Application of DNA metabarcoding to characterize the diet of the moon jellyfish Aurelia coerulea polyps and ephyrae

Tingting Sun Lei Wang Jianmin Zhao Zhijun Dong

Tingting Sun, Lei Wang, Jianmin Zhao, Zhijun Dong. Application of DNA metabarcoding to characterize the diet of the moon jellyfish Aurelia coerulea polyps and ephyrae[J]. Acta Oceanologica Sinica. doi: 10.1007/s13131-021-1800-8
Citation: Tingting Sun, Lei Wang, Jianmin Zhao, Zhijun Dong. Application of DNA metabarcoding to characterize the diet of the moon jellyfish Aurelia coerulea polyps and ephyrae[J]. Acta Oceanologica Sinica. doi: 10.1007/s13131-021-1800-8

doi: 10.1007/s13131-021-1800-8

Application of DNA metabarcoding to characterize the diet of the moon jellyfish Aurelia coerulea polyps and ephyrae

Funds: The National Key Research and Development Program of China under contract No. 2018YFC1406501; the Strategic Priority Research Program of the Chinese Academy of Sciences under contract No. XDA23050301; the National Natural Science Foundation of China under contract No. 41876138; the Instrument Developing Project of the Chinese Academy of Sciences under contract No. YJKYYQ20180047; the Key Research and Development Program of Yantai under contract No. 2018ZHGY073.
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  • Figure  1.  Sampling site for Aurelia coerulea polyps and ephyrae in Fenghuang Lake, southern Yellow Sea.

    Figure  2.  Neighbor joining tree for prey taxa in the polyps and ephyrae of the moon jellyfish Aurelia coerulea using the Tajima-Nei model with 1 000 bootstrap replications. + Presence.

    Figure  3.  Rank abundance of phylogenetic class and order of prey organisms detected in the polyps and ephyrae of the moon jellyfish Aurelia coerulea. The y axis shows percent of total reads that each taxonomic contributes. a. Class and b. order.

    Table  1.   Prey taxa detected in the polyps and ephyrae of the moon jellyfish Aurelia coerulea. The classification system used here is Cavalier-Smith’s system of classification (Cavalier-Smith, 1998)

    AnnelidaPolychaetaSpionidaPseudopolydora paucibranchiata100%11.130MN165825
    Polydora sp.99%0.070MN165843
    SabellidaHydroides panamensis 100%02.49MN165831
    TerebellidaCtenodrilus serratus 100%00.03MN165847
    ScolecidaArenicola brasiliensis 100%00.03MN165854
    ArthropodaMalacostracaBrachyuraHemigrapsus takanoi100%0.690MN165834
    MaxillopodaCalanoidaLabidocera sp.96%6.650.01MN165826
    Eurytemora affinis 99%1.260.06MN165828
    Acartia pacifica 100%0.120MN165842
    Eurytemora pacifica99%48.470.33MN165822
    CyclopoidaCyclopina sp. 95%1.640.06MN165829
    HarpacticoidaThalestridae sp.99%02.21MN165832
    Stenhelia sp.92%0.131.85MN165833
    Amphiascoides atopus99%01.43MN165835
    Normanellidae sp.98%01.00MN165836
    Mesochra sp.99%00.42MN165839
    Tisbe sp.99%00.01MN165863
    Amonardia sp.100%07.72MN165827
    Uncultured copepod94%00.43MN165837
    ChordataAscidiaceaStolidobranchiataStyela clava100%00.01MN165861
    CiliophoraOligohymenophoreaSessilidaPseudovorticella sp.198%<0.010.02MN165851
    Pseudovorticella sp.2 100%00.02MN165853
    PhyllopharyngeaEndogenidaAcineta sp.99%00.02MN165848
    SpirotricheaChoreotrichidaRimostrombidium veniliae99%00.01MN165857
    TintinninaChoreotrichia sp.100%0<0.01MN165862
    Uncultured clilate97%0<0.01MN165864
    TelonemeaTelonemidaTelonema sp.99%00.01MN165852
    CnidariaHydrozoaFiliferaRathkea octopunctata100%10.7960.48MN165823
    CapitataSarsia tubulosa100%18.4018.47MN165824
    Cladonema californicum100%0.332.47MN165830
    Ectopleura larynx99%<0.010.03MN165845
    StaurozoaStauromedusaeHaliclystus sp.100%00.04MN165849
    NematodaAdenophoreaChromadoridaNeochromadora sp. 96%00.01MN165855
    EnoplidaOncholaimus sp.91%00.01MN165856
    Anticomidae sp.100%00.02MN165858
    Enoplus taipingensis100%00.01MN165860
    PlatyhelminthesRhabditophoraPolycladidaNotoplana australis 100%0.160MN165838
    MacrostomidaMicrostomum sp.99%0.050.10MN165840
    Macrostomum pusillum 99%0.020.03MN165844
    RhabdocoelaPromesostoma sp.99%0.070.05MN165841
    OchrophytaPhaeophyceaeChordarialesHalothrix ambigua100%00.01MN165865
    BacillariophytaCentricaeNaviculalesNavicula sp.99%00.07MN165846
    DiscoidalesThalassiosira guillardii100%0<0.01MN165859
    DeuteromycotinaHyphomycetesHyphomycetalesAspergillus sp.100%0.010MN165850
    Note: The datasets generated for this study are available for download via GenBank with accession numbers MN165822-MN165865.
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  • [1] Albaina A, Aguirre M, Abad D, et al. 2016. 18S rRNA V9 metabarcoding for diet characterization: a critical evaluation with two sympatric zooplanktivorous fish species. Ecology and Evolution, 6(6): 1809–1824. doi: 10.1002/ece3.1986
    [2] Arai M N. 1997. A Functional Biology of Scyphozoa. London, UK: Chapman & Hall, 58–91
    [3] Ballard J W O, Melvin R G. 2010. Linking the mitochondrial genotype to the organismal phenotype. Molecular Ecology, 19(8): 1523–1539. doi: 10.1111/j.1365-294X.2010.04594.x
    [4] Båmstedt U. 1990. Trophodynamics of the scyphomedusae Aurelia aurita. Predation rate in relation to abundance, size and type of prey organism. Journal of Plankton Research, 12(1): 215–229. doi: 10.1093/plankt/12.1.215
    [5] Båmstedt U, Wild B, Martinussen M. 2001. Significance of food type for growth of ephyrae Aurelia aurita (Scyphozoa). Marine Biology, 139(4): 641–650. doi: 10.1007/s002270100623
    [6] Bayha K M, Dawson M N. 2010. New family of allomorphic jellyfishes, Drymonematidae (Scyphozoa, Discomedusae), emphasizes evolution in the functional morphology and trophic ecology of gelatinous zooplankton. The Biological Bulletin, 219(3): 249–267. doi: 10.1086/BBLv219n3p249
    [7] Bohmann K, Monadjem A, Noer C L, et al. 2011. Molecular diet analysis of two African free-tailed bats (Molossidae) using high throughput sequencing. PLoS ONE, 6(6): e21441. doi: 10.1371/journal.pone.0021441
    [8] Brassea-Pérez E, Schramm Y, Heckel G, et al. 2019. Metabarcoding analysis of the Pacific harbor seal diet in Mexico. Marine Biology, 166(8): 106. doi: 10.1007/s00227-019-3555-8
    [9] Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336. doi: 10.1038/nmeth.f.303
    [10] Cardona L, de Quevedo I Á, Borrell A, et al. 2012. Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS ONE, 7(3): e31329. doi: 10.1371/journal.pone.0031329
    [11] Cardona L, Martínez-Iñigo L, Mateo R, et al. 2015. The role of sardine as prey for pelagic predators in the western Mediterranean Sea assessed using stable isotopes and fatty acids. Marine Ecology Progress Series, 531: 1–14. doi: 10.3354/meps11353
    [12] Carrizo S S, Schiariti A, Nagata R M, et al. 2016. Preliminary observations on ephyrae predation by Lychnorhiza lucerna medusa (Scyphozoa; Rhizostomeae). Der Zoologische Garten, 85(1-2): 74–83. doi: 10.1016/j.zoolgart.2015.09.011
    [13] Cavalier-Smith T. 1998. A revised six-kingdom system of life. Biological Reviews of the Cambridge Philosophical Society, 73: 203–266. doi: 10.1017/s0006323198005167
    [14] Costello J H, Colin S P, Dabiri J O. 2008. Medusan morphospace: phylogenetic constraints, biomechanical solutions, and ecological consequences. Invertebrate Biology, 127(3): 265–290. doi: 10.1111/j.1744-7410.2008.00126.x
    [15] Dawson M N, Gupta A S, England M H. 2005. Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. Proceedings of the National Academy of Sciences of the United States of America, 102(34): 11968–11973. doi: 10.1073/pnas.0503811102
    [16] Deagle B E, Chiaradia A, McInnes J, et al. 2010. Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out?. Conservation Genetics, 11(5): 2039–2048. doi: 10.1007/s10592-010-0096-6
    [17] Dong Zhijun. 2019. Blooms of the moon jellyfish Aurelia: causes, consequences and controls. In: Sheppard C, ed. World Seas: An Environmental Evaluation. 2nd ed. Amsterdam, the Netherlands: Elsevier, 163–171, doi: 10.1016/B978-0-12-805052-1.00008-5
    [18] Dong Zhijun, Liu Dongyan, Keesing J K. 2010. Jellyfish blooms in China: dominant species, causes and consequences. Marine Pollution Bulletin, 60(7): 954–963. doi: 10.1016/j.marpolbul.2010.04.022
    [19] Dong Zhijun, Liu Dongyan, Keesing J K. 2014. Contrasting trends in populations of Rhopilema esculentum and Aurelia aurita in Chinese waters. In: Pitt K A, Lucas C H, eds. Jellyfish Blooms. Dordrecht, the Netherlands: Springer, 207–218, doi: 10.1007/978-94-007-7015-7_9
    [20] Dong Zhijun, Liu Zhongyuan, Liu Dongyan. 2015. Genetic characterization of the scyphozoan jellyfish Aurelia spp. in Chinese coastal waters using mitochondrial markers. Biochemical Systematics and Ecology, 60: 15–23. doi: 10.1016/j.bse.2015.02.018
    [21] Duarte C M, Pitt K A, Lucas C H, et al. 2013. Is global ocean sprawl a cause of jellyfish blooms?. Frontiers in Ecology and the Environment, 11(2): 91–97. doi: 10.1890/110246
    [22] Ficetola G F, Coissac E, Zundel S, et al. 2010. An In silico approach for the evaluation of DNA barcodes. BMC Genomics, 11: 434. doi: 10.1186/1471-2164-11-434
    [23] Graham W M, Kroutil R M. 2001. Size-based prey selectivity and dietary shifts in the jellyfish, Aurelia aurita. Journal of Plankton Research, 23(1): 67–74. doi: 10.1093/plankt/23.1.67
    [24] Gröndahl F. 1988. Interactions between polyps of Aurelia aurita and planktonic larvae of scyphozoans: an experimental study. Marine Ecology-Progress Series, 45: 87–93. doi: 10.3354/meps045087
    [25] Gröndahl F. 1989. Evidence of gregarious settlement of planula larvae of the scyphozoan Aurelia aurita: an experimental study. Marine Ecology-Progress Series, 56: 119–125. doi: 10.3354/meps056119
    [26] Han C H, Uye S I. 2010. Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita s.l. Plankton and Benthos Research, 5(3): 98–105. doi: 10.3800/pbr.5.98
    [27] Higgins III J E, Ford M D, Costello J H. 2008. Transitions in morphology, nematocyst distribution, fluid motions, and prey capture during development of the scyphomedusa Cyanea capillata. The Biological Bulletin, 214(1): 29–41. doi: 10.2307/25066657
    [28] Hirai J, Hidaka K, Nagai S, et al. 2017. Molecular-based diet analysis of the early post-larvae of Japanese sardine Sardinops melanostictus and Pacific round herring Etrumeus teres. Marine Ecology Progress Series, 564: 99–113. doi: 10.3354/meps12008
    [29] Hu Simin, Guo Zhiling, Li Tao, et al. 2015. Molecular analysis of in situ diets of coral reef copepods: evidence of terrestrial plant detritus as a food source in Sanya Bay, China. Journal of Plankton Research, 37(2): 363–371. doi: 10.1093/plankt/fbv014
    [30] Huang Yousong. 2013. PCR-based in situ dietary analysis of two common copepods in Bohai Sea and Yellow Sea coastal waters (in Chinese)[dissertation]. Qingdao: Ocean University of China
    [31] Jarman S N, McInnes J C, Faux C, et al. 2013. Adélie penguin population diet monitoring by analysis of food DNA in scats. PLoS ONE, 8(12): e82227. doi: 10.1371/journal.pone.0082227
    [32] Kamiyama T. 2013. Planktonic ciliates as food for the scyphozoan Aurelia aurita (s.l.): effects on asexual reproduction of the polyp stage. Journal of Experimental Marine Biology and Ecology, 445: 21–28. doi: 10.1016/j.jembe.2013.03.018
    [33] Kamiyama T. 2018. Planktonic ciliates as food for the scyphozoan Aurelia coerulea: feeding and growth responses of ephyra and metephyra stages. Journal of Oceanography, 74: 53–63. doi: 10.1007/s10872-017-0438-9
    [34] Kodama T, Hirai J, Tamura S, et al. 2017. Diet composition and feeding habits of larval Pacific bluefin tuna Thunnus orientalis in the Sea of Japan: integrated morphological and metagenetic analysis. Marine Ecology Progress Series, 583: 211–226. doi: 10.3354/meps12341
    [35] Kogovšek T, Bogunović B, Malej A. 2010. Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series. Hydrobiologia, 645: 81–96. doi: 10.1007/s10750-010-0217-8
    [36] Lo W T, Chen I L. 2008. Population succession and feeding of scyphomedusae, Aurelia aurita, in a eutrophic tropical lagoon in Taiwan. Estuarine, Coastal and Shelf Science, 76(2): 227–238. doi: 10.1016/j.ecss.2007.07.015
    [37] Lucas C H, Graham W M, Widmer C. 2012. Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Advances in Marine Biology, 63: 133–196. doi: 10.1016/b978-0-12-394282-1.00003-x
    [38] Magoč T, Salzberg S L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2957–2963. doi: 10.1093/bioinformatics/btr507
    [39] Malej A, Turk V, Lučić D, et al. 2007. Direct and indirect trophic interactions of Aurelia sp. (Scyphozoa) in a stratified marine environment (Mljet Lakes, Adriatic Sea). Marine Biology, 151(3): 827–841. doi: 10.1007/s00227-006-0503-1
    [40] McInnes J C, Alderman R, Lea M A, et al. 2017. High occurrence of jellyfish predation by black-browed and Campbell albatross identified by DNA metabarcoding. Molecular Ecology, 26(18): 4831–4845. doi: 10.1111/mec.14245
    [41] O’Rorke R, Lavery S, Chow S, et al. 2012. Determining the diet of larvae of western rock lobster (Panulirus cygnus) using high-throughput DNA sequencing techniques. PLoS ONE, 7(8): e42757. doi: 10.1371/journal.pone.0042757
    [42] O’Rorke R, Lavery S D, Wang M, et al. 2014. Determining the diet of larvae of the red rock lobster (Jasus edwardsii) using high-throughput DNA sequencing techniques. Marine Biology, 161(3): 551–563. doi: 10.1007/s00227-013-2357-7
    [43] Östman C. 1997. Abundance, feeding behaviour and nematocysts of scyphopolyps (Cnidaria) and nematocysts in their predator, the nudibranch Coryphella verrucosa (Mollusca). Hydrobiologia, 355(1): 21–28. doi: 10.1023/A:1003065726381
    [44] Pompanon F, Deagle B E, Symondson W O C, et al. 2012. Who is eating what: diet assessment using next generation sequencing. Molecular Ecology, 21(8): 1931–1950. doi: 10.1111/j.1365-294x.2011.05403.x
    [45] Purcell J E. 1997. Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates and effects on prey populations. Annales de l'Institute Oceanographique, 73(2): 125–137
    [46] Purcell J E. 2012. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annual Review of Marine Science, 4: 209–235. doi: 10.1146/annurev-marine-120709-142751
    [47] Purcell J E, Baxter E J, Fuentes V. 2013. Jellyfish as products and problems of aquaculture. In: Allan G, Burnell G, eds. Advances in Aquaculture Hatchery Technology. Cambridge, UK: Woodhead Publishing, 404–430, doi: 10.1533/9780857097460.2.404
    [48] Purcell J E, Hoover R A, Schwarck N T. 2009. Interannual variation of strobilation by the scyphozoan Aurelia labiata in relation to polyp density, temperature, salinity, and light conditions in situ. Marine Ecology Progress Series, 375: 139–149. doi: 10.3354/meps07785
    [49] Purcell J E, Sturdevant M V. 2001. Prey selection and dietary overlap among zooplanktivorous jellyfish and juvenile fishes in Prince William Sound, Alaska. Marine Ecology Progress Series, 210: 67–83. doi: 10.3354/meps210067
    [50] Riisgård H U, Madsen C V. 2011. Clearance rates of ephyrae and small medusae of the common jellyfish Aurelia aurita offered different types of prey. Journal of Sea Research, 65(1): 51–57. doi: 10.1016/j.seares.2010.07.002
    [51] Schiariti A, Morandini A C, Jarms G, et al. 2014. Asexual reproduction strategies and blooming potential in Scyphozoa. Marine Ecology Progress Series, 510: 241–253. doi: 10.3354/meps10798
    [52] Scorrano S, Aglieri G, Boero F, et al. 2017. Unmasking Aurelia species in the Mediterranean Sea: an integrative morphometric and molecular approach. Zoological Journal of the Linnean Society, 180(2): 243–267. doi: 10.1111/zoj.12494
    [53] Skikne S A, Sherlock R E, Robison B H. 2009. Uptake of dissolved organic matter by ephyrae of two species of scyphomedusae. Journal of Plankton Research, 31(12): 1563–1570. doi: 10.1093/plankt/fbp088
    [54] Su Maoliang, Liu Huifen, Liang Xuemei, et al. 2018. Dietary analysis of marine fish species: enhancing the detection of prey-specific DNA sequences via high-throughput sequencing using blocking primers. Estuaries and Coasts, 41(2): 560–571. doi: 10.1007/s12237-017-0279-1
    [55] Sullivan B K, Suchman C L, Costello J H. 1997. Mechanics of prey selection by ephyrae of the scyphomedusa Aurelia aurita. Marine Biology, 130(2): 213–222. doi: 10.1007/s002270050241
    [56] Thiebot J B, Arnould J P Y, Gómez-Laich A, et al. 2017. Jellyfish and other gelata as food for four penguin species-insights from predator-borne videos. Frontiers in Ecology and the Environment, 15(8): 437–441. doi: 10.1002/fee.1529
    [57] Titelman J, Hansson L J. 2006. Feeding rates of the jellyfish Aurelia aurita on fish larvae. Marine Biology, 149(2): 297–306. doi: 10.1007/s00227-005-0200-5
    [58] Tsikhon-Lukanina E A, Reznichenko O G, Lukasheva T A. 1996. Food consumption by scyphistomae of the jellyfish Aurelia aurita in the Black Sea. Oceanology, 35(6): 815–818
    [59] Uye S I. 2011. Human forcing of the copepod-fish-jellyfish triangular trophic relationship. Hydrobiologia, 666(1): 71–83. doi: 10.1007/s10750-010-0208-9
    [60] Uye S, Shimauchi H. 2005. Population biomass, feeding, respiration and growth rates, and carbon budget of the scyphomedusa Aurelia aurita in the Inland Sea of Japan. Journal of Plankton Research, 27(3): 237–248. doi: 10.1093/plankt/fbh172
    [61] Wang Nan, Li Chaolun. 2015. The effect of temperature and food supply on the growth and ontogeny of Aurelia sp. 1 ephyrae. Hydrobiologia, 754(1): 157–167. doi: 10.1007/s10750-014-1981-7
    [62] Wang Yantao, Zheng Shan, Sun Song, et al. 2015. Effect of temperature and food type on asexual reproduction in Aurelia sp. 1 polyps. Hydrobiologia, 754(1): 169–178. doi: 10.1007/s10750-014-2020-4
    [63] Zheng Shan, Sun Xiaoxia, Wang Yantao, et al. 2015. Significance of different microalgal species for growth of moon jellyfish ephyrae, Aurelia sp.1. Journal of Ocean University of China, 14(5): 823–828. doi: 10.1007/s11802-015-2775-x
    [64] Zoccarato L, Celussi M, Pallavicini A, et al. 2016. Aurelia aurita ephyrae reshape a coastal microbial community. Frontiers in Microbiology, 7: 749. doi: 10.3389/fmicb.2016.00749
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