scholarship Council.

Research Areas and Centers

Academic Focus: Center for Infection and Inflammation Research (ZIEL)

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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Fuchs, B., Wang, W., Graspeuntner, S., Li, Y., Insua, S., Herbst, E. M., Dirksen, P., Böhm, A. M., Hemmrich, G., Sommer, F., Domazet-Lošo, T., Klostermeier, U. C., Anton-Erxleben, F., Rosenstiel, P., Bosch, T. C. G., & Khalturin, K. (2014). Regulation of polyp-to-jellyfish transition in Aurelia aurita. Current Biology, 24(3), 263-273. https://doi.org/10.1016/j.cub.2013.12.003

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abstract = "Background The life cycle of scyphozoan cnidarians alternates between sessile asexual polyps and pelagic medusa. Transition from one life form to another is triggered by environmental signals, but the molecular cascades involved in the drastic morphological and physiological changes remain unknown. Results We show in the moon jelly Aurelia aurita that the molecular machinery controlling transition of the sessile polyp into a free-swimming jellyfish consists of two parts. One is conserved and relies on retinoic acid signaling. The second, novel part is based on secreted proteins that are strongly upregulated prior to metamorphosis in response to the seasonal temperature changes. One of these proteins functions as a temperature-sensitive {"}timer{"} and encodes the precursor of the strobilation hormone of Aurelia. Conclusions Our findings uncover the molecule framework controlling the polyp-to-jellyfish transition in a basal metazoan and provide insights into the evolution of complex life cycles in the animal kingdom.",

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doi = "10.1016/j.cub.2013.12.003",

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AU - Fuchs, Björn

AU - Wang, Wei

AU - Graspeuntner, Simon

AU - Li, Yizhu

AU - Insua, Santiago

AU - Herbst, Eva Maria

AU - Dirksen, Philipp

AU - Böhm, Anna Marei

AU - Hemmrich, Georg

AU - Sommer, Felix

AU - Domazet-Lošo, Tomislav

AU - Klostermeier, Ulrich C.

AU - Anton-Erxleben, Friederike

AU - Rosenstiel, Philip

AU - Bosch, Thomas C G

AU - Khalturin, Konstantin

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N2 - Background The life cycle of scyphozoan cnidarians alternates between sessile asexual polyps and pelagic medusa. Transition from one life form to another is triggered by environmental signals, but the molecular cascades involved in the drastic morphological and physiological changes remain unknown. Results We show in the moon jelly Aurelia aurita that the molecular machinery controlling transition of the sessile polyp into a free-swimming jellyfish consists of two parts. One is conserved and relies on retinoic acid signaling. The second, novel part is based on secreted proteins that are strongly upregulated prior to metamorphosis in response to the seasonal temperature changes. One of these proteins functions as a temperature-sensitive "timer" and encodes the precursor of the strobilation hormone of Aurelia. Conclusions Our findings uncover the molecule framework controlling the polyp-to-jellyfish transition in a basal metazoan and provide insights into the evolution of complex life cycles in the animal kingdom.

AB - Background The life cycle of scyphozoan cnidarians alternates between sessile asexual polyps and pelagic medusa. Transition from one life form to another is triggered by environmental signals, but the molecular cascades involved in the drastic morphological and physiological changes remain unknown. Results We show in the moon jelly Aurelia aurita that the molecular machinery controlling transition of the sessile polyp into a free-swimming jellyfish consists of two parts. One is conserved and relies on retinoic acid signaling. The second, novel part is based on secreted proteins that are strongly upregulated prior to metamorphosis in response to the seasonal temperature changes. One of these proteins functions as a temperature-sensitive "timer" and encodes the precursor of the strobilation hormone of Aurelia. Conclusions Our findings uncover the molecule framework controlling the polyp-to-jellyfish transition in a basal metazoan and provide insights into the evolution of complex life cycles in the animal kingdom.

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Regulation of polyp-to-jellyfish transition in Aurelia aurita

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UN SDGs

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