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HAO Wenjin, WICHELS Antje, FUCHS Bernhardt, TANG Xuexi, GERDTS Gunnar. Bacterial community succession in response to dissolved organic matter released from live jellyfish[J]. HaiyangYuHuZhao, 2019, 37(4): 1229-1244

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

HAO Wenjin1,2, WICHELS Antje3, FUCHS Bernhardt4, TANG Xuexi2, GERDTS Gunnar3
1 School of Life Science, Nantong University, Nantong 226019, China;
2 Department of Marine Ecology, College of Marine Life Sciences, Ocean University of China, Qingdao 266000, China;
3 Alfred Wegener Institute for Polar and Marine Research, Biologische Anstalt Helgoland, Helgoland 27498, Germany;
4 Max-Planck-Institute for Marine Microbiology, Department Molecular Ecology, Celsiusstr. 1, Bremen 28359, Germany
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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Received: 2018-05-02   Revised: 2018-07-14
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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. Environmental Microbiology, 9(10):2 417-2 429.
Allers E, Niesner C, Wild C, Pernthaler J. 2008. Microbes enriched in seawater after addition of coral mucus.Applied and Environmental Microbiology, 74(10):3 274-3 278.
Alonso C, Pernthaler J. 2006. Roseobacter and SAR11 dominate microbial glucose uptake in coastal North Sea waters. Environmental Microbiology, 8(11):2 022-2 030.
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, 73:3 528-3 535.
Amon R M W, Benner R. 1994. Rapid cycling of highmolecular-weight dissolved organic matter in the ocean.Nature, 369(6481):549-552.
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.
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.
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. Environmental Microbiology, 8(12):2 201-2 213.
Baumann L, Baumann P, Mandel M, Allen R D. 1972.Taxonomy of aerobic marine eubacteria. Journal of Bacteriology, 110(1):402-429.
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.
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 Oceanography, 51(5):2 077-2 083.
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. Environmental Science and Pollution Research, 22(18):13 638-13 653.
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.
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.
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. Environmental Microbiology, 9(6):1 456-1 463.
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.
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 Environmental Microbiology, 66(12):5 116-5 122.
Cottrell M T, Kirchman D L. 2000b. Natural assemblages of marine proteobacteria and members of the CytophagaFlavobacter cluster consuming low- and high-molecularweight dissolved organic matter. Applied and Environmental Microbiology, 66(4):1 692-1 697.
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. Environmental Microbiology, 15(9):2 616-2 628.
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.
Eilers H, Pernthaler J, Amann R. 2000a. Succession of pelagic marine bacteria during enrichment:a close look at cultivation-induced shifts. Applied and Environmental Microbiology, 66(11):4 634-4 640.
Eilers H, Pernthaler J, Glöckner F O, Amann R. 2000b.Culturability and in situ abundance of pelagic bacteria from the North Sea. Applied and Environmental Microbiology, 66(7):3 044-3 051.
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 Environmental Microbiology, 65(8):3 721-3 726.
Gómez-Consarnau L, Lindh M V, Gasol J M, Pinhassi J. 2012. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environmental Microbiology, 14(9):2 361-2 378.
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. Environmental Microbiology, 14(1):52-66.
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 Environmental Microbiology, 66(10):4 237-4 246.
Hamner W M, Dawson M N. 2009. A review and synthesis on the systematics and evolution of jellyfish blooms:advantageous aggregations and adaptive assemblages.Hydrobiologia, 616(1):161-191.
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.
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.
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. Netherlands Journal of Sea Research, 25(1-2):113-130.
Hedges J I. 1992. Global biogeochemical cycles:progress and problems. Marine Chemistry, 39(1-3):67-93.
Hopkinson BM, Barbeau KA. 2012. Iron transporters in marine prokaryotic genomes and metagenomes.Environmental Microbiology, 14:114-128.
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.
Kim Y W, Lee S H, Hwang I G, Yoon K S. 2012. Effect of temperature on growth of Vibrio paraphemolyticus and Vibrio vulnificus in flounder, salmon sashimi and oyster meat. International Journal of Environmental Research and Public Health, 9(12):4 662-4 675.
Kirchman D L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiology Ecology, 39(2):91-100.
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.
Kujawinski E B. 2011. The impact of microbial metabolism on marine dissolved organic matter. Annual Review of Marine Science, 3:567-599.
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.
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 Environmental Microbiology, 64(7):2 691-2 696.
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.
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.
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.
McCarthy M D, Hedges J I, Benner R. 1998. Major bacterial contribution to marine dissolved organic nitrogen.Science, 281(5374):231-234.
Möller H. 1980. Population dynamics of Aurelia aurita medusae in Kiel Bight, Germany (FRG). Marine Biology, 60(2-3):123-128.
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.
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.
Ogawa H, Tanoue E. 2003. Dissolved organic matter in oceanic waters. Journal of Oceanography, 59(2):129-147.
Parsons T R, Lalli C M. 2002. Jellyfish population explosions:revisiting a hypothesis of possible causes. La Mer, 40:111-121.
Pernthaler A, Pernthaler J, Amann R. 2002. Fluorescence in situ hybridization and catalyzed reporter deposition for the Identification of marine bacteria. Applied and Environmental Microbiology, 68(6):3 094-3 101.
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.
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 Environmental Microbiology, 69(1):199-211.
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 Environmental Microbiology, 70(11):6 753-6 766.
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.
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 Environmental Microbiology, 66(12):5 334-5 339,
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.
Riemann L, Steward G F, Azam F. 2000. Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Applied and Environmental Microbiology, 66(2):578-587.
Riemann L, Titelman J, Bamstedt U. 2006. Links between jellyfish and microbes in a jellyfish dominated fjord.Marine Ecology Progress Series, 325:29-42.
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.
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.
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.
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.
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.
Tinta T, Kogovšek T, Malej A, Turk V. 2012. Jellyfish modulate bacterial dynamic and community structure. PLoS One, 7(6):e39274.
Tinta T, Malej A, Kos M, Turk V. 2010. Degradation of the Adriatic medusa Aurelia sp. by ambient bacteria.Hydrobiologia, 645(1):179-191.
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.
Zeder M, Ellrott A, Amann R. 2011. Automated sample area definition for high-throughput microscopy. Cytometry.Part A, 79(4):306-310.