Microbial Diversity in Inactive Chimney Structures from Deep-Sea Hydrothermal Systems

Abstract

Massive chimney structures, which are characteristic of many hydrothermally active zones, harbor diverse microbial communities containing both thermophilic and hyperthermophilic microbes. However, vent chimneys ultimately become hydrothermally inactive, and the changes that occur in the microbial communities upon becoming inactive have not been documented. We thus collected inactive chimneys from two geologically and geographically distinct hydrothermal fields, Iheya North in the western Pacific Ocean and the Kairei field in the Indian Ocean. The chimneys displayed easily distinguishable strata, which were analyzed with regard to both mineralogical and microbiological properties. X-ray diffraction pattern and energy-dispersive spectroscopic analyses revealed that the main mineral components of the chimney substructures from Iheya North and the Kairei field were barite (BaSO4) and chalcopyrite (CuFeS2), respectively. Microbial cell densities in the substructures determined by DAPI counting ranged from 1.7 × 107 cells g−1 to 3.0 × 108 cells g−1 . The proportions of archaeal rDNA in the whole microbial rDNA assemblages in all substructures were, at most, a few percent as determined by quantitative fluorogenic PCR. The microbial rDNA clone analysis and whole-cell fluorescence in situ hybridization revealed a community that was decidedly different from any communities previously reported in active chimneys. Curiously, both samples revealed the abundant presence of a group of Bacteria related to a magnetosome-bearing bacterium, “ Magnetobacterium bavaricum” of the Nitrospirae division. These results suggest that inactive chimneys provide a distinct microbial habitat.

This is a preview of subscription content, access via your institution.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

References

  1. 1.

    SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694

    PubMed  Google Scholar 

  2. 2.

    JA Baross JW Deming (1995) Growth at high temperatures: isolation, taxonomy, physiology, and ecology. DM Karl (Eds) The Microbiology of Deep-Sea Hydrothermal vents. CRC Press Boca Raton, FL 169–217

    Google Scholar 

  3. 3.

    DA Benson MS Boguski DJ Lipman J Ostell BFF Ouellette (1998) ArticleTitleGenBank. Nucleic Acids Res 26 1–7 Occurrence Handle10.1093/nar/26.1.1 Occurrence Handle1:CAS:528:DyaK1cXovVWlug%3D%3D Occurrence Handle9399790

    Article  CAS  PubMed  Google Scholar 

  4. 4.

    RP Blakemore NA Blakemore DA Bazylinski TT Moench (1989) Magnetotactic bacteria. JT Stakey MP Bryant N Pfennig JG Hol (Eds) Bergey’s Manual of Systematic Bacteriology, vol 3. Williams & Wilkins Baltimore 1882–1889

    Google Scholar 

  5. 5.

    DA Butterfield (2000) Deep ocean hydrothermal vents. H Sigurdsson BF Houghton SR McNutt H Rymer J Stix (Eds) Encyclopedia of Volcanoes. Academic Press San Diego 857–875

    Google Scholar 

  6. 6.

    EF Delong (1992) ArticleTitleArchaea in coastal marine environments. Proc Natl Acad Sci USA 89 5685–5689 Occurrence Handle1:CAS:528:DyaK38Xks1Kntrs%3D Occurrence Handle1608980

    CAS  PubMed  Google Scholar 

  7. 7.

    KJ Edwards PL Bond TM Gihring JF Banfield (2000) ArticleTitleAn archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287 1796–1799 Occurrence Handle1:CAS:528:DC%2BD3cXhvVWltb0%3D Occurrence Handle10710303

    CAS  PubMed  Google Scholar 

  8. 8.

    Y Fouquet P Cambon A Falick D Rickard D Desbruyers (1996) ArticleTitleFormation of large sulfide mineral deposits along fast spreading ridges: Example from off-axial deposits at 12°43’N on the East Pacific Rise. Earth Planet Sci Lett 144 147–162 Occurrence Handle10.1016/0012-821X(96)00142-2 Occurrence Handle1:CAS:528:DyaK28Xmt1agu7c%3D

    Article  CAS  Google Scholar 

  9. 9.

    T Gamo H Chiba T Yomanaka T Okudaira J Hashimoto S Tsuchida J Ishibashi S Kataoka U Tsunogai K Okamura Y Sano R Shinjo (2001) ArticleTitleChemical characteristics of newly discovered black smoker fluids and associated hydrothermal plumes at the Rodriguez Triple Junction, Central Indian Ridge. Earth Planet Sci Lett 193 371–379 Occurrence Handle10.1016/S0012-821X(01)00511-8 Occurrence Handle1:CAS:528:DC%2BD3MXovFymtrs%3D

    Article  CAS  Google Scholar 

  10. 10.

    JA Huber DA Butterfield JA Baross (2002) ArticleTitleTemporal changes in archaeal diversity and chemistry in a mid-ocean ridge subseafloor habitat. Appl Environ Microbiol 68 1585–1594 Occurrence Handle10.1128/AEM.68.4.1585-1594.2002 Occurrence Handle1:CAS:528:DC%2BD38XivFGltrk%3D Occurrence Handle11916672

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    SE Humphris PM Herzig DJ Miller JC Alt K Becker D Brown G Bruegmann H Chiba Y Fouquet JB Gemmell G Guerin MD Hannington NG Holm JJ Honnorez GJ Iturrino R Knott R Ludwig K Nakamura S Petersen AL Reysenbach OA Rona S Smith AA Sturz MK Tivey X Zhao (1995) ArticleTitleThe internal structure of an active sea-floor massive sulphide deposit. Nature 377 713–716 Occurrence Handle10.1038/377713a0 Occurrence Handle1:CAS:528:DyaK2MXovFyguro%3D

    Article  CAS  Google Scholar 

  12. 12.

    J Ishibashi T Urabe (1995) Hydrothermal activity related to arc-backarc magmatism in the western Pacific. B Taylor (Eds) Backarc Basins: Tectonics and Magmatism. Plenum Press New York 451–495

    Google Scholar 

  13. 13.

    DM Karl (1995) Ecology of free-living, hydrothermal vent communities. DM Karl (Eds) The Microbiology of Deep-Sea Hydrothermal Vents. CRC Press Boca Raton, FL 35–124

    Google Scholar 

  14. 14.

    DJ Lane (1991) 16S/23S rRNA sequencing. E Stackebrandt M Goodfellow (Eds) Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons New York 115–175

    Google Scholar 

  15. 15.

    R Lathe (1985) ArticleTitleSynthetic oligonucleotide probes deduced from amino acid sequence data. Theoretical and practical considerations. J Mol Biol 183 1–12 Occurrence Handle1:CAS:528:DyaL2MXksFSls7Y%3D Occurrence Handle4009718

    CAS  PubMed  Google Scholar 

  16. 16.

    T Maniatis EF Fritsch J Sambrook (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  17. 17.

    TM McCollom EL Shock (1997) ArticleTitleGeochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim Cosmochim Acta 61 4375–4391 Occurrence Handle10.1016/S0016-7037(97)00241-X Occurrence Handle1:CAS:528:DyaK2sXns1egtrw%3D Occurrence Handle11541662

    Article  CAS  PubMed  Google Scholar 

  18. 18.

    AL Reysenbach K Longnecker J Kirshtein (2000) ArticleTitleNovel bacterial and archaeal lineages from an in situ growth chamber deployed at a mid-Atlantic ridge hydrothermal vent. Appl Environ Microbiol 66 3798–3806 Occurrence Handle1:CAS:528:DC%2BD3cXmsVWqu7k%3D Occurrence Handle10966393

    CAS  PubMed  Google Scholar 

  19. 19.

    PA Rona SD Scott (1993) ArticleTitleA special issue on sea-floor hydrothermal mineralization: new perspectives. Econ Geol 88 1935–1976

    Google Scholar 

  20. 20.

    WC Shanks SuffixIII (2001) Stable isotopes in seafloor hydrothermal systems: vent fluids Hydrothermal deposits, hydrothermal alteration, and microbial process. JW Valley DR Cole (Eds) Stable Isotope Geochemistry, 43. SeriesTitleRev Mineral Geochem . . 469–525

    Google Scholar 

  21. 21.

    WC III Shanks JL Bischoff (1980) ArticleTitleGeochemistry, sulfur isotope composition, and accumulation rates of Red Sea geothermal deposits. Econ Geol 74 445–459

    Google Scholar 

  22. 22.

    S Spring R Amann W Ludwig K-H Schleifer H Gemerden N Petersen (1993) ArticleTitleDominating role of an unusual magnetotactic bacterium in the microaerobic zone of a fresh water sediment. Appl Environ Microbiol 59 2397–2403 Occurrence Handle1:CAS:528:DyaK3sXmt1Wnu74%3D

    CAS  Google Scholar 

  23. 23.

    Strunk O, Ludwig W (1995) ARB—a software environment for sequence data. Department of Microbiology, Technical University of Munich, Munich, Germany

  24. 24.

    Swofford DL (1999) PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4.02 ed. Sinauer Associates, Sunderland, MA

  25. 25.

    K Takai Y Fujiwara (2002) Hydrothermal vents: Biodiversity in deep-sea hydrothermal vents. G Bitton (Eds) Encyclopedia of Environmental Microbiology. John Wiley & Sons New York 1604–1617

    Google Scholar 

  26. 26.

    K Takai K Horikoshi (1999) ArticleTitleGenetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152 1285–1297 Occurrence Handle1:CAS:528:DyaK1MXlslSrtr0%3D Occurrence Handle10430559

    CAS  PubMed  Google Scholar 

  27. 27.

    K Takai K Horikoshi (2000) ArticleTitleRapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66 5066–5072 Occurrence Handle10.1128/AEM.66.11.5066-5072.2000 Occurrence Handle1:CAS:528:DC%2BD3cXnvFyqsLc%3D Occurrence Handle11055964

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    K Takai A Inoue K Horikoshi (1999) ArticleTitle Thermaerobacter marianensis gen. nov., sp. nov., an aerobic extremely thermophilic marine bacterium from the 11,000 m deep Mariana Trench. Int J Syst Bacteriol 49 619–62 Occurrence Handle1:CAS:528:DyaK1MXjt1Cru7c%3D Occurrence Handle10319484

    CAS  PubMed  Google Scholar 

  29. 29.

    K Takai T Komatsu F Inagaki K Horikoshi (2001) ArticleTitleDistribution of archaea in a black smoker chimney structure. Appl Environ Microbiol 67 3618–3629 Occurrence Handle1:CAS:528:DC%2BD3MXlvFSksr4%3D Occurrence Handle11472939

    CAS  PubMed  Google Scholar 

  30. 30.

    CL Van Dover SE Humphris D Fornari CM Cavanaugh R Collier SK Goffredi J Hashimoto MD Lilley AL Reysenbach TM Shank KL Von Damm A Banta RM Gellant D Götz D Green J Hall TL Harmer LA Hurtado P Johnson ZP McKiness C Meredith E Olson IL Pan M Turnipseed Y Won CR Young III RC Vrijenhoek (2001) ArticleTitleBiogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294 818–823 Occurrence Handle11557843

    PubMed  Google Scholar 

  31. 31.

    C Vetriani HW Jannasch BJ MACGregor DA Stahl A-L Reysenbach (1999) ArticleTitlePopulation structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65 4375–4384

    Google Scholar 

  32. 32.

    CO Wirsen HW Jannasch SJ Molyneaux (1993) ArticleTitleChemosynthetic microbial activity at Mid-Atlantic ridge hydrothermal vent sites. J Geophys Res 98 9693–9703 Occurrence Handle1:CAS:528:DyaK3sXlt1Cms74%3D

    CAS  Google Scholar 

  33. 33.

    RA Zierenberg Y Fouquet DJ Miller JM Bahr PA Baker T Bjerkgard CA Brunner RC Duckworth RH James KS Lackschewitz LL Marquez P Nehlig JM Peter CA Rigsby PJ Schultheiss WC III Shanks BRT Simoneit M Summit DAH Teagle M Urbat GG Zuffa (1998) ArticleTitleThe deep structure of a sea-floor hydrothermal deposit. Nature 392 485–488 Occurrence Handle10.1038/33126 Occurrence Handle1:CAS:528:DyaK1cXisFentbg%3D

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the captains and crews of the R/Vs Natsushima and Yokosuka and the DSVs Shinkai 2000 and 6500 operation groups for their technical expertise. We also thank Katsuyuki Uematsu and Tadashi Yokoyama for their help with the electron microprobe and X-ray powder diffractometer, respectively. We are grateful to Hisako Hirayama, Takuro Nunoura, Hanako Oida, and Masae Suzuki for their laboratory assistance. Mineralogical characterization was partly performed at the facility of the Mineralogical Institute of University of Tokyo.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Y. Suzuki.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Suzuki, Y., Inagaki, F., Takai, K. et al. Microbial Diversity in Inactive Chimney Structures from Deep-Sea Hydrothermal Systems. Microb Ecol 47, 186–196 (2004). https://doi.org/10.1007/s00248-003-1014-y

Download citation

Keywords

  • Chalcopyrite
  • Metal Sulfide
  • Western Pacific Ocean
  • Related Bacterium
  • Iron Silicate