Bacterial community succession in response to dissolved organic matter released from live jellyfish
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摘要
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 j ellyfish 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 lamarcki'i 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 analy sis fingerprints.Catalyzed reporter depo sition 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.
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 j ellyfish 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 lamarcki'i 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 analy sis fingerprints.Catalyzed reporter depo sition 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.
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 j ellyfish 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 lamarcki'i 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 analy sis fingerprints.Catalyzed reporter depo sition 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.
引文
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Alonso-Saez L,Gasol JM.2007.Seasonal variations in thecontributions 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.
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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 j ellyfish A urelia a urita in a Mediterranean coastal lagoon.Environmental Science and Pollution Research,22(1 8):1 3 638-1 3 653.
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Dinasquet J,Kragh T,Schroter M L,Sondergaard 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(1 1):4 634-4 640.
Eilers H,Pernthaler J,Gl(o|¨)ckner 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.
Gl(o|¨)ckner 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,Schuler M,Fuchs B M,Bennke C,Teeling H,Waldmann J,Richter M,Barbe V,Bataille E,Glockner 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.
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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):161-1 91.
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,12 1(3):527-5 32.
Hao W J,Gerdts G,Peplies J,Wichels A.2015.Bacterial communities associated with four ctenophore genera fromthe German Bight(North Sea).FEMS Microbiology Ecology,91(1):1-1 1.
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Hopkinson BM,Barbeau KA.2012.Iron transporters in marine prokaryotic genomes and metagenomes.Environmental Microbiology,14:1 14-128.
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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):1113-1 122.
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Alonso-Saez L,Gasol JM.2007.Seasonal variations in thecontributions 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.
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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,Glockner 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.
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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 j ellyfish A urelia a urita in a Mediterranean coastal lagoon.Environmental Science and Pollution Research,22(1 8):1 3 638-1 3 653.
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Dinasquet J,Kragh T,Schroter M L,Sondergaard 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.
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Eilers H,Pernthaler J,Gl(o|¨)ckner 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.
Gl(o|¨)ckner 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,Schuler M,Fuchs B M,Bennke C,Teeling H,Waldmann J,Richter M,Barbe V,Bataille E,Glockner 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.
Gonzalez J M,Simo R,Massana R,Covert J S,Casamayor E O,Pedrós-AlióC,Moran MA.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):161-1 91.
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,12 1(3):527-5 32.
Hao W J,Gerdts G,Peplies J,Wichels A.2015.Bacterial communities associated with four ctenophore genera fromthe German Bight(North Sea).FEMS Microbiology Ecology,91(1):1-1 1.
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,14:1 14-128.
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,H.wang I G,Yoon K S.2012.Effect of temperature on growth of Vibrio paraphemolyticus and Vibrio vulnficus 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,53:15 1-160.
Kuj awinski 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):1113-1 122.
Llobet-Brossa E,Rossello-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.1 996.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(2 1):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.
M(o|¨)ller 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.2~(nd)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.2~(nd)edn.Wiley,New York,p.207-241.
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