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Bacterial community succession in response to dissolved organic matter released from live jellyfish

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Abstract

Jellyfish blooms have increased worldwide, and the outbreaks of jellyfish population not only affect the food web structures via voracious predation but also play an important role in the dynamics of nutrients and oxygen in planktonic food webs. However, it remains unclear whether specific carbon compounds released through jellyfish metabolic processes have the potential to shape bacterial community composition. Therefore, in this study, we aimed to investigate the compositional succession of the bacterioplankton community in response to the dissolved organic matter (DOM) released by the live Scyphomedusae Cyanea lamarckii and Chrysaora hysoscella collected from Helgoland Roads of the North Sea. The bacterial community was significantly stimulated by the DOM released form live jellyfish and different dominant phylotypes were observed for these two Scyphomedusae species. Furthermore, the bacterial community structures in the different DOM sources, jellyfish-incubated media, Kabeltonne seawater, and artificial seawater (DOM-free) were significantly different, as revealed by automated ribosomal intergenic spacer analysis fingerprints. Catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) revealed a rapid species-specific shift in bacterial community composition. Gammaproteobacteria dominated the community instead of the Bacteroidetes community for C. lamarckii, whereas Gammaproteobacteria and Bacteroidetes dominated the community for C. hysoscella. The significant differences in the bacterial community composition and succession indicate that the components of the DOM released by jellyfish might differ with jellyfish species.

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References

  • Allers E, Gómez-Consarnau L, Pinhassi J, Gasol J M, Šimek K, Pernthaler J. 2007. Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ mental Microbiology, 9(10): 2417–2429.

    Article  Google Scholar 

  • Allers E, Niesner C, Wild C, Pernthaler J. 2008. Microbes enriched in seawater after addition of coral mucus. Applied and Environ mental Microbiology, 74 (10): 3274–3278.

    Article  Google Scholar 

  • Alonso C, Pernthaler J. 2006. Roseobacter and SAR11 dominate microbial glucose uptake in coastal North Sea waters. Environ mental Microbiology, 8 (11): 2022–2030.

    Article  Google Scholar 

  • Alonso-Sáez L, Gasol JM. 2007. Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern mediterranean coastal waters. Applied and Environmental Microbiology, 73: 3528–3535.

    Article  Google Scholar 

  • Amon R M W, Benner R. 1994. Rapid cycling of highmolecular-weight dissolved organic matter in the ocean. Nature, 369 (6481): 549–552.

    Article  Google Scholar 

  • Azam F, Fenchel T, Field J G, Gray J S, Meyer-Reil L A, Thingstad F. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series, 10: 257–263.

    Article  Google Scholar 

  • Barz K, Hirche H J. 2007. Abundance, distribution and prey composition of Scyphomedusae in the southern North Sea. Marine Biology, 151 (3): 1 021–1 033.

    Article  Google Scholar 

  • Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E, Würdemann C A, Quast C, Kuhl H, Knaust F, Woebken D, Bischof K, Mussmann M, Choudhuri J V, Meyer F, Reinhardt R, Amann R I, Glöckner F O. 2006. Whole genome analysis of the marine Bacteroidetes ‘Gramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ mental Microbiology, 8 (12): 2 201–2 213.

    Article  Google Scholar 

  • Baumann L, Baumann P, Mandel M, Allen R D. 1972. Taxonomy of aerobic marine eubacteria. Journal of Bacteriology, 110 (1): 402–429.

    Google Scholar 

  • Benner R, Pakulski J D, McCarthy M, Hedges J I, Hatcher P G. 1992. Bulk chemical characteristics of dissolved organic matter in the ocean. Science, 255 (5051): 1 561–1 564.

    Article  Google Scholar 

  • Billett D S M, Bett B J, Jacobs C L, Rouse I P, Wigham B D. 2006. Mass deposition of jellyfish in the deep Arabian Sea. Limnology and Oceanogr aphy, 51 (5): 2 077–2 083.

    Article  Google Scholar 

  • Blanchet M, Pringault O, Bouvy M, Catala P, Oriol L, Caparros J, Ortega-Retuerta E, Intertaglia L, West N, Agis M, Got P, Joux F. 2015. Changes in bacterial community metabolism and composition during the degradation of dissolved organic matter from the jellyfish Aurelia aurita in a Mediterranean coastal lagoon. Environ mental Sci ence and Pollution Research, 22 (18): 13 638–13 653.

    Article  Google Scholar 

  • Brodeur R D, Sugisaki H, Hunt G L Jr. 2002. Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Marine Ecology Progress Series, 233: 89–103.

    Article  Google Scholar 

  • Carlson C A, Hansell D A, Peltzer E T, Smith W O Jr. 2000. Stocks and dynamics of dissolved and particulate organic matter in the southern Ross Sea, Antarctica. Deep Sea Research Part II: Topical Studies in Oceanography, 47 (15-16): 3 201–3 225.

    Article  Google Scholar 

  • Cho J C, Stapels M D, Morris R M, Vergin K L, Schwalbach M S, Givan S A, Barofsky D F, Giovannoni S J. 2007. Polyphyletic photosynthetic reaction centre genes in oligotrophic marine Gammaproteobacteria. Environ mental Microbiology, 9 (6): 1 456–1 463.

    Article  Google Scholar 

  • Condon R H, Steinberg D K, del Giorgio P A, Bouvier T C, Bronk D A, Graham W M, Ducklow H W. 2011. Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proceedings of the National Academy of Sciences of the United States of America, 108 (25): 10 225–10 230.

    Article  Google Scholar 

  • Cottrell M T, Kirchman D L. 2000a. Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Applied and Environ mental Microbiology, 66 (12): 5 116–5 122.

    Article  Google Scholar 

  • Cottrell M T, Kirchman D L. 2000b. Natural assemblages of marine proteobacteria and members of the Cytophaga - Flavobacter cluster consuming low- and high-molecularweight dissolved organic matter. Applied and Environ mental Microbiology, 66 (4): 1 692–1 697.

    Article  Google Scholar 

  • Dinasquet J, Kragh T, Schrøter M L, Søndergaard M, Riemann L. 2013. Functional and compositional succession of bacterioplankton in response to a gradient in bioavailable dissolved organic carbon. Environ mental Microbiology, 15 (9): 2 616–2 628.

    Article  Google Scholar 

  • Doyle T K, De Haas H, Cotton D, Dorschel B, Cummins V, Houghton J D R, Davenport J, Hays G C. 2008. Widespread occurrence of the jellyfish Pelagia noctiluca in Irish coastal and shelf waters. Journal of Plankton Research, 30 (8): 963–968.

    Article  Google Scholar 

  • Eilers H, Pernthaler J, Amann R. 2000a. Succession of pelagic marine bacteria during enrichment: a close look at cultivation-induced shifts. Applied and Environ mental Microbiology, 66 (11): 4 634–4 640.

    Article  Google Scholar 

  • Eilers H, Pernthaler J, Glöckner F O, Amann R. 2000b. Culturability and in situ abundance of pelagic bacteria from the North Sea. Applied and Environ mental Microbiology, 66 (7): 3 044–3 051.

    Article  Google Scholar 

  • Glöckner F O, Fuchs B M, Amann R. 1999. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Applied and Environ mental Microbiology, 65 (8): 3 721–3 726.

    Google Scholar 

  • Gómez-Consarnau L, Lindh M V, Gasol J M, Pinhassi J. 2012. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ mental Microbiology, 14 (9): 2 361–2 378.

    Article  Google Scholar 

  • Gómez-Pereira P R, Schüler M, Fuchs B M, Bennke C, Teeling H, Waldmann J, Richter M, Barbe V, Bataille E, Glöckner F O, Amann R. 2012. Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean. Environ mental Microbiology, 14 (1): 52–66.

    Article  Google Scholar 

  • González J M, Simó R, Massana R, Covert J S, Casamayor E O, Pedrós-Alió C, Moran M A. 2000. Bacterial community structure associated with a dimethylsulfoniopropionateproducing North Atlantic algal bloom. Applied and Environ mental Microbiology, 66 (10): 4 237–4 246.

    Article  Google Scholar 

  • Hamner W M, Dawson M N. 2009. A review and synthesis on the systematics and evolution of jellyfish blooms: advantageous aggregations and adaptive assemblages. Hydrobio logia, 616 (1): 161–191.

    Article  Google Scholar 

  • Hansson L J, Norrman B. 1995. Release of dissolved organic carbon (DOC) by the scyphozoan jellyfish Aurelia aurita and its potential influence on the production of planktic bacteria. Marine Biology, 121 (3): 527–532.

    Article  Google Scholar 

  • Hao W J, Gerdts G, Peplies J, Wichels A. 2015. Bacterial communities associated with four ctenophore genera from the German Bight (North Sea). FEMS Microbiology Ecology, 91 (1): 1–11.

    Article  Google Scholar 

  • Hay S J, Hislop J R G, Shanks A M. 1990. North Sea Scyphomedusae; summer distribution, estimated biomass and significance particularly for 0-group Gadoid fish. Neth erlands Journal of Sea Research, 25 (1-2): 113–130.

    Article  Google Scholar 

  • Hedges J I. 1992. Global biogeochemical cycles: progress and problems. Marine Chemistry, 39 (1-3): 67–93.

    Article  Google Scholar 

  • Hopkinson BM, Barbeau KA. 2012. Iron transporters in marine prokaryotic genomes and metagenomes. Environmental Microbiology, 14: 114–128.

    Article  Google Scholar 

  • Hoppe H G. 1991. Microbial extracellular enzyme activity: a new key parameter in aquatic ecology. In: Chróst R J ed. Microbial Enzymes in Aquatic Environments. Springer, New York. p.60–83.

    Chapter  Google Scholar 

  • Kim Y W, Lee S H, Hwang I G, Yoon K S. 2012. Effect of temperature on growth of Vibrio para p hemolyticus and Vibrio vulnificus in flounder, salmon sashimi and oyster meat. Int ernational Journal of Environ mental Research and Public Health, 9 (12): 4 662–4 675.

    Article  Google Scholar 

  • Kirchman D L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiology Ecology, 39 (2): 91–100.

    Google Scholar 

  • Kisand V, Rocker D, Simon M. 2008. Significant decomposition of riverine humic-rich DOC by marine but not estuarine bacteria assessed in sequential chemostat experiments. Aquatic Microbial Ecology, 53: 151–160.

    Article  Google Scholar 

  • Kujawinski E B. 2011. The impact of microbial metabolism on marine dissolved organic matter. Annual Review of Marine Science, 3: 567–599.

    Article  Google Scholar 

  • Lebrato M, de Jesus Mendes P, Steinberg D K, Cartes J E, Jones B M, Birsa L M, Benavides M, Oschlies A. 2013. Jelly biomass sinking speed reveals a fast carbon export mechanism. Limnology and Oceanography, 58 (3): 1 113–1 122.

    Article  Google Scholar 

  • Llobet-Brossa E, Rosselló-Mora R, Amann R. 1998. Microbial community composition of Wadden Sea sediments as revealed by fluorescence in situ hybridization. Applied and Environ mental Microbiology, 64 (7): 2 691–2 696.

    Google Scholar 

  • Lucas C H, Graham W M, Widmer C. 2012. Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Adv ances in Marine Biology, 63: 133–196.

    Article  Google Scholar 

  • Martinez J, Smith D C, Steward G F, Azam F. 1996. Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquatic Microbial Ecology, 10: 223–230.

    Article  Google Scholar 

  • McBride M J, Xie G, Martens E C, Lapidus A, Henrissat B, Rhodes R G, Goltsman E, Wang W, Xu J, Hunnicutt D W, Staroscik A M, Hoover T R, Cheng Y Q, Stein J L. 2009. Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis. Applied and Environmental Microbiology, 75 (21): 6 864–6 875.

    Article  Google Scholar 

  • McCarthy M D, Hedges J I, Benner R. 1998. Major bacterial contribution to marine dissolved organic nitrogen. Science, 281 (5374): 231–234.

    Article  Google Scholar 

  • Möller H. 1980. Population dynamics of Aurelia aurita medusae in Kiel Bight, Germany (FRG). Marine Biology, 60 (2-3): 123–128.

    Article  Google Scholar 

  • Nagata T. 2000. Production mechanisms of dissolved organic matter. In: Kirchman D L ed. Microbial Ecology of the Oceans. 2nd edn. Wiley, New York. p.121–152.

    Google Scholar 

  • Nagata T. 2008. Organic matter-bacteria interactions in seawater. In: Kirchman D L ed. Microbial Ecology of the Oceans. 2nd edn. Wiley, New York. p.207–241.

    Chapter  Google Scholar 

  • Ogawa H, Tanoue E. 2003. Dissolved organic matter in oceanic waters. Journal of Oceanogr aphy, 59 (2): 129–147.

    Article  Google Scholar 

  • Parsons T R, Lalli C M. 2002. Jellyfish population explosions: revisiting a hypothesis of possible causes. La Mer, 40: 111–121.

    Google Scholar 

  • Pernthaler A, Pernthaler J, Amann R. 2002. Fluorescence in situ hybridization and catalyzed reporter deposition for the Identification of marine bacteria. Applied and Environ mental Microbiology, 68 (6): 3 094–3 101.

    Article  Google Scholar 

  • Pernthaler A, Pernthaler J, Amann R. 2004. Sensitive multicolor fluorescence in situ hybridization for the identification of environmental microorganisms. In: Kowalchuk G A, de Bruijn F, Head I M, Van der Zijpp A J, van Elsas J D eds. Molecular Microbial Ecology Manual. 2nd edn. Kluwer Academic Press, Dordrecht. p.711–725.

    Google Scholar 

  • Pinhassi J, Berman T. 2003. Differential growth response of colony-forming α- and γ-proteobacteria in dilution culture and nutrient addition experiments from Lake Kinneret (Israel), the eastern Mediterranean Sea, and the Gulf of Eilat. Applied and Environ mental Microbiology, 69 (1): 199–211.

    Article  Google Scholar 

  • Pinhassi J, Sala M M, Havskum H, Peters F, Guadayol Ò, Malits A, Marrasé C. 2004. Changes in bacterioplankton composition under different phytoplankton regimens. Applied and Environ mental Microbiology, 70 (11): 6 753–6 766.

    Article  Google Scholar 

  • Pitt K A, Welsh D T, Condon R H. 2009. Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production. Hydrobiologia, 616 (1): 133–149.

    Article  Google Scholar 

  • Ranjard L, Brothier E, Nazaret S. 2000. Sequencing bands of ribosomal intergenic spacer analysis fingerprints for characterization and microscale distribution of soil bacterium populations responding to mercury spiking. Applied and Environ mental Microbiology, 66 (12): 5 334–5 339, https://doi.org/10.1128/AEM.66.12.5334-5339.2000.

    Article  Google Scholar 

  • Riemann L, Azam F. 2002. Widespread N -acetyl- D -glucosamine uptake among pelagic marine bacteria and its ecological implications. Applied and Environmental Microbiology, 68 (11): 5 554–5 562.

    Article  Google Scholar 

  • Riemann L, Steward G F, Azam F. 2000. Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Applied and Environ mental Microbiology, 66 (2): 578–587.

    Article  Google Scholar 

  • Riemann L, Titelman J, Bamstedt U. 2006. Links between jellyfish and microbes in a jellyfish dominated fjord. Marine Ecology Progress Series, 325: 29–42.

    Article  Google Scholar 

  • Russell F S. 1970. The Medusae of the British Isles. II. Pelagic Scyphozoa with a Supplement to the First Volume on Hydromedusae. Cambridge University Press, Cambridge.

    Google Scholar 

  • Sapp M, Wichels A, Wiltshire K H, Gerdts G. 2007. Bacterial community dynamics during the winter-spring transition in the North Sea. FEMS Microbiology Ecology, 59 (3): 622–637.

    Article  Google Scholar 

  • Simon M, Glöckner F O, Amann R. 1999. Different community structure and temperature optima of heterotrophic picoplankton in various regions of the Southern Ocean. Aquatic Microbial Ecology, 18: 275–284.

    Article  Google Scholar 

  • Steinberg D K, Saba G K. 2008. Nitrogen consumption and metabolism in marine zooplankton. In: Capone D G, Bronk D A, Mulholland M R, Carpenter E J eds. Nitrogen in the Marine Environment. 2nd edn. Academic Press, Amsterdam.

    Google Scholar 

  • Teeling H, Fuchs B M, Becher D, Klockow C, Gardebrecht A, Bennke C M, Kassabgy M, Huang S X, Mann A J, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann F D, Callies U, Gerdts G, Wichels A, Wiltshire K H, Glöckner F O, Schweder T, Amann R. 2012. Substratecontrolled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science, 336 (6081): 608–611.

    Article  Google Scholar 

  • Tinta T, Kogovšek T, Malej A, Turk V. 2012. Jellyfish modulate bacterial dynamic and community structure. PLoS One, 7 (6): e39274.

    Article  Google Scholar 

  • Tinta T, Malej A, Kos M, Turk V. 2010. Degradation of the Adriatic medusa Aurelia sp. by ambient bacteria. Hydrobiologia, 645 (1): 179–191.

    Article  Google Scholar 

  • Titelman J, Riemann L, Sørnes T A, Nilsen T, Griekspoor P, Båmstedt U. 2006. Turnover of dead jellyfish: stimulation and retardation of microbial activity. Marine Ecology Progress Series, 325: 43–58.

    Article  Google Scholar 

  • Zeder M, Ellrott A, Amann R. 2011. Automated sample area definition for high-throughput microscopy. Cytometry. Part A, 79 (4): 306–310.

    Article  Google Scholar 

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Acknowledgement

This study was part of a Ph.D. thesis within the Food Web Project at the Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research (Germany), and we are grateful for the funding from the China Scholarship Council. Many thanks to Jutta Niggemann and Thorsten Dittmar (ICBM COU Oldenburg) who supported the preparation of the DOM free seawater strongly with material and technical support. Furthermore, we thank the crew of the AADE research vessel for providing samples as well as the entire team of the AWI Food Web Project.

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Correspondence to Wenjin Hao.

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Hao, W., Wichels, A., Fuchs, B. et al. Bacterial community succession in response to dissolved organic matter released from live jellyfish. J. Ocean. Limnol. 37, 1229–1244 (2019). https://doi.org/10.1007/s00343-019-8106-0

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