Skip to main content

Advertisement

Log in

Methane-derived carbonate build-ups and associated microbial communities at cold seeps on the lower Crimean shelf (Black Sea)

  • Original Article
  • Published:
Facies Aims and scope Submit manuscript

Abstract

In the euxinic waters of the NW’ Black Sea shelf, tower-like carbonate build-ups up to several metres in height grow at sites of cold methane seepage. These structures are part of an unique microbial ecosystem that shows a considerable biodiversity and a remarkable degree of organization. The accretion of the build-ups is promoted by the growth of centimetre-sized, methane-filled spheres constructed by calcifying microbial mats. Progressive mineralization of these spheres involves the early precipitation of strongly luminescent high-Mg-calcite rich in iron sulphides, and closely interfingered aragonite phases that finally create the stable (mega-) thrombolithic fabric of the towers. Within the microbial mats, microorganisms occur in distinctive spatial arrangements. Major players among the microbial consortia are the archaea groups ANME-1 and ANME-2, Crenarchaeota, and sulphate-reducing bacteria (SRB) of the Desulfosarcina/Desulfobacterium group. The intracellular precipitation of iron sulphides (greigite) by some of these bacteria, growing in close association with ANME-2, suggests iron cycling as an additional biogeochemical pathway involved in the anaerobic oxidation of methane (AOM).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Aloisi G, Bouloubassi I, Heijs SK, Pancost RD, Pierre C, Sinninghe Damsté JS, Gottschal JC, Forney LJ, Rouchy J-M (2002) CH4-consuming microorganisms and the formation of carbonate crusts at cold seeps. Earth Planet Sci Lett 203:195–203

    Article  CAS  Google Scholar 

  • Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990a) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Blumenberg M, Seifert R, Reitner J, Pape T, Michaelis W (2004) Membrane lipid patterns typify distinct anaerobic methanotrophic consortia. Proc Natl Acad Sci USA 101:11111–11116

    Article  CAS  PubMed  Google Scholar 

  • Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jørgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626

    Article  CAS  PubMed  Google Scholar 

  • Brown BV (1993) A further chemical alternative to critical-point-drying for preparing small (or large) flies. Fly Times 11:10

    Google Scholar 

  • Burggraf S, Mayer T, Amann R, Schadhauser S, Woese C, Stetter K (1994) Identifying members of the domain Archaea with rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 60:3112–3119

    CAS  PubMed  Google Scholar 

  • Burne RV, Moore LS (1987) Microbialites: organosedimentary deposits of benthic microbial communities. Palaios 2:241–254

    Google Scholar 

  • Burton EA (1993) Controls on marine carbonate cement mineralogy: review and reassessment. Chem Geol 105:163–179

    Article  CAS  Google Scholar 

  • Campbell KA, Farmer JD, Des Marais D (2002) Ancient hydrocarbon seeps from the Mesozoic convergent margin of California: carbonate geochemistry, fluids and paleoenvironments. Geofluids 2:63–94

    Article  CAS  Google Scholar 

  • Cazenave S, Chapoulie R, Villeneuve G (2003) Cathodoluminescence of synthetic and natural calcite: the effects of manganese and iron on orange emission. Mineral Petrol 78:243–253

    Article  CAS  Google Scholar 

  • Egorov VN, Luth U, Luth C, Gulin MB (1998) Gas seeps in the submarine Dnieper Canyon, Black Sea: acoustic, video and trawl data. In: Luth U, Luth C, Thiel H (eds) Methane gas seep explorations in the Black Sea (MEGASEEBS), Project Report. Ber Zent Meeres Klimaforsch, Univ Hamburg, Hamburg, pp 11–21

    Google Scholar 

  • Frankel RB, Bazylinski DA, Johnson MS, Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73:994–1000

    CAS  PubMed  Google Scholar 

  • Gal’chenko VF (2004) On the problem of anaerobic methane oxidation. Microbiology (translated from Mikrobiologiya) 73:698–707

    CAS  Google Scholar 

  • Goedert JL, Squires RL (1990) Eocene deep-sea communities in localized limestones formed by subduction-related methane seeps, southwestern Washington. Geology 18:1182–1185

    Article  Google Scholar 

  • Greinert J, Bohrmann JG, Suess E (2001) Gas hydrate-associated carbonates and methane-venting at Hydrate Ridge: classification, distribution, and origin of authigenic lithologies. In: Natural gas hydrates: occurrence, distribution, and detection. Geophys Monogr 124, American Geophysics Union

  • Hinrichs K-U, Hayes JM, Sylva SP, Brewer PG, DeLong EF (1999) Methane-consuming archaebacteria in marine sediments. Nature 398:802–805

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann F, Janussen D, Dröse W, Arp G, Reitner J (2003) Histological investigation of organisms with hard skeletons: a case study of siliceous sponges. Biotech Histochem 78

    Google Scholar 

  • Ivanov MV, Polikarpov GG, Lein AY, Galtchenko VF, Egorov VN, Gulin SB, Gulin MB, Rusanov II, Miller YM, Kuptsov VI (1991) Biogeochemistry of the carbon cycle in the region of methane gas seeps of the Black Sea. Dokl Akad Nauk USSR 320:1235–1240

    Google Scholar 

  • Krüger M, Meyerdierks A, Glöckner FO, Amann R, Widdel F, Kube M, Reinhardt R, Kahnt J, Böcher R, Thauer RK, Shima S (2003) A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426:878–881

    Article  PubMed  Google Scholar 

  • Lein AY, Ivanov MV, Pimenov NV, Gulin MB (2002) Geochemical characteristics of the carbonate constructions formed during microbial oxidation of methane under anaerobic conditions. Microbiology 70:78–90

    Article  Google Scholar 

  • Luth C, Luth U, Gebruk AV, Thiel H (1999) Methane gas seeps along the oxic/anoxic gradient in the Black Sea: manifestations, biogenic sediment compounds, and preliminary results on benthic ecology. Mar Ecol Prog Ser 20:221–249

    Article  CAS  Google Scholar 

  • Manz W, Eisenbrecher M, Neu TR, Szewzyk U (1998) Abundance 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

    Article  CAS  Google Scholar 

  • Manz W, Arp G, Schumann-Kindel G, Szewzyk U, Reitner J (2000) Widefield deconvolution epifluorescence microscopy combined with fluorescence in situ hybridization reveals the spatial arrangement of bacteria in sponge tissue. J Microbiol Methods 40:125–134

    Article  CAS  PubMed  Google Scholar 

  • Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, Knittel K, Gieseke A, Peterknecht K, Pape T, Boetius A, Amann R, Jørgensen BB, Widdel F, Peckmann J, Pimenov NV, Gulin MB (2002) Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297:1013–1015

    Article  CAS  PubMed  Google Scholar 

  • Nauhaus K, Treude T, Boetius A, Krüger M (2005) Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ Microbiol 7:98–106

    Article  CAS  PubMed  Google Scholar 

  • Orphan V, Hinrichs K-U, Ussler W III, Paull CK, Taylor LT, Sylva SP, Hayes JM, DeLong EF (2001) Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl Environ Microbiol 67:1922–1934

    Article  CAS  PubMed  Google Scholar 

  • Orphan V, House CH, Hinrichs K-U, McKeegan KD, DeLong EF (2002) Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci USA 99:7663–7668

    Article  CAS  PubMed  Google Scholar 

  • Pagel M, Barbin V, Blanc P, Ohnenstetter D (2000) Cathodoluminescence in Geosciences. Springer, Heidelberg

    Google Scholar 

  • Peckmann J, Thiel V (2004) Carbon cycling at ancient methane-seeps. Chem Geol 205:443–467

    Article  CAS  Google Scholar 

  • Peckmann J, Thiel V, Michaelis W, Clari P, Gaillard C, Martire L, Reitner J (1999) Cold seep deposits of Beauvoisin (Oxfordian; southeastern France) and Marmorito (Miocene; northern Italy): microbially induced, authigenic carbonates. Int J Earth Sci 88:60–75

    Article  CAS  Google Scholar 

  • Peckmann J, Reimer A, Luth U, Luth C, Hansen BT, Heinicke C, Hoefs J, Reitner J (2001) Methane-derived carbonates and authigenic pyrite from the northwestern Black Sea. Mar Geol 177:129–150

    Article  CAS  Google Scholar 

  • Pimenov NV, Rusanov II, Poglazova MN, Mityushina LL, Sorokin DY, Khmelenina VN, Trotsenko YA (1997) Bacterial mats on coral-like structures at methane seeps in the Black Sea. Microbiology (translated from Mikrobiologiya) 66:354–360

    CAS  Google Scholar 

  • Podda F, Zuddas P, Minacci A, Pepi M, Baldi F (2000) Heavy metal coprecipitation with hydrozincite [Zn5(CO3)2(OH)6] from mine waters caused by photosynthetic microorganisms. Appl Environ Microbiol 66:5092–5098

    Article  CAS  PubMed  Google Scholar 

  • Polikarpov GG, Egorov VN, Nezhdanov AI, Gulin SB, Kulev YD, Gulin MB (1989) The phenomenon of active gas escapes from mounds on the slope of the western Black Sea. Dokl Akad Nauk USSR pp 13–16

  • Pósfai M, Buseck PR, Bazylinsky DA, Frankel RB (1998) Iron sulfides from magnetotactic bacteria: structure, composition, and phase transitions. Am Mineral 83:1469–1481

    Google Scholar 

  • Reitner J, Peckmann J, Blumenberg M, Michaelis W, Reimer A, Thiel V (2005) Concretionary methane-seep carbonates and associated microbial communities in Black Sea sediments. Palaeogeogr Palaeoclimatol Palaeoecol (in press)

  • Riding R (2000) Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47:179–214

    Article  CAS  Google Scholar 

  • Romeis B (1989) Mikroskopische Technik. Urban and Schwarzenberg, München

    Google Scholar 

  • Schlegel HG (1985) Allgemeine Mikrobiologie. Georg Thieme, Stuttgart, New York

    Google Scholar 

  • Schüler D (1999) Formation of magnetosomes in magnetotactic bacteria. J Mol Microbiol Biotechnol 1:79–86

    PubMed  Google Scholar 

  • Shapiro R, Fricke H (2002) Tepee Buttes: fossilized methane-seep ecosystems. GSA Field Guide 3:94–101

    Google Scholar 

  • Thiel V, Peckmann J, Richnow HH, Luth U, Reitner J, Michaelis W (2001) Molecular signals for anaerobic methane oxidation in Black Sea seep carbonates and a microbial mat. Mar Chem 73:97–112

    Article  CAS  Google Scholar 

  • Tourova TP, Kolganova TP, Kusnetsov KB, Pimenov N (2002) Phylogenetic diversity of the archaeal component of bacterial mats on coral-like structures in zones of methane seeps in the Black Sea. Microbiology (translated from Mikrobiologiya) 71:196–201

    CAS  Google Scholar 

  • Valentine DL (2002) Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Antonie van Leeuwenhook 81:271–282

    Article  CAS  Google Scholar 

  • Walter LN (1986) Relative efficiency of carbonate dissolution and precipitation during diagenesis: a progress report on the role of solution chemistry. SEPM Spec Publ 38:1–11

    Google Scholar 

Download references

Acknowledgements

This paper is dedicated to the memory of Erik Flügel. Always being open to new ideas, he promoted our work and stimulated our scientific development with great emphasis. He was more than a colleague. We thank the crew of the R/V ‘Professor Logachev’ for excellent collaboration during the cruise and Martin Ischebek for the on-board fixation of biological samples. We are grateful to Joachim Hoefs, Bent T. Hansen, Andreas Kronz (all GZG, Göttingen) and Michael Joachimski (Erlangen) for analytical assistance. This study received financial support through program GHOSTDABS (03G0559A) of the Bundesministerium für Bildung und Forschung and the Deutsche Forschungsgemeinschaft (GEOTECHNOLOGIEN). This is publication No. 11 of the research program GHOSTDABS, and publication No. RCOM0298 of the DFG-Research Center for Ocean Margins

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joachim Reitner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reitner, J., Peckmann, J., Reimer, A. et al. Methane-derived carbonate build-ups and associated microbial communities at cold seeps on the lower Crimean shelf (Black Sea). Facies 51, 66–79 (2005). https://doi.org/10.1007/s10347-005-0059-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10347-005-0059-4

Keywords

Navigation