Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish <italic style="font-style: italic">Rhopilema esculentum</italic>

Jianlong GE; Xiaohui CHEN; Changlin LIU; Jie TAN; Li BIAN; Lifei CHEN; Siqing CHEN

doi:10.1007/s00343-021-0252-5

Your Location：

Home >

Browse articles >

Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum

Biology | Updated：2023-04-27

- Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum
- Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum
- 海洋湖沼学报（英文） 2022年40卷第1期页码：226-234
- Affiliations：
  
  1.Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266071, China
  2.Yancheng Huayi Aquatic Products Co. Ltd., Yancheng 224300, China
- Author bio：
  
  Siqing CHEN, E-mail: chensq@ysfri.ac.cn
- Funds：
  
  the National Natural Science Foundation of China(31702327);the Key Program for International S&T Cooperation Projects of China(2017YFE0111100-5);the Fund of Key Laboratory of Sustainable Development of Marine Fisheries;Ministry of Agriculture and Rural Affairs of China and Central Public-interest Scientific Institution Basal Research Fund;Yellow Sea Fisheries Research Institute;Chinese Academy of Fishery Sciences(20603022019020);© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2022
- DOI：10.1007/s00343-021-0252-5
  中图分类号：
- 收稿：2020-07-26，
  
  录用：2020-11-24，
  
  网络首发：2021-02-04，
  
  纸质出版：2022-01
- Accepted：
Scan QR Code
Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum[J]. 海洋湖沼学报（英文）, 2022,40(1):226-234.

Jianlong GE, Xiaohui CHEN, Changlin LIU, et al. Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum[J]. Journal of Oceanology and Limnology, 2022, 40(1): 226-234.
Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum[J]. 海洋湖沼学报（英文）, 2022,40(1):226-234. DOI： 10.1007/s00343-021-0252-5.

Jianlong GE, Xiaohui CHEN, Changlin LIU, et al. Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum[J]. Journal of Oceanology and Limnology, 2022, 40(1): 226-234. DOI： 10.1007/s00343-021-0252-5.

摘要

Abstract

Strobilation is a well-organized metamorphosis process in scyphozoan jellyfish

through which the benthic polyp develops into the pelagic medusa. So far

knowledge on the molecular mechanisms behind the drastic morphological and physiological changes remains limited. In the present study

the metabolic profiles in polyp and strobila stages of jellyfish

Rhopilema esculentum

were examined using ultra-performance liquid chromatography coupled to a mass spectrometer. A total of 3 071 metabolites with putative annotation were detected

of which 167 were identified as differential metabolites between the polyp and strobila. Among the metabolites

31 significantly decreased and 136 significantly increased in abundance in the strobila. Thyroxin

one of the previously proposed strobilation inducer of

Aurelia

was not detected in this study. The indole-containing compounds are known for triggering strobilation in Discomedusae. Two indole derivatives and an indole-isomer containing metabolite were detected among the most significantly increased metabolites

which may be potential endogenous molecules for strobilation initiation. The membrane-associated phospholipids and the inflammation and oxidative stress-related eicosanoids were found to have significant changes. Although the functions of these metabolites in strobilation are not yet completely known

they provide some clues to the induction of the process of strobilation and metabolic responses that take place during strobilation.

关键词

Keywords

references

C Bachert . The role of histamine in allergic disease: reappraisal of its inflammatory potential . Allergy , 2002 . 57 ( 4 ): 287 - 296 . DOI: 10.1034/j.1398-9995.2002.1r3542.x http://doi.org/10.1034/j.1398-9995.2002.1r3542.x .

S Berking , N Czech , M Gerharz , K Herrmann , U Hoffmann , H Raifer , G Sekul , B Siefker , A Sommerei , F Vedder . 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 , 2005 . 49 ( 8 ): 969 - 976 . DOI: 10.1387/ijdb.052024sb http://doi.org/10.1387/ijdb.052024sb .

N J Berrill . Developmental analysis of scyphomedusae . Biological Reviews , 1949 . 24 ( 4 ): 393 - 409 . DOI: 10.1111/j.1469-185X.1949.tb00581.x http://doi.org/10.1111/j.1469-185X.1949.tb00581.x .

R E Black , K L Webb . Metabolism of 131 I in relation to strobilation of Chrysaora quinquecirrha (Scyphozoa) . Comparative Biochemistry and Physiology Part A: Physiology , 1973 . 45 ( 4 ): 1023 - 1029 . DOI: 10.1016/0300-9629(73)90339-3 http://doi.org/10.1016/0300-9629(73)90339-3 .

V Brekhman , A Malik , B Haas , N Sher , T Lotan . Transcriptome profiling of the dynamic life cycle of the scypohozoan jellyfish Aurelia aurita . BMC Genomics , 2015 . 16 ( 1 ): 74 DOI: 10.1186/s12864-015-1320-z http://doi.org/10.1186/s12864-015-1320-z .

N Bryan , H Ahswin , N Smart , Y Bayon , S Wohlert , J A Hunt . Reactive oxygen species (ROS)—a family of fate deciding molecules pivotal in constructive inflammation and wound healing . European Cells and Materials , 2012 . 24 249 - 265 . DOI: 10.22203/eCM.v024a18 http://doi.org/10.22203/eCM.v024a18 .

P Cabrales-Arellano , T Islas-Flores , P E Thomé , M A Villanueva . Indomethacin reproducibly induces metamorphosis in Cassiopea xamachana scyphistomae . PeerJ , 2017 . 5 e2979 DOI: 10.7717/peerj.2979 http://doi.org/10.7717/peerj.2979 .

J K Chen , G W Ding . Effect of temperature on the strobilation of jellyfish ( Rhopilema esculent a Kishinouye, Scyphozoa, Rhizostomeae) . Acta Zoologica Sinica , 1983 . 29 ( 3 ): 195 - 206 . http://agris.fao.org/openagris/search.do?recordID=US201302133872 http://agris.fao.org/openagris/search.do?recordID=US201302133872 , .

M A Crawford , K L Webb . An ultrastructural study of strobilation in Chrysaora quinquecirrha with special reference to neurosecretion . Journal of Experimental Zoology , 1972 . 182 ( 2 ): 251 - 269 . DOI: 10.1002/jez.1401820209 http://doi.org/10.1002/jez.1401820209 .

G W Ding , J K Chen . The life history of Rhopilema esculent a Kishinouye . Journal of Fisheries of China , 1981 . 5 ( 2 ): 93 - 102 . http://www.researchgate.net/publication/313423283_The_life_history_of_Rhopilema_-_esculenta_Kishinouye http://www.researchgate.net/publication/313423283_The_life_history_of_Rhopilema_-_esculenta_Kishinouye , .

Z J Dong , D Y Liu , J K Keesing . Jellyfish blooms in China: dominant species, causes and consequences . Marine Pollution Bulletin , 2010 . 60 ( 7 ): 954 - 963 . DOI: 10.1016/j.marpolbul.2010.04.022 http://doi.org/10.1016/j.marpolbul.2010.04.022 .

P R Esser , U Wölfle , C Dürr , F D von Loewenich , C M Schempp , M A Freudenberg , T Jakob , S F Martin . Contact sensitizers induce skin inflammation via ROS production and hyaluronic acid degradation . PLoS One , 2012 . 7 ( 7 ): e41340 DOI: 10.1371/journal.pone.0041340 http://doi.org/10.1371/journal.pone.0041340 .

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

J L Ge , C L Liu , J Tan , L Bian , S Q Chen . Transcriptome analysis of scyphozoan jellyfish Rhopilema esculentum from polyp to medusa identifies potential genes regulating strobilation . Development Genes and Evolution , 2018 . 228 ( 6 ): 243 - 254 . DOI: 10.1007/s00427-018-0621-z http://doi.org/10.1007/s00427-018-0621-z .

D A Gold , N Nakanishi , N M Hensley , K Cozzolino , M Tabatabaee , M Martin , V Hartenstein , D K Jacobs . Structural and developmental disparity in the tentacles of the moon jellyfish Aurelia sp. 1 . PLoS One , 2015 . 10 ( 8 ): e0134741 DOI: 10.1371/journal.pone.0134741 http://doi.org/10.1371/journal.pone.0134741 .

H Harizi , J B Corcuff , N Gualde . Arachidonic-acid, derived eicosanoids: roles in biology and immunopathology . Trends in Molecular Medicine , 2008 . 14 ( 10 ): 461 - 469 . DOI: 10.1016/j.molmed.2008.08.005 http://doi.org/10.1016/j.molmed.2008.08.005 .

R R Helm , C W Dunn . Indoles induce metamorphosis in a broad diversity of jellyfish, but not in a crown jelly (Coronatae) . PLoS One , 2017 . 12 ( 12 ): e0188601 DOI: 10.1371/journal.pone.0188601 http://doi.org/10.1371/journal.pone.0188601 .

R R Helm , S Tiozzo , M K S Lilley , F Lombard , C W Dunn . Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles . EvoDevo , 2015 . 6 ( 1 ): 11 DOI: 10.1186/s13227-015-0005-7 http://doi.org/10.1186/s13227-015-0005-7 .

R R Helm . Evolution and development of scyphozoan jellyfish . Biological Reviews , 2018 . 93 ( 12 ): 1228 - 1250 . DOI: 10.1111/brv.12393 http://doi.org/10.1111/brv.12393 .

K Herrmann , B Siefker , S Berking . Sterile polystyrene culture dishes induce transformation of polyps into medusae in Aurelia aurita (Scyphozoa, Cnidaria) . Methods in Cell Science , 2004 . 25 ( 3-4 ): 135 - 136 . DOI: 10.1007/s11022-004-5592-y http://doi.org/10.1007/s11022-004-5592-y .

T A Ichu , J Han , C H Borchers , M Lesperance , C C Helbing . Metabolomic insights into system-wide coordination of vertebrate metamorphosis . BMC Developmental Biology , 2014 . 14 ( 1 ): 5 DOI: 10.1186/1471-213X-14-5 http://doi.org/10.1186/1471-213X-14-5 .

M Kroiher , B Siefker , S Berking . Induction of segmentation in polyps of Aurelia aurita (Scyphozoa, Cnidaria) into medusae and formation of mirror-image medusa anlagen . International Journal of Developmental Biology , 2000 . 44 ( 5 ): 485 - 490 . http://www.uni-koeln.de/math-nat-fak/zoologie/expmorph/morph/agberking/publikationen/segmentation_ft485.pdf http://www.uni-koeln.de/math-nat-fak/zoologie/expmorph/morph/agberking/publikationen/segmentation_ft485.pdf , .

H Kuniyoshi , I Okumura , R Kuroda , N Tsujita , K Arakawa , J Shoji , T Saito , H Osada . Indomethacin induction of metamorphosis from the asexual stage to sexual stage in the Moon Jellyfish, Aurelia aurita . Bioscience, Biotechnology, and Biochemistry , 2012 . 76 ( 7 ): 1397 - 1400 . DOI: 10.1271/bbb.120076 http://doi.org/10.1271/bbb.120076 .

M J Loeb , D K Hayes . Strobilation in the Chesapeake Bay sea nettle, Chrysaora quinquecirrha . V. Neurons and neurosecretion . Transactions of the American Microscopical Society , 1981 . 100 ( 3 ): 264 - 270 . DOI: 10.2307/3225551 http://doi.org/10.2307/3225551 .

M J Loeb . Strobilation in the Chesapeake Bay sea nettle Chrysaora quinquecirrha —III. Dissociation of the neck-inducing factor from strobilating polyps . Comparative Biochemistry and Physiology Part A: Physiology , 1974a . 49 ( 3 ): 423 - 432 . DOI: 10.1016/0300,9629(74)90558-1 http://doi.org/10.1016/0300,9629(74)90558-1 .

M J Loeb . Strobilation in the Chesapeake bay sea nettle, Chrysaora quinquecirrha —II. Partial characterization of the neck-inducing factor from strobilating polyps . Comparative Biochemistry and Physiology Part A: Physiology , 1974b . 47 ( 1 ): 291 - 301 . DOI: 10.1016/0300-9629(74)90073-5 http://doi.org/10.1016/0300-9629(74)90073-5 .

T C Luehr , E M Koide , X D Wang , J Han , C H Borchers , C C Helbing . Metabolomic insights into the effects of thyroid hormone on Rana [ Lithobates ] catesbeiana metamorphosis using whole-body matrix assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) . General and Comparative Endocrinology , 2018 . 265 237 - 245 . DOI: 10.1016/j.ygcen.2018.02.012 http://doi.org/10.1016/j.ygcen.2018.02.012 .

M Mittal , M R Siddiqui , K Tran , S P Reddy , A B Malik . Reactive oxygen species in inflammation and tissue injury . Antioxidants & Redox Signaling , 2014 . 20 ( 7 ): 1126 - 1167 . DOI: 10.1089/ars.2012.5149 http://doi.org/10.1089/ars.2012.5149 .

J E Olmon , K L Webb . Metabolism of 131 I in relation to strobilation of Aurelia aurita L. (Scyphozoa) . Journal of Experimental Marine Biology and Ecology , 1974 . 16 ( 2 ): 113 - 122 . DOI: 10.1016/0022-0981(74)90014-8 http://doi.org/10.1016/0022-0981(74)90014-8 .

L Prieto , D Astorga , G Navarro , J Ruiz . Environmental control of phase transition and polyp survival of a massive-outbreaker jellyfish . PLoS One , 2010 . 5 ( 11 ): e13793 DOI: 10.1371/journal.pone.0013793 http://doi.org/10.1371/journal.pone.0013793 .

J E Purcell , S I Uye , W T Lo . Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review . Marine Ecology Progress Series , 2007 . 350 153 - 174 . DOI: 10.3354/meps07093 http://doi.org/10.3354/meps07093 .

M Rahmati , A Mobasheri , M Mozafari . Inflammatory mediators in osteoarthritis: a critical review of the state, of-the-art, current prospects, and future challenges . Bone , 2016 . 85 81 - 90 . DOI: 10.1016/j.bone.2016.01.019 http://doi.org/10.1016/j.bone.2016.01.019 .

W E Schwab . The ontogeny of swimming behavior in the scyphozoan, Aurelia aurita . I. Electrophysiological analysis . Biological Bulletin , 1977 . 152 ( 2 ): 233 - 250 . DOI: 10.2307/1540562 http://doi.org/10.2307/1540562 .

D B Spangenberg . Iodine induction of metamorphosis in Aurelia . Journal of Experimental Zoology , 1967 . 165 ( 3 ): 441 - 449 . DOI: 10.1002/jez.1401650312 http://doi.org/10.1002/jez.1401650312 .

D B Spangenberg . Thyroxine induced metamorphosis in Aurelia . Journal of Experimental Zoology , 1971 . 178 ( 2 ): 183 - 194 . DOI: 10.1002/jez.1401780205 http://doi.org/10.1002/jez.1401780205 .

D B Spangenberg . Thyroxine in Early Strobilation in Aurelia aurita . American Zoologist , 1974 . 14 ( 2 ): 825 - 831 . DOI: 10.1093/icb/14.2.825 http://doi.org/10.1093/icb/14.2.825 .

D B Spangenberg . Rhopalium development in Aurelia aurita ephyrae . Hydrobiologia , 1991 . 216 ( 1 ): 45 - 49 . DOI: 10.1007/BF00026442 http://doi.org/10.1007/BF00026442 .

X Y Yang , X Z Li , S M Zhang . Metabolomics analysis of oral mucosa reveals profile perturbation in reticular oral lichen planus . Clinica Chimica Acta , 2018 . 487 28 - 32 . DOI: 10.1016/j.cca.2018.09.021 http://doi.org/10.1016/j.cca.2018.09.021 .

P P Yin , A R Jia , K Heimann , M S Zhang , X Liu , W Zhang , C H Liu . Hot water pretreatment-induced significant metabolite changes in the sea cucumber Apostichopus japonicus . Food Chemistry , 2020 . 314 126211 DOI: 10.1016/j.foodchem.2020.126211 http://doi.org/10.1016/j.foodchem.2020.126211 .

K You , C H Ma , H W Gao , F Q Li , M Z Zhang , Y T Qiu , B Wang . Research on the jellyfish ( Rhopilema esculentum Kishinouye) and associated aquaculture techniques in China: current status . Aquaculture International , 2007 . 15 ( 6 ): 479 - 488 . DOI: 10.1007/s10499-007-9114-1 http://doi.org/10.1007/s10499-007-9114-1 .

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Metabolomic and proteomic responses ofPhaeodactylum tricornutumto hypoxia

Integration of metabolomics and transcriptomics revealed the biosynthetic mechanism of anti-parasitic compounds in Salinivibrio proteolyticus strain YCSC6

Species-specific detection and quantification of scyphomedusae in Jiaozhou Bay, China, using a quantitative real-time PCR assay

Inductive effect of bioactive substances on strobilation of jellyfish Aurelia coerulea

Carbon distribution strategy of Aurelia coerulea polyps in the strobilation process in relation to temperature and food supply

Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum

Metabolomics provide insights into the endogenous mechanism of strobilation in the scyphozoan jellyfish Rhopilema esculentum

DOI：10.1007/s00343-021-0252-5

摘要

Abstract

关键词

Keywords

references