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Monitoring Microbial Community Composition by Fluorescence In Situ Hybridization During Cultivation of the Marine Cold-Water Sponge Geodia barretti

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Abstract

To determine the stability and specificity of microbes associated with the marine cold-water sponge Geodia barretti during cultivation, we compared the microbial community of freshly retrieved specimens to that of cultivated explants by fluorescence in situ hybridization (FISH). G. barretti hosts a specific homogeneous microbial community in its mesohyl, which is maintained during a cultivation period of 8 months. In 10-day-old explants, bright colonies of unusually large bacterial cells, located predominantly at canal walls, were observed in addition to the common bacteria. Bacteria of the aberrant type included both lineages present in whole sponges and foreign ones, notably numerous genera of sulfate-reducing bacteria. We assume that these represent infectious bacteria that eluded the innate immune system of the sponge. Explants that resist these microbial attacks during the critical phase of cultivation eliminate infectious bacteria. The intrinsic microbial community of G. barretti is not affected by these infections and remains persistent over a cultivation period of at least several months.

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References

  • RI Amann L Krumholz DA Stahl (1990) ArticleTitleFluorescent–oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology J Bacteriol 172 762–770

    Google Scholar 

  • EH Belarbi AC Gómez Y Chisti FG Camacho EM Grima (2003) ArticleTitleProducing drugs from marine sponges Biotechnol Adv 21 585–598 Occurrence Handle10.1016/S0734-9750(03)00100-9

    Article  Google Scholar 

  • H Daims A Brühl R Amann K-H Schleifer M Wagner (1999) ArticleTitleThe domain–specific probe EUB338 is insufficient for the detection of all Bacteria: Development and Evaluation of a more comprehensive probe set Syst Appl Microbiol 22 434–444

    Google Scholar 

  • C Debitus G Guella I Mancini J Waikedre J-P Guemas JL Nicolas F Pietra (1998) ArticleTitleQuinolones from a bacterium and tyrosine metabolites from its host sponge, Suberea creba from the Coral Sea Mar Biotechnol 6 136–141

    Google Scholar 

  • S DeCaralt G Agell M-J Uriz (2003) ArticleTitleLong-term culture of sponge explants: conditions enhancing survival and growth, and assessment of bioactivity Biomol Eng 20 339–347 Occurrence Handle10.1016/S1389-0344(03)00045-5

    Article  Google Scholar 

  • R Devereux MD Kane J Winfrey DA Stahl (1992) ArticleTitleGenus- and group-specific hybridization probes for determinative ans environmental studies of sulfate-reducing bacteria Syst Appl Microbiol 15 601–609

    Google Scholar 

  • AR Duckworth GA Samples AE Wright SA Pomponi (2003) ArticleTitle In vitro culture of the tropical sponge Axinella corrugata (Demospongiae): Effect of food cell concentration on growth, clearance rate, and biosynthesis of stevensine Mar Biotechnol 5 519–527 Occurrence Handle10.1007/s10126-002-0111-0

    Article  Google Scholar 

  • R Ebel M Brenzinger A Kunze HJ Proksch (1997) ArticleTitleWound activation of protoxins in marine sponge Aplysina aerophoba J Chem Ecol 23 1451–1462 Occurrence Handle10.1023/B:JOEC.0000006475.10310.3a

    Article  Google Scholar 

  • J Faulkner (2000) ArticleTitleMarine pharmacology Antonie van Leeuwenhoek 77 135–145 Occurrence Handle10.1023/A:1002405815493

    Article  Google Scholar 

  • AB Friedrich I Fischer P Proksch J Hacker U Hentschel (2001) ArticleTitleTemporal variation of the microbial community associated with the mediterranean sponge Aplysina aerophoba FEMS Microbiol Ecol 38 105–113 Occurrence Handle10.1111/j.1574-6941.2001.tb00888.x

    Article  Google Scholar 

  • MJ Garson AE Flowers RI Webb RD Charan EJ McCaffrey (1998) ArticleTitleA sponge/dinoflagellate association in the haplosclerid demosponge Haliclona sp: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation Cell Tissue Res 293 365–373 Occurrence Handle10.1007/s004410051128

    Article  Google Scholar 

  • FO Glöckner BM Fuchs R Amann (1999) ArticleTitleBacterioplankton composition of lakes and oceans: a first comparison based on fluorescence in situ hybridization Appl Environ Microbiol 65 3721–3726

    Google Scholar 

  • U Hentschel M Schmid M Wagner L Fieseler C Gernert J Hacker (2001) ArticleTitleIsolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola FEMS Microbiol Ecol 35 305–312 Occurrence Handle10.1111/j.1574-6941.2001.tb00816.x

    Article  Google Scholar 

  • U Hentschel J Hopke M Horn AB Friedrich M Wagner J Hacker BS Moore (2002) ArticleTitleMolecular evidence for a uniform microbial community in sponges from different oceans Appl Environ Microbiol 68 4431–4440 Occurrence Handle10.1128/AEM.68.9.4431-4440.2002

    Article  Google Scholar 

  • U Hentschel L Fieseler M Wehrl C Gernert M Steinert J Hacker M Horn (2003) Microbial diversity of marine sponges WEG Müller (Eds) Marine Molecular Biotechnology Springer Berlin 59–88

    Google Scholar 

  • F Hoffmann D Janussen W Dröse G Arp J Reitner (2003a) ArticleTitleHistological investigation of organisms with hard skeletons: a case study of siliceous sponges Biotech Histochem 78 191–199 Occurrence Handle10.1080/10520290310001613042

    Article  Google Scholar 

  • F Hoffmann HT Rapp T Zöller J Reitner (2003b) ArticleTitleGrowth and regeneration in cultivated fragments of the boreal deep water sponge Geodia barretti Bowerbank, 1858 (Geodiidae, Tetractinellida, Demospongiae) J Biotechnol 100 109–118 Occurrence Handle10.1016/S0168-1656(02)00258-4

    Article  Google Scholar 

  • F Hoffmann HT Rapp H Peters T Pape J Reitner (2004) ArticleTitleSedimentary inclusions in the deep-water sponge Geodia barretti (Geodiidae, Demospongiae) from the Korsfjord, Western Norway Sarsia 89 1–8

    Google Scholar 

  • F Hoffmann O Larsen HT Rapp R Osinga (2005a) ArticleTitleOxygen dynamics in choanosomal sponge explants Mar Biol Res 1 160–163

    Google Scholar 

  • F Hoffmann O Larsen V Thiel HT Rapp T Pape W Michaelis J Reitner (2005b) ArticleTitleAn anaerobic world in sponges Geomicrobiol J 22 1–10 Occurrence Handle10.1080/01490450590922505

    Article  Google Scholar 

  • BB Jørgensen (1989) Biogeochemistry of chemoautotrophic bacteria HG Schlegel B Bowien (Eds) Autotrophic Bacteria Science Tech & Springer-Verlag New York 117–146

    Google Scholar 

  • W Manz R Amann W Ludwig M Wagner K-H Schleifer (1992) ArticleTitlePhylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions System Appl Microbiol 15 593–600

    Google Scholar 

  • W Manz M Eisenbrecher TR Neu U Szewzyk (1998) ArticleTitleAbundance and spatial organization of gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides FEMS Microbiol Ecol 25 43–61 Occurrence Handle10.1111/j.1574-6941.1998.tb00459.x

    Article  Google Scholar 

  • W Manz G Arp G Schumann-Kindel U Szewzyk J Reitner (2000) ArticleTitleWidefield deconvolution epifluorescence microscopy combined with fluorescence in situ hybridization reveals the spatial arrangement of bacteria in sponge tissue J Microbiol Methods 40 125–134 Occurrence Handle10.1016/S0167-7012(99)00103-7

    Article  Google Scholar 

  • H Margot C Acebal E Toril R Amils JLF Puentes (2002) ArticleTitleConsistent association of crenarchaeal Archaea with sponges of the genus Axinella Mar Biol 140 739–745 Occurrence Handle10.1007/s00227-001-0740-2

    Article  Google Scholar 

  • AMS Mayer MT Hamann (2004) ArticleTitleMarine pharmacology in 2000: marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiplatelet, antituberculosis, and antiviral activities; affecting the cardiovascular, immune, and nervous systems and other miscellaneous mechanisms of action Mar Biotechnol 6 37–52 Occurrence Handle10.1007/s10126-003-0007-7

    Article  Google Scholar 

  • W Müller B Blumbach I Müller (1999a) ArticleTitleEvolution of the innate and adaptive immune systems: relationships between potential immune molecules in the lowest metazoan phylum (Porifera) and those in vertebrates Transplantation 68 1215–1227 Occurrence Handle10.1097/00007890-199911150-00001

    Article  Google Scholar 

  • WEG Müller W Wimmer W Schatton M Böhm R Batel Z Filic (1999b) ArticleTitleInitiation of an aquaculture of sponges for the sustainable production of bioactive metabolites in open systems: example, Geodia cydonium Mar Biotechnol 1 569–579 Occurrence Handle10.1007/PL00011812

    Article  Google Scholar 

  • WEG Müller VA Grebenjuk GL Pennec H-C Schröder F Brümmer U Hentschel IM Müller H-J Breter (2004) ArticleTitleSustainable production of bioactive compounds by sponges—cell culture and gene cluster approach: a review Mar Biotechnol 6 105–117 Occurrence Handle10.1007/s10126-002-0098-6

    Article  Google Scholar 

  • MHG Munro JW Blunt EJ Dumdei SJH Hickford RE Lill S Li CN Battershill AR Duckworth (1999) ArticleTitleThe discovery and development of marine compounds with pharmaceutical potential J Biotechnol 70 15–25 Occurrence Handle10.1016/S0168-1656(99)00052-8

    Article  Google Scholar 

  • M Mußmann K Ishii R Rabus R Amann (2005) ArticleTitleDiversity and distribution of cultured and uncultured delta Proteobacteria in an intertidal mud flat of the Wadden Sea Environ Microbiol 7 405–418 Occurrence Handle10.1111/j.1462-2920.2005.00708.x

    Article  Google Scholar 

  • M Nickel F Brümmer (2003) ArticleTitle In vitro sponge fragment culture of Chondrosia reniformis (Nardo, 1847) J Biotechnol 100 147–159 Occurrence Handle10.1016/S0168-1656(02)00256-0

    Article  Google Scholar 

  • R Osinga J Tramper RH Wijffels (1999) ArticleTitleCultivation of marine sponges Mar Biotechnol 1 509–532 Occurrence Handle10.1007/PL00011807

    Article  Google Scholar 

  • R Osinga R Kleijn E Groenendijk P Niesink J Tramper RH Wijffels (2001) ArticleTitleDevelopment of in vivo sponge cultures: particle feeding by the tropical sponge Pseudosuberites aff. andrewsi Mar Biotechnol 3 544–554 Occurrence Handle10.1007/s1012601-0078-2

    Article  Google Scholar 

  • T Pape M Blumenberg V Thiel W Michaelis (2004) ArticleTitleBiphytanes as biomarkers for sponge-associated Archaea Boll Mus Ist biol Univ Genova 68 509–515

    Google Scholar 

  • Pape, T, Hoffmann, F, Queric, N-V, Juterzenka, Kv, Reitner, J, Michaelis, W (2006). Dense populations of Archaea associated with the hadromerid demosponge Tentorium semisuberites from Arctic deep waters. Polar Biol DOI: 10.1007/s00300-005-0103-4

    Google Scholar 

  • SA Pomponi (1999) ArticleTitleThe bioprocess—technological potential of the sea J Biotechnol 70 5–13 Occurrence Handle10.1016/S0168-1656(99)00053-X

    Article  Google Scholar 

  • CM Preston KY Wu TF Molinski EF DeLong (1996) ArticleTitleA psychrophilic crenarcheon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov Proc Natl Acad Sci USA 93 6241–6246 Occurrence Handle10.1073/pnas.93.13.6241

    Article  Google Scholar 

  • R Pronzato G Bavestrello C Cerrano G Magnino R Manconi J Pantelis A Sarà M Sidri (1999) ArticleTitleSponge farming in the Mediterranean Sea: new perspectives Memoirs Queensland Mus 44 485–491

    Google Scholar 

  • K Ravenschlag K Sahm C Knoblauch BB Jörgensen R Amann (2000) ArticleTitleCommunity structure, cellular rRNA content, and activity of sulfate-reducing bacteria in marine arctic sediments Appl Environ Microbiol 66 3592–3602 Occurrence Handle10.1128/AEM.66.8.3592-3602.2000

    Article  Google Scholar 

  • HM Reiswig (1981) ArticleTitlePartial carbon and energy budgets of the bacteriosponge Verongia fistularis (Porifera: Demospongiae) in Barbados Mar Ecol Progress Ser 2 273–293

    Google Scholar 

  • DL Santavy P Willenz RR Colwell (1990) ArticleTitlePhenotypic study of bacteria associated with the carribean sclerosponge, Ceratoporella nicholsoni Appl Environ Microbiol 56 1750–1762

    Google Scholar 

  • G Schumann-Kindel M Bergbauer W Manz U Szewyk J Reitner (1997) ArticleTitleAerobic and anaerobic microorganisms in modern sponges: a possible relationship to fossilization-processes Facies 36 268–272

    Google Scholar 

  • D Sipkema HGHJ Heilig ADL Akkermans R Osinga J Tramper RH Wijffels (2003) ArticleTitleSponge-cell culture? A molecular identification method for sponge cells Mar Biotechnol 5 443–449 Occurrence Handle10.1007/s10126-002-0090-1

    Article  Google Scholar 

  • M Sjögren U Goransson AL Johnson M Dahlstrom R Andersson J Bergman PR Jonsson L Bohlin (2004) ArticleTitleAntifouling activity of brominated cyclopeptides from the marine sponge Geodia barretti J Nat Prod 67 368–372 Occurrence Handle10.1021/np0302403

    Article  Google Scholar 

  • S Sölter R Dieckmann M Blumenberg W Francke (2002) ArticleTitleBarettin, revisited? Tetrahedr Lett 43 3385–3386 Occurrence Handle10.1016/S0040-4039(02)00470-7

    Article  Google Scholar 

  • DA Stahl RI Amann (1991) Development and application of nucleic acid probes in bacterial systematics E Stackebrandt M Godfellow (Eds) Sequencing and Hybridization Techniques in Bacterial Systematics John Wiley & Sons Chicester, UK 205–248

    Google Scholar 

  • V Thiel A Jenisch G Wörheide A Löwenberg J Reitner W Michaelis (1999) ArticleTitleMid-chain branched alkanoic acids from “living fossil” demosponges: a link to ancient sedimentary lipids? Org Geochem 30 1–14 Occurrence Handle10.1016/S0146-6380(98)00200-9

    Article  Google Scholar 

  • X Turon MA Becerro MJ Uriz (2000) ArticleTitleDistribution of brominated compounds within the sponge Aplysina aerophoba: coupling of X-ray microanalysis with cryofixation techniques Cell Tissue Res 301 311–322 Occurrence Handle10.1007/s004410000233

    Article  Google Scholar 

  • MD Unson ND Holland DJ Faulkner (1994) ArticleTitleA brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue Mar Biol 124 1–10 Occurrence Handle10.1007/BF00350100

    Article  Google Scholar 

  • J Vacelet (1975) ArticleTitleÉtude en microscopiie électronique de l’association entre bactéries et spongiaires du genre Verongia (Dyctioceratida) J Micros Biol Cell 23 271–288

    Google Scholar 

  • J Vacelet C Donadey (1977) ArticleTitleElectron microscope study of the association between some sponges and bacteria J Exp Mar Biol Ecol 30 301–314 Occurrence Handle10.1016/0022-0981(77)90038-7

    Article  Google Scholar 

  • NS Webster JEM Watts RT Hill (2001) ArticleTitleDetection and phylogenetic analysis of novel Crenarcheote and Euryarcheote 16S ribosomal RNA gene sequence from a Great Barrier Reef sponge Mar Biotechnol 3 600–608 Occurrence Handle10.1007/s10126-001-0065-7

    Article  Google Scholar 

  • CR Wilkinson (1984) ArticleTitleImmunological evidence for Precambrian origin of bacterial symbioses in marine sponges Proc R Soc Lond B 220 509–517 Occurrence Handle10.1098/rspb.1984.0017

    Article  Google Scholar 

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Acknowledgments

We thank the crew of the Marine Biological Station of Bergen University and R/V Hans Brattström for cooperation during sampling and cultivation of sponges. Access to these installations has been supported by the IHP (Improving Human Research Potential) Programme from the European Union through Contract No. HPRI-CT-1999-00056. Wolfgang Dröse is kindly acknowledged for preparation of tissue sections and assistance with FISH. This article represents publication no. 50 of the research program BOSMAN (03F0358 C). Financial support was provided by the Bundesministerium für Bildung und Forschung (BMBF), Germany.

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Hoffmann, F., Rapp, H.T. & Reitner, J. Monitoring Microbial Community Composition by Fluorescence In Situ Hybridization During Cultivation of the Marine Cold-Water Sponge Geodia barretti . Mar Biotechnol 8, 373–379 (2006). https://doi.org/10.1007/s10126-006-5152-3

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