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Indoles can induce strobilation in aposymbiotic Cassiopea andromeda polyps but are associated with developmental abnormalities

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Abstract

The upside-down jellyfish Cassiopea has become a model organism for the study of symbiosis between dinoflagellates and cnidarian hosts. Most previous studies have indicated that the presence of symbiotic zooxanthellae is a key requirement for strobilation in Cassiopea. Indole compounds have been shown to induce strobilation in many scyphozoans, including symbiotic Cassiopea xamachana. To determine if indoles could induce aposymbiotic Cassiopea polyp strobilation, we acquired algal-free Cassiopea andromeda polyps and used three indoles (indomethacin, 2-methyl indole, and 5-methoxy-2-methyl indole) to induce metamorphosis by applying single doses within a range of 0.005–100 μM. Analysis showed that indoles successfully induced aposymbiotic polyp strobilation and that the induction effects were compound- and dose-dependent. 5-Methoxy-2-methyl indole and 2-methyl indole were significantly more effective than indomethacin (P < 0.001). Data showed that it took 3 to 9 days for 5-methoxy-2-methyl indole or 2-methyl indole to induce strobilation and that 25 μM of 2-methyl indole was the most effective inducer of strobilation in algae-free C. andromeda polyps. Indole-induced strobilation was associated with several developmental abnormalities, including failed or retarded regeneration of residual polyps after strobilation, a reduction in the size of ephyrae, and abnormal morphology of the ephyrae.

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References

  • Astorga, D., J. Ruiz & L. Prieto, 2012. Ecological aspects of early life stages of Cotylorhiza tuberculata (Scyphozoa: Rhizostomae) affecting its pelagic population success, Jellyfish Blooms IV Springer, Dordrecht: 141–155.

    Chapter  Google Scholar 

  • Banaszak, A. T. & R. K. Trench, 1995. Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses. II. The synthesis of mycosporine-like amino acids in response to exposure to UV in Anthopleura elegantissima and Cassiopeia xamachana. Journal of Experimental Marine Biology and Ecology 194(2): 233–250.

    Article  CAS  Google Scholar 

  • Bayha, K. M., M. N. Dawson, A. G. Collins, M. S. Barbeitos & S. H. Haddock, 2010. Evolutionary relationships among scyphozoan jellyfish families based on complete taxon sampling and phylogenetic analyses of 18S and 28S ribosomal DNA. Integrative and Comparative Biology 50(3): 436–455.

    Article  CAS  Google Scholar 

  • Berking, S., N. Czech, M. Gerharz, K. Herrmann, U. Hoffmann, H. Raifer, G. Sekul, B. Siefker, A. Sommerei & F. Vedder, 2005. A newly discovered oxidant defence system and its involvement in the development of Aurelia aurita (Scyphozoa, Cnidaria): reactive oxygen species and elemental iodine control medusa formation. International Journal of Developmental Biology 49(8): 969–976.

    Article  CAS  Google Scholar 

  • Cabrales-Arellano, P., T. Islas-Flores, P. E. Thome & M. A. Villanueva, 2017. Indomethacin reproducibly induces metamorphosis in Cassiopea xamachana scyphistomae. PeerJ 5: e2979.

    Article  Google Scholar 

  • Calder, D. R., 1973. Laboratory observations on the life history of Rhopilema verrilli (Scyphozoa: Rhizostomeae). Marine Biology 21(2): 109–114.

    Article  Google Scholar 

  • Coffroth, M. A. & S. R. Santos, 2005. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156(1): 19–34.

    Article  CAS  Google Scholar 

  • Fitt, W., 1984. The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and molluscs with zooxanthellae. Marine Biology 81(1): 9–17.

    Article  Google Scholar 

  • Fitt, W. K., D. K. Hofmann, M. Wolk & M. Rahat, 1987. Requirement of exogenous inducers for metamorphosis of axenic larvae and buds of Cassiopea andromeda (Cnidaria: Scyphozoa). Marine Biology 94(3): 415–422.

    Article  CAS  Google Scholar 

  • Fuchs, B., W. Wang, S. Graspeuntner, Y. Li, S. Insua, E. M. Herbst, P. Dirksen, A. M. Bohm, G. Hemmrich, F. Sommer, T. Domazet-Loso, U. C. Klostermeier, F. Anton-Erxleben, P. Rosenstiel, T. C. Bosch & K. Khalturin, 2014. Regulation of polyp-to-jellyfish transition in Aurelia aurita. Current Biology 24(3): 263–273.

    Article  CAS  Google Scholar 

  • Gohar, H. A. F. & A. M. Eisawy, 1960. The development of Cassiopea andromeda. Publication of the Marine Biological Station, Ghardaqa, Red Sea 11: 147–190.

    Google Scholar 

  • Heins, A., T. Glatzel & S. Holst, 2015. Revised descriptions of the nematocysts and the asexual reproduction modes of the scyphozoan jellyfish Cassiopea andromeda (Forskål, 1775). Zoomorphology 134(3): 351–366.

    Article  Google Scholar 

  • Helm, R. R., 2018. Evolution and development of scyphozoan jellyfish. Biological Reviews of the Cambridge Philosophical Society 93(2): 1228–1250.

    Article  Google Scholar 

  • Helm, R. R. & C. W. Dunn, 2017. Indoles induce metamorphosis in a broad diversity of jellyfish, but not in a crown jelly (Coronatae). PLoS ONE 12(12): e0188601.

    Article  Google Scholar 

  • Hofmann, D. K. & B. P. Kremer, 1981. Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): significance of endosymbiotic dinoflagellates. Marine Biology 65(1): 25–33.

    Article  CAS  Google Scholar 

  • Hofmann, D. K., R. Neumann & K. Henne, 1978. Strobilation, budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa). Marine Biology 47(2): 161–176.

    Article  Google Scholar 

  • Hofmann, D. K., W. K. Fitt & J. Fleck, 1996. Checkpoints in the life-cycle of Cassiopea spp.: Control of metagenesis and metamorphosis in a tropical jellyfish. International Journal of Developmental Biology 40(1): 331–338.

    CAS  PubMed  Google Scholar 

  • Kikinger, R., 1992. Cotylorhiza tuberculata (Cnidaria: Scyphozoa)-life history of a stationary population. Marine Ecology 13(4): 333–362.

    Article  Google Scholar 

  • Kroiher, M., B. Siefker & S. Berking, 2000. Induction of segmentation in polyps of Aurelia aurita (Scyphozoa, Cnidaria) into medusae and formation of mirror-image medusa anlagen. Intjdevbiol 44(5): 485.

    CAS  Google Scholar 

  • Kuniyoshi, H., I. Okumura, R. Kuroda, N. Tsujita, K. Arakawa, J. Shoji, T. Saito & H. Osada, 2012. Indomethacin induction of metamorphosis from the asexual stage to sexual stage in the moon jellyfish Aurelia Aurita. Bioscience Biotechnology and Biochemistry 76(7): 1397–1400.

    Article  CAS  Google Scholar 

  • Lampert, K. P., 2016. Cassiopea and Its Zooxanthellae 26. In The Cnidaria, Past, Present and Future: The World of Medusa and Her Sisters. Springer, Cham: 415–423.

    Chapter  Google Scholar 

  • Ludwig, F. D., 1969. Die zooxanthellen bei Cassiopea andromeda Eschscholtz 1829 (Polyp-Stadium) und ihre Bedeutung für die strobilation. Verlag nicht ermittelbar.

  • McGill, C. J. & C. M. Pomory, 2008. Effects of bleaching and nutrient supplementation on wet weight in the jellyfish Cassiopea xamachana (Bigelow) (Cnidaria: Scyphozoa). Marine and Freshwater Behaviour and Physiology 41(3): 179–189.

    Article  Google Scholar 

  • Mellas, R. E., S. E. McIlroy, W. K. Fitt & M. A. Coffroth, 2014. Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp. Journal of Experimental Marine Biology and Ecology 459: 38–44.

    Article  Google Scholar 

  • Newkirk, C. R., T. K. Frazer & M. Q. Martindale, 2018. Acquisition and proliferation of algal symbionts in bleached polyps of the upside-down jellyfish, Cassiopea xamachana. Journal of Experimental Marine Biology and Ecology 508: 44–51.

    Article  Google Scholar 

  • Ohdera, A. H., M. J. Abrams, C. L. Ames, D. M. Baker, L. P. Suescún-Bolivar, A. G. Collins, C. J. Freeman, E. Gamero-Mora, T. L. Goulet, D. K. Hofmann, A. Jaimes-Becerra, P. F. Long, A. C. Marques, L. A. Miller, L. D. Mydlarz, A. C. Morandini, C. R. Newkirk, S. P. Putri, J. E. Samson, S. N. Stampar, B. Steinworth, M. Templeman, P. E. Thomé, M. Vlok, C. M. Woodley, J. C. Y. Wong, M. Q. Martindale, W. K. Fitt & M. Medina, 2018. Upside-down but headed in the right direction: review of the highly versatile Cassiopea xamachana system. Frontiers in Ecology and Evolution 6: 35.

    Article  Google Scholar 

  • Pitt, K. A., E. F. Hourahane, A. Johnston, K. I. Pacey & J. D. Houghton, 2020. Optimising the application of 5-methoxy-2-methyl-indole to induce strobilation in moon jellyfish polyps. Marine Biology 167(10): 1–7.

    Article  Google Scholar 

  • Rahat, M. & O. Adar, 1980. Effect of symbiotic zooxanthellae and temperature on budding and strobilation in Cassiopeia andromeda (Eschscholz). The Biological Bulletin 159(2): 394–401.

    Article  Google Scholar 

  • Rippingale, R. J. & S. J. Kelly, 1995. Reproduction and survival of Phyllorhiza punctata (Cnidaria: Rhizostomeae) in a seasonally fluctuating salinity regime in Western Australia. Marine Freshwater Research 46(8): 1145–1151.

    Article  Google Scholar 

  • Spangenberg, D. B., 1967. Iodine induction of metamorphosis in Aurelia. Journal of Experimental Zoology 165(3): 441–449.

    Article  CAS  Google Scholar 

  • Sugiura, Y., 1966. On the life-history of Rhizostome medusae IV. Cephea Cephea. Embryologia 9(2): 105–122.

    Article  CAS  Google Scholar 

  • Thornhill, D. J., M. W. Daniel, T. C. LaJeunesse, G. W. Schmidt & W. K. Fitt, 2006. Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. Journal of Experimental Marine Biology and Ecology 338(1): 50–56.

    Article  Google Scholar 

  • Wang, N., M. Wang, Y. Wang & C. Li, 2020. Inductive effect of bioactive substances on strobilation of jellyfish Aurelia coerulea. Journal of Oceanology and Limnology 38(5): 1548–1558.

    Article  CAS  Google Scholar 

  • Yamamori, L., K. Okuizumi, C. Sato, S. Ikeda & H. Toyohara, 2017. Comparison of the inducing effect of indole compounds on medusa formation in different classes of medusozoa. Zoological Science 34(3): 173–178.

    Article  CAS  Google Scholar 

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Acknowledgements

We are very grateful to Azeroth aquarium in the New District of Jiangbei in Nanjin for providing us with Cassiopea andromeda polyps. We also thank Professor David Randall from University of British Columbia for his kind help with English language editing.

Funding

This work was contribution to the Regional Demonstration Project of the 13th Five-Year Plan of Marine Economy Innovation & Development in Xiamen (funded by the State Oceanic Administration, People's Republic of China under Grant Agreement No. 16PZY002SF18).

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Author notes

  1. Liqiu Deng and Shuhong Wang have contributed equally to this work and share first authorship.

Authors and Affiliations

  1. Fisheries College, Jimei University, Xiamen, 361021, Fujian, China

    Liqiu Deng, Shuhong Wang, Ting Wang, Yuxuan Zhao & Qi Luo

  2. Ornamental Aquarium Engineering Research Centre in Universities of Fujian Province, Xiamen, 361021, China

    Liqiu Deng & Shuhong Wang

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  1. Liqiu Deng
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Contributions

Conceptualization: SW and LD; Methodology: LD; Material preparation, data collection and analysis: LD, TW, YZ and QL; Original draft preparation, LD; Reviewing and Editing, resources, supervision, and funding acquisition: SW. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Shuhong Wang.

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Deng, L., Wang, S., Wang, T. et al. Indoles can induce strobilation in aposymbiotic Cassiopea andromeda polyps but are associated with developmental abnormalities. Hydrobiologia 849, 3275–3285 (2022). https://doi.org/10.1007/s10750-022-04883-z

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