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Effect of variation of environmental conditions on the microbial communities of deep-sea vent chimneys, cultured in a bioreactor

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Abstract

Both cultivation and molecular techniques were used to investigate the microbial diversity and dynamic of a deep-sea vent chimney. The enrichment cultures performed in a gas-lift bioreactor were inoculated with a black smoker chimney sample collected on TAG site on the mid-Atlantic ridge. To mimic as close as possible environmental conditions, the cultures were performed in oligotrophic medium with nitrogen, hydrogen and carbon dioxide (N2/H2/CO2) gas sweeping. Also, the temperature was first settled at a temperature of 85°C and colloidal sulphur was added. Then, the temperature was lowered to 60°C and sulphur was omitted. Archaeal and bacterial diversity was studied in both culture and natural samples. Through 16S rRNA gene sequences analysis of the enrichment cultures microorganisms affiliated to Archeoglobales, Thermococcales were detected in both conditions while, Deferribacterales and Thermales were detected only at 65°C in the absence of sulphur. Single-stranded conformational polymorphism and quantitative PCR permit to study the microbial community dynamic during the two enrichment cultures. The effect of environmental changes (modification of culture conditions), i.e. temperature, medium composition, electron donors and acceptors availability were shown to affect the microbial community in culture, as this would happen in their environment. The effect of environmental changes, i.e. temperature and medium composition was shown to affect the microbial community in culture, as this could happen in their environment. The modification of culture conditions, such as temperature, organic matter concentration, electron donors and acceptors availability allowed to enrich different population of prokaryotes inhabiting hydrothermal chimneys.

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References

  • Atomi H, Fukui T, Kanai T, Morikawa M, Imanaka T (2004) Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archae 1:263–267

    Article  CAS  Google Scholar 

  • Campbell AC, Palmer MR, Klinkhammer GP, Bowers TS, Edmond JM, Lawrence JR, Casey JF, Thompson G, Humphris S, Rona P, Karson JA (1988) Chemistry of hot springs on the Mid-Atlantic Ridge. Nature 335:514–519

    Article  CAS  Google Scholar 

  • Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N (2002) Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36[deg]14′N, MAR). Chem Geol 191:345–359

    Article  CAS  Google Scholar 

  • Corbari L, Cambon-Bonavita M-A, Long GJ, Grandjean F, Zbinden M, Gaill F, Compère P (2008) Iron oxide deposits associated with the ectosymbiotic bacteria in the hydrothermal vent shrimp Rimicaris exoculata. Biogeosciences 5:1295–1310

    CAS  Google Scholar 

  • Delbes C, Moletta R, Godon JJ (2000) Monitoring of activity dynamics of an anaerobic digester bacterial community using 16S rRNA polymerase chain reaction single strand conformation polymorphism analysis. Environ Microbiol 2:506–515

    Article  PubMed  CAS  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) Seaview and Phylowin two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    PubMed  CAS  Google Scholar 

  • Geslin C, Le Romancer M, Erauso G, Gaillard M, Perrot G, Prieur D (2003) PAV1, the first virus-like particle isolated from a hyperthermophilic Euryarchaeote, Pyrococcus abyssi. J Bacteriol 185:3888–3894

    Article  PubMed  CAS  Google Scholar 

  • Godfroy A, Meunier J-R, Guezennec J, Lesongeur F, Raguénès G, Rimbault A, Barbier G (1996) Thermococcus fumicolans sp. nov. a new hyperthermophilic archaeum isolated from deep-sea hydrothermal vent in North Fiji bassin. Int J Syst Bacteriol 46:1113–1119

    PubMed  CAS  Google Scholar 

  • Godfroy A, Lesongeur F, Raguénès G, Quérellou J, Antoine E, Meunier J-R, Guezennec J, Barbier G (1997) Thermococcus hydrothermalis sp. nov., a new hyperthermophilic archaeon isolated from deep-sea hydrothermal vent. Int J Syst Bacteriol 47:622–626

    PubMed  CAS  Google Scholar 

  • Godfroy A, Raven NDH, Sharp RJ (2000) Physiology and continuous culture of the hyperthermophilic deep-sea vent archaeon Pyrococcus abyssi ST549. FEMS Microbiol Lett 186:127–132

    Article  PubMed  CAS  Google Scholar 

  • Haring M, Vestergaard G, Rachel R, Chen L, Garrett RA, Prangishvili D (2005) Virology: independent virus development outside a host. Nature 436:1101–1102

    Article  PubMed  CAS  Google Scholar 

  • Houghton JL, Seyfried WE Jr, Banta A, Reysenbach A-L (2007) Continuous enrichment culturing of thermophiles under sulfate and nitrate-reducing conditions and at deep-sea hydrostatic pressures. Extremophiles 11:371–382

    Article  PubMed  CAS  Google Scholar 

  • Huber R, Stoffers P, Cheminee JL, Richnow HH, Stetter KO (1990) Hyperthermophilic archaebacteria within the crater and open sea plume of erupting Macdonald seamount. Nature 345:179–182

    Article  Google Scholar 

  • Inagaki F, Takai K, Nealson KH, Horikoshi K (2004) Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the {epsilon}-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54:1477–1482

    Article  PubMed  CAS  Google Scholar 

  • Kashefi K, Tor JM, Holmes DE, Gaw Van Praagh CV, Reysenbach AL, Lovley DR (2002) Geoglobus ahangari gen. nov., sp. nov., a novel hyperthermophilic archaeon capable of oxidizing organic acids and growing autotrophically on hydrogen with Fe(III) serving as the sole electron acceptor. Int J Syst Evol Microbiol 52:719–728

    Article  PubMed  CAS  Google Scholar 

  • Loisel P, Harmand J, Zemb O, Latrille E, Lobry C, Delgenès J-P, Godon J-J (2006) Denaturing gradient electrophoresis (DGE) and single-strand conformation polymorphism (SSCP) molecular fingerprintings revisited by simulation and used as a tool to measure microbial diversity. Environ Microbiol 8:720–731

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Garcia P, Gaill F, Moreira D (2002) Wide bacterial diversity associated with tubes of the vent worm Riftia pachyptila. Environ Microbiol 4:204–215

    Article  PubMed  CAS  Google Scholar 

  • Losekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A, Amann R (2007) Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Appl Environ Microbiol 73:3348–3362

    Article  PubMed  CAS  Google Scholar 

  • Marteinsson VT (1999) Isolation and characterization of Thermus thermophilus Gy1211 from a deep-sea hydrothermal vent. Extremophiles 3:247–251

    Article  PubMed  CAS  Google Scholar 

  • McCliment EA, Voglesonger KM, O’Day PA, Dunn EE, Holloway JR, Cary SC (2006) Colonization of nascent, deep-sea hydrothermal vents by a novel Archaeal and Nanoarchaeal assemblage. Environ Microbiol 8:114–125

    Article  PubMed  CAS  Google Scholar 

  • Miroshnichenko ML, Bonch-Osmolovskaya EA (2006) Recent developments in the thermophilic microbiology of deep sea hydrothermals vents. Extremophiles 10:85–96

    Article  PubMed  Google Scholar 

  • Miroshnichenko ML, Slobodkin AI, Kostrikina NA, L’Haridon S, Nercessian O, Spring S, Stackebrandt E, Bonch-Osmolovskaya EA, Jeanthon C (2003a) Deferribacter abyssi sp. nov., an anaerobic thermophile from deep-sea hydrothermal vents of the Mid-Atlantic Ridge. Int J Syst Evol Microbiol 53:1637–1641

    Article  PubMed  CAS  Google Scholar 

  • Miroshnichenko ML, L’Haridon S, Nercessian O, Antipov AN, Kostrikina NA, Tindall BJ, Schumann P, Spring S, Stackebrandt E, Bonch-Osmolovskaya EA, Jeanthon C (2003b) Vulcanithermus mediatlanticus gen. nov., sp. nov., a novel member of the family Thermaceae from a deep-sea hot vent. Int J Syst Evol Microbiol 53:1143–1148

    Article  PubMed  CAS  Google Scholar 

  • Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73:127–141

    Article  PubMed  CAS  Google Scholar 

  • Muyzer G, Teske A, Wirsen KO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vents samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–172

    Article  PubMed  CAS  Google Scholar 

  • Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiol 148:257–266

    CAS  Google Scholar 

  • Nakagawa S, Takai K, Horikoshi K, Sako Y (2004) Aeropyrum camini sp. nov., a strictly aerobic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 54:329–335

    Article  PubMed  CAS  Google Scholar 

  • Nercessian O, Fouquet Y, Pierre C, Prieur D, Jeanthon C (2005) Diversity of Bacteria and Archaea associated with a carbonate-rich metalliferous sediment sample from the Rainbow vent field on the Mid-Atlantic Ridge. Environ Microbiol 7:698–714

    Article  PubMed  CAS  Google Scholar 

  • Page A, Tivey MK, Stakes DS, Reysenbach A-L (2008) Temporal and spatial archaeal colonization of hydrothermal vent deposits. Environ Microbiol 10:874–884

    Article  PubMed  CAS  Google Scholar 

  • Postec A, Pignet P, Cueff-Gauchard V, Schmitt A, Querellou J, Godfroy A (2005a) Optimisation of growth conditions for continuous culture of the hyperthermophilic archaeon Thermococcus hydrothermalis and development of sulphur-free defined and minimal media. Res Microbiol 156:82–87

    Article  PubMed  CAS  Google Scholar 

  • Postec A, Urios L, Lesongeur F, Ollivier B, Quérellou J, Godfroy A (2005b) Continuous enrichment culture and molecular monitoring to investigate the microbial diversity of thermophiles inhabiting the deep-sea hydrothermal ecosystems. Curr Microbiol 50:138–144

    Article  PubMed  CAS  Google Scholar 

  • Postec A, Lesongeur F, Pignet P, Ollivier B, Quérellou J, Godfroy A (2007) Continuous enrichment cultures: insights into prokaryotic diversity and metabolic interactions in deep-sea vent chimneys. Extremophiles 11:747–757

    Article  PubMed  Google Scholar 

  • Pukall R, Buntefuss D, Fruhling A, Rohde M, Kroppenstedt RM, Burghardt J, Lebaron P, Bernard L, Stackebrandt E (1999) Sulfitobacter mediterraneus sp. nov., a new sulphite-oxidizing member of the {alpha}-proteobacteria. Int J Syst Bacteriol 49:513–519

    Article  PubMed  CAS  Google Scholar 

  • Raven N, Ladwa N, Sharp R (1992) Continuous culture of the hyperthermophilic archaeum Pyrococcus furiosus. Appl Microbiol Biotechnol 38:263–267

    Article  CAS  Google Scholar 

  • Sako Y, Nomura N, Ushida A, Ishida Y, Morii H, Hoaki T, Maruyama T (1996) Aeropyrum pernix, gen. nov; sp. nov., a novel aerobic hyperthermophilic archaeon growing at temperatures up to 100°C. Int J Syst Bacteriol 46:1070–1077

    Article  PubMed  CAS  Google Scholar 

  • Schmidt C, Vuillemin R, Le Gall C, Gaill F, Le Bris N (2008) Geochemical energy sources for microbial primary production in the environment of hydrothermal vent shrimps. Mar Chem 108:18–31

    Article  CAS  Google Scholar 

  • Schrenk MO, Kelley DS, Delaney JR, Baross JA (2003) Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl Environ Microbiol 69:3580–3592

    Article  PubMed  CAS  Google Scholar 

  • Slobodkin A, Campbell B, Cary SC, Bonch-Osmolovskaya E, Jeanthon C (2001) Evidence for the presence of thermophilic Fe(III)-reducing microorganisms in deep-sea hydrothermal vents at 13°N (East Pacific Rise). FEMS Microbiol Ecol 36:235–243

    PubMed  CAS  Google Scholar 

  • Sokolova TG, Jeanthon C, Kostrikina NA, Chernyh NA, Lebedinski AV, Stackebrandt E, Bonch-Osmolovkaya EA (2004) The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 8:317–323

    Article  PubMed  CAS  Google Scholar 

  • Takai K, Horikoshi K (1999) Molecular phylogenetic analysis of archaeal intron-containing genes coding for rRNA obtained from a deep-subsurface geothermal water pool. Appl Environ Microbiol 65:5586–5589

    PubMed  CAS  Google Scholar 

  • Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072

    Article  PubMed  CAS  Google Scholar 

  • Takai K, Nunoura T, Ishibashi J-I, Lupton J, Suzuki R, Hamasaki H, Ueno Y, Kawagucci S, Gamo T, Suzuki Y, Hirayama H, Horikoshi K (2008) Variability in the microbial communities and hydrothermal fluid chemistry at the newly discovered Mariner hydrothermal field, southern Lau Basin. J Geophys Res 113. doi:10.1029/2007JG000521

  • Teske A, Sorensen KB (2007) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2:3–18

    Article  PubMed  CAS  Google Scholar 

  • Tor JM, Amend JP, Lovley DR (2003) Metabolism of organic compounds in anaerobic, hydrothermal sulphate-reducing marine sediments. Environ Microbiol 5:583–591

    Article  PubMed  CAS  Google Scholar 

  • Webster G, Newberry CJ, Fry JC, Weightman AJ (2003) Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16 s rDNA-based techniques: a cautionary tale. J Microbiol Methods 55:155–164

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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Acknowledgments

The authors want to thank the captain and crew of the research vessels Atalante and the Victor team for their work during the EXOMAR cruise (chief scientist Anne Godfroy). Frédérique Duthoit (LMEE, UMR 6197) is thanked for his help on the quantitative-PCR technique. All people working in the department of Microbiology LMEE laboratory in Brest are thanked for the hospitality and help during various part of the work. We also thank Jim Holden, Mathilde Le Roy and Helene Ver Eecke for their contribution on the isolation of ironreducing microorganisms. We thank Yves Fouquet for the mineralogical analysis of the chimney sample. This work was supported by ANR DEEP OASES and Ministère de l’Éducation Nationale, de la Recherche et de la Technologie (grant for NB).

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Authors and Affiliations

  1. Laboratoire de Microbiologie des Environnements Extrêmes, UMR6197 IFREMER, Centre de Brest, BP70/IUEM-Place Nicolas Copernic, 29280, Plouzané, France

    Nathalie Byrne, Françoise Lesongeur, Nadège Bienvenu, Claire Geslin, Karine Alain, Daniel Prieur & Anne Godfroy

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  1. Nathalie Byrne
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  2. Françoise Lesongeur
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  3. Nadège Bienvenu
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  4. Claire Geslin
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  5. Karine Alain
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  6. Daniel Prieur
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  7. Anne Godfroy
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Correspondence to Nathalie Byrne.

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Communicated by A. Driessen.

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Byrne, N., Lesongeur, F., Bienvenu, N. et al. Effect of variation of environmental conditions on the microbial communities of deep-sea vent chimneys, cultured in a bioreactor. Extremophiles 13, 595–608 (2009). https://doi.org/10.1007/s00792-009-0242-6

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  • DOI: https://doi.org/10.1007/s00792-009-0242-6

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