Abstract
Spatial increases and temporal shifts in outbreaks of gelatinous plankton have been observed over the past several decades in many estuarine and coastal ecosystems. The effects of these blooms on marine ecosystem functioning and particularly on the dynamics of the heterotrophic bacteria are still unclear. The response of the bacterial community from a Mediterranean coastal lagoon to the addition of dissolved organic matter (DOM) from the jellyfish Aurelia aurita, corresponding to an enrichment of dissolved organic carbon (DOC) by 1.4, was assessed for 22 days in microcosms (8 l). The high bioavailability of this material led to (i) a rapid mineralization of the DOC and dissolved organic nitrogen from the jellyfish and (ii) the accumulation of high concentrations of ammonium and orthophosphate in the water column. DOM from jellyfish greatly stimulated heterotrophic prokaryotic production and respiration rates during the first 2 days; then, these activities showed a continuous decay until reaching those measured in the control microcosms (lagoon water only) at the end of the experiment. Bacterial growth efficiency remained below 20 %, indicating that most of the DOM was respired and a minor part was channeled to biomass production. Changes in bacterial diversity were assessed by tag pyrosequencing of partial bacterial 16S rRNA genes, DNA fingerprints, and a cultivation approach. While bacterial diversity in control microcosms showed little changes during the experiment, the addition of DOM from the jellyfish induced a rapid growth of Pseudoalteromonas and Vibrio species that were isolated. After 9 days, the bacterial community was dominated by Bacteroidetes, which appeared more adapted to metabolize high-molecular-weight DOM. At the end of the experiment, the bacterial community shifted toward a higher proportion of Alphaproteobacteria. Resilience of the bacterial community after the addition of DOM from the jellyfish was higher for metabolic functions than diversity, suggesting that jellyfish blooms can induce durable changes in the bacterial community structure in coastal lagoons.
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References
Aminot A, Kérouel R (2007) Dosage automatique des nutriments dans les eaux marines. Méthodes en flux continu. Ifremer, MEDD, Quae (eds) (in French)
Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85:523–536
Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791
Bengtsson MM, Wagner K, Burns NR, Herberg ER, Wanek W, Kaplan LA, Battin TJ (2014) No evidence of aquatic priming effects in hyporheic zone microcosms. Sci Rep 4:5187
Berdjeb L, Pollet T, Domaizon I, Jacquet S (2011) Effect of grazers and viruses on bacterial community structure and production in two contrasting trophic lakes. BMC Microbiol 11:88
Berggren M, Lapierre J-F, del Giorgio PA (2012) Magnitude and regulation of bacterioplankton respiratory quotient across freshwater environmental gradients. ISME J 6:984–993
Bonnet D, Molinero JC, Schohn T, Daly Yahia MN (2012) Seasonal changes in the population dynamics of Aurelia aurita in Thau lagoon. Cah Biol Mar 53:343–347
Briand E, Pringault O, Jacquet S, Torréton J-P (2004) The use of oxygen microprobes tomeasure bacterial respiration for determining bacterioplankton growth efficiency. Limnol Oceanogr Methods 2:406–416
Cauwet G (1994) HTCO method for dissolved organic carbon analysis in seawater: influence of catalyst on blank estimation. Mar Chem 47:55–64
Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser 43:1–10
Collos Y, Harrison PJ (2012) Acclimation and toxicity of high ammonium concentrations to unicellular algae. Mar Pollut Bull 80:8–23
Condon RH, Steinberg DK, Del Giorgio PA, Bouvier TC, Bronk DA, Graham WM, Ducklow HW (2011) Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc Natl Acad Sci U S A 108:10225–10230
Condon RH et al (2012) Questioning the rise of gelatinous. Bioscience 62:160–169
Cotner JB, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121
Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga–Flavobacter cluster consuming low- and high molecular-weight dissolved organic matter. Appl Environ Microbiol 66:1692–1697
De Wit R (2011) Biodiversity of coastal lagoon ecosystems and their vulnerability to global change. In: Grillo O, Venore G (ed) Ecosystems biodiversity. Tech Open Access Publisher pp 29–40
del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541
del Giorgio PA, Condon R, Bouvier T, Longnecker K, Bouvier C, Sherr E, Gasol JM (2011) Coherent patterns in bacterial growth, growth efficiency, and leucine metabolism along a northeastern Pacific inshore–offshore transect. Limnol Oceanogr 56:1–16
Dinasquet J, Granhag L, Riemann L (2012) Stimulated bacterioplankton growth and selection for certain bacterial taxa in the vicinity of the ctenophore Mnemiopsis leidyi. Front Microbiol 3:302
Dinasquet J, Kragh T, Schrøter M-L, Søndergard M, Riemann L (2013) Functional and compositional succession of bacterioplankton in response to a gradient in bioavailable dissolved organic carbon. Environ Microbiol 15:2616–2628
Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125
Ducklow HW, Carlson CA (1992) Oceanic bacterial production. Adv Microb Ecol 12:113–181
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Fagervold SK, Urios L, Intertaglia L, Batailler N, Lebaron P, Suzuki MT (2013) Pleionea mediterranea gen. nov., sp. nov., a gammaproteobacterium isolated from coastal seawater. Int J Syst Evol Microbiol 63:2700–2705
Fernández-Gómez B, Richter M, Schüler M, Pinhassi J, Acinas SG, González JM, Pedrós-Alió C (2012) Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7:1026–1037
Ferretti JA, Calesso DF (2011) Toxicity of ammonia to surf clam (Spisula solidissima) larvae in saltwater. Mar Environ Res 71:189–194
Fonte ES, Amado AM, Meirelles-Pereira F, Esteves FA, Rosado AS, Farjalla VF (2013) The combination of different carbon sources enhances bacterial growth efficiency in aquatic ecosystems. Microb Ecol 66:871–878
Ghai R, Mizuno CM, Picazo A, Camacho A, Rodriguez-Valera F (2013) Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep 3:2471
Ghiglione JF, Murray AE (2012) Pronounced summer to winter differences and higher wintertime richness in coastal Antarctic marine bacterioplankton. Environ Microbiol 14:617–629
Ghiglione JF, Larcher M, Lebaron P (2005) Spatial and temporal scales of variation in bacterioplankton community structure in the NW Mediterranean Sea. Aquat Microb Ecol 40:229–240
Guenet B, Danger M, Harrault L, Allard B, Jauset-Alcala M, Bardoux G, Benest D, Abbadie L, Lacroix G (2014) Fast mineralization of land-born C in inland waters: first experimental evidences of aquatic priming effect. Hydrobiologia 721:35–44
Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504
Holmes RM, Aminot A, Kérouel R, Hooker BA, Petersen BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808
Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898
Jürgens K, Massana R (2008) Protistan grazing on marine bacterioplankton. In: Kirchman DL (ed) Microbial ecology of the oceans, 2nd edn. Wiley, Hoboken, pp 383–441
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon: a prokaryotic 16S rRNA Gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721
Kirschner AKT, Wihlidal P, Velimirov B (2004) Variability and predictability of the empirical conversion factor for converting 3H-thymidine uptake into bacterial carbon production for a eutrophic lake. J Plank Res 26:1559–1566
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498
Lawaetz AJ, Stedmon CA (2009) Fluorescence intensity calibration using the Raman scatter peak of water. Appl Spectrosc 63:936–940
Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier Science BV, Amsterdam
Lo W-T, Chen IL (2008) Population succession and feeding of scyphomedusae, Aurelia aurita, in a eutrophic tropical lagoon in Taiwan. Estuar Coast Shelf Sci 76:227–238
Lo W-T, Purcell JE, Hung J-J, Su H-M, Hsu P-K (2008) Enhancement of jellyfish (Aurelia aurita) populations by extensive aquaculture rafts in a coastal lagoon in Taiwan. ICES J Mar Sci 65:453–461
Massana R, Pedrós-Alió C, Casamayor EO, Gasol JM (2001) Changes in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters. Limnol Oceanogr 46:1181–1188
McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, Chisholm SW, DeLong EF (2010) Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci U S A 107:16420–16427
Nagata T, Meon B, Kirchman DL (2003) Microbial degradation of peptidoglycan in seawater. Limnol Oceanogr 48:745–754
Noble RT, Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14:113–118
Ovchinnikova TV, Balandin SV, Aleshina GM, Tagaev AA, Leonova YF, Krasnodembsky ED, Men’shenin AV, Kokryakov VN (2006) Aurelin, a novel antimicrobial peptide from jellyfish Aurelia aurita with structural features of defensins and channel-blocking toxins. Biochem Biophys Res Commun 348:514–523
Pedrós-Alió C (2012) The rare bacterial biosphere. Annu Rev Mar Sci 4:449–466
Pimm SL (1984) The complexity and stability of ecosystems. Nature 307:321–326
Pinhassi J, Azam F, Hemphala J, Long RA, Martinez J, Zweifel UL, Hagström A (1999) Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat Microb Ecol 17:13–26
Pitt KA, Welsh DT, Condon RH (2009) Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production. Hydrobiologia 616:133–149
Pizzetti I, Fuchs BM, Gerdts G, Wichels A, Wiltshire KH, Amann R (2011) Temporal variability of coastal Planctomycetes clades at Kabeltonne Station, North Sea. Appl Environ Microbiol 77:5009–5017
Pujo-Pay M, Raimbault P (1994) Improvement of the wet oxidation procedure for simultaneous determination of particulate organic nitrogen and phosphorus collected on filters. Mar Ecol Prog Ser 105:203–207
Purcell JE (2012) Jellyfish and Ctenophore blooms coincide with human proliferations and environmental perturbations. Annu Rev Mar Sci 4:1.1–1.27
Riemann L, Titelman J, Båmstedt U (2006) Links between jellyfish and microbes in a jellyfish dominated fjord. Mar Ecol Prog Ser 325:29–42
Sarmento H, Gasol JM (2012) Use of phytoplankton derived dissolved organic carbon by bacterioplankton large phylogenetic groups. Environ Microbiol 14:2348–2360
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Schneider G (1988) Chemische zusammensetzung und biomasseparameter der ohrenqualle Aurelia aurita. Helgoländer Meeresunters 42:319–327
Shade A, Read JS, Welkie DG, Kratz TK, Wu CH, McMahon KD (2011) Resistance, resilience and recovery: aquatic bacterial dynamics after water column disturbance. Environ Microbiol 13:2752–2767
Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 103:12115–12120
Staden R, Judge DP, Bonfield JK (2003) Managing sequencing projects in the GAP4 environment. In: Krawetz SA, Womble DD (eds) Introduction to bioinformatics. A theoretical and practical approach. Humana, Totawa
Tinta T, Malej A, Kos M, Turk V (2010) Degradation of the Adriatic medusa Aurelia sp. by ambient bacteria. Hydrobiologia 645:179–191
Tinta T, Kogovsek T, Malej A, Turk V (2012) Jellyfish modulate bacterial dynamic and community structure. Plos One 7:e39274
Titelman J, Riemann L, Sørnes TA, Nilsen T, Griekspoor P, Båmstedt U (2006) Turnover of dead jellyfish: stimulation and retardation of microbial activity. Mar Ecol Prog Ser 325:43–58
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
West EJ, Welsh DT, Pitt KA (2009) Influence of decomposing jellyfish on the sediment oxygen demand and nutrient dynamics. Hydrobiologia 616:151–160
Williams T, Joux F, Lauro FM, Matallana-Surget S, Cavicchioli R (2011) Physiology of marine oligotrophic ultramicrobacteria. In: Horikoshi K, Antranikian G, Robb F, Stetter K, Bull AT (eds) Extremophiles handbook. Springer, Heidelberg, pp 1179–1199
Yamamoto J, Hirose M, Ohtani T, Sugimoto K, Hirase K, Shimamoto N, Shimura T, Honda N, Fujimori Y, Mukai T (2008) Transportation of organic matter to the sea floor by carrion falls of the giant jellyfish Nemopilema nomurai in the Sea of Japan. Mar Biol 153:311–317
Zemb O, Haegeman B, Delgenes JP, Lebaron P, Godon JJ (2007) SAFUM: statistical analysis of SSCP fingerprints using PCA projections, dendrograms and diversity estimators. Mol Ecol Notes 7:767–770
Acknowledgments
This study was supported by the CNRS-EC2CO program through the GELPROC project (2010–2012): “Interactions between gelatinous plankton and dynamics of prokaryotic communities.” We wish to thank P. Roman for the jellyfish maintenance. We are grateful to the BIO2MAR platform (http://bio2mar.obs-banyuls.fr) for providing technical support and access to instrumentation. We thank the two anonymous reviewers for their comments that greatly improved the manuscript.
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Blanchet, M., Pringault, O., Bouvy, M. et al. 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 Sci Pollut Res 22, 13638–13653 (2015). https://doi.org/10.1007/s11356-014-3848-x
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DOI: https://doi.org/10.1007/s11356-014-3848-x