References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-6-2383-2009

Biogeochemistry of a low-activity cold seep in the Larsen B area, western Weddell Sea, Antarctica

Niemann

¹ ² Fischer

³ Graffe

⁴ Knittel

¹ Montiel

⁵ Heilmayer

⁴ ⁶ Nöthen

⁴ Pape

³ Kasten

⁴ Bohrmann

³ Boetius

¹ ⁴ Gutt

⁴

Max Planck Institute for Marine Microbiology, Bremen, Germany

Institute for Environmental Geosciences, University of Basel, Basel, Switzerland

MARUM – Center for Marine Environmental Sciences and Department of Geosciences, Univ. of Bremen, Bremen, Germany

Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany

Universidad de Magallanes, Punta Arenas, Chile

German Aerospace Centre, Bonn, Germany

02 11 2009

6 11 2383 2395

2009

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

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The full text article is available as a PDF file from https://bg.copernicus.org/articles/6/2383/2009/bg-6-2383-2009.pdf

First videographic indication of an Antarctic cold seep ecosystem was recently obtained from the collapsed Larsen B ice shelf, western Weddell Sea (Domack et al., 2005). Within the framework of the R/V Polarstern expedition ANTXXIII-8, we revisited this area for geochemical, microbiological and further videographical examinations. During two dives with ROV Cherokee (MARUM, Bremen), several bivalve shell agglomerations of the seep-associated, chemosynthetic clam Calyptogena sp. were found in the trough of the Crane and Evans glacier. The absence of living clam specimens indicates that the flux of sulphide and hence the seepage activity is diminished at present. This impression was further substantiated by our geochemical observations. Concentrations of thermogenic methane were moderately elevated with 2 μM in surface sediments of a clam patch, increasing up to 9 μM at a sediment depth of about 1 m in the bottom sections of the sediment cores. This correlated with a moderate decrease in sulphate from about 28 mM at the surface down to 23.4 mM, an increase in sulphide to up to 1.43 mM and elevated rates of the anaerobic oxidation of methane (AOM) of up to 600 pmol cm−3 d−1 at about 1 m below the seafloor. Molecular analyses indicate that methanotrophic archaea related to ANME-3 are the most likely candidates mediating AOM in sediments of the Larsen B seep.

References 1

Anderson, J. B.: Antarctic Marine Geology, Cambridge University Press, Cambridge, 297 pp., 1999.

Beal, E. J., House, C. H., and Orphan, V. J.: Manganese- and Iron-Dependent Marine Methane Oxidation, Science, 325, 184–187, https://doi.org/10.1126/science.1169984, 2009.

Bernard, B. B., Brooks, J. M., and Sackett, W. M.: Natural gas seepage in the Gulf of Mexico, Earth Planet. Sci. Lett., 31, 48–54, 1976.

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

Boudreau, B. P.: Diagenetic models and their implementation: modelling transport and reactions in aquatic sediments, Springer, Berlin, 414 pp., 1997.

Childress, J. J. and Fisher, C. R.: The Biology of Hydrothermal Vent Animals – Physiology, Biochemistry, and Autotrophic Symbioses, Oceanogr. Mar. Biol., 30, 337–441, 1992.

de Beer, D., Sauter, E., Niemann, H., Kaul, N., Foucher, J. P., Witte, U., Schlüter, M., and Boetius, A.: In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby Mud Volcano, Limnol. Oceanogr., 51, 1315–1331, 2006.

Domack, E., Ishman, S., Leventer, A., Sylva, S., Willmott, V., and Huber, B.: Chemotrophic Ecosystem Beneath the Larsen Ice Shelf, EOS Transactions of the American Geophysical Union, 86, 269–276, 2005.

Ettwig, K. F., Shima, S., van de Pas-Schoonen, K. T., Kahnt, J., Medema, M. H., op den Camp, H. J. M., Jetten, M. S. M., and Strous, M.: Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea, Environ. Microbiol., 10, 3164–3173, https://doi.org/10.1111/j.1462-2920.2008.01724.x, 2008.

Fisher, C. R.: Chemoautotrophic and Methanotrophic Symbioses in Marine-Invertebrates, Rev. Aquat. Sci., 2, 399–436, 1990.

Fogo, J. K. and Popowsky, M.: Spectrophotometric Determination of Hydrogen Sulfide – Methylene Blue Method, Anal. Chem., 21, 732–734, 1949.

Fossing, H. and Jørgensen, B. B.: Measurement of Bacterial Sulfate Reduction in Sediments – Evaluation of a Single-Step Chromium Reduction Method, Biogeochemistry, 8, 205–222, 1989.

Foustoukos, D. I. and Seyfried Jr., W. E.: Hydrocarbons in Hydrothermal Vent Fluids: The Role of Chromium-Bearing Catalysts, Science, 304, 1002–1005, 2004.

Garcia, J.-L., Olliver, B., and Whitman, W. B.: The Order Methanomicrobiales, in: The Prokaryotes, edited by: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. H., and Stackebrandt, E., Springer, 208–230, 2006.

Gerdes, D., Klages, M., Arntz, W. E., Herman, R. L., Galeron, J., and Hain, S.: Quantitative investigations on macrobenthos communities of the southeastern Weddell Sea shelf based on multibox corer samples, Polar Biol., 12, 291–301, 1992.

Girguis, P. R., Cozen, A. E., and DeLong, E. F.: Growth and population dynamics of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria in a continuous-flow bioreactor, Appl. Environ. Microb., 71, 3725–3733, 2005.

Goffredi, S. K. and Barry, J. P.: Species-specific variation in sulfide physiology between closely related Vesicomyid clams, Mar. Ecol.-Prog. Ser., 225, 227–238, 2002.

Grasshoff, K., Ehrhardt, M., and Kremling, K.: Methods of seawater analysis, 2 ed., Wiley-VCH, Weinheim, 447 pp., 1983.

Grehan, A. J. and Juniper, S. K.: Clam distribution and subsurface hydrothermal processes at Chowder Hill (Middle Valley), Juan de Fuca Ridge, Mar. Ecol.-Prog. Ser., 130, 105–115, 1996.

Gutt, J.: The Expedition ANTARKTIS-XXIII/8 of the Research Vessel "Polarstern" in 2006/2007, Reports on Polar and Marine Research, edited by: Riemann, F., Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, 152 pp., 2008.

Harley, J., Nel, W., and Pretorius, V.: Flame Ionization Detector for Gas Chromatography, Nature, 181, 177–178, 1958.

Hathway, B.: Continental rift to back-arc basin: Jurassic-Cretaceous stratigraphical and structural evolution of the Larsen Basins, Antarctic Peninsula, J. Geol. Soc. London, 157, 417–432, 2000.

Hensen, C., Nuzzo, M., Hornibrook, E., Pinheiro, L. M., Bock, B., Magalhaes, V. H., and Bruckmann, W.: Sources of mud volcano fluids in the Gulf of Cadiz – indications for hydrothermal imprint, Geochim. Cosmochim. Ac., 71, 1232–1248, 2007.

Hinrichs, K.-U., Hayes, J. M., Sylva, S. P., Brewer, P. G., and DeLong, E. F.: Methane-consuming archaebacteria in marine sediments, Nature, 398, 802–805, 1999.

Hinrichs, K.-U. and Boetius, A.: The anaerobic oxidation of methane: New insights in microbial ecology and biogeochemistry, in: Ocean Margin Systems, edited by: Wefer, G., Billett, D., and Hebbeln, D., Springer Verlag, Berlin-Heidelberg, 457–477, 2002.

Inagaki, F., Tsunogai, U., Suzuki, M., Kosaka, A., Machiyama, H., Takai, K., Nunoura, T., Nealson, K. H., and Horikoshi, K.: Characterization of C1-metabolizing prokaryotic communities in methane seep habitats at the Kuroshima Knoll, southern Ryukyu arc, by analyzing pmoA, mmoX, mxaF, mcrA, and 16S rRNA genes, Appl. Environ. Microb., 70, 7445–7455, 2004.

James, A. T. and Martin, A. J. P.: Gas-liquid partition chromatography: the separation and micro-estimation of volatile fatty acids from formic acid to dodecanoic acid, Biochem. J., 50, 679–690, 1952.

James, A. T. and Burns, B. J.: Microbial alteration of subsurface natural gas accumulations, AAPG Bull., 68, 957–960, 1984.

Janssen, P. H., Schuhmann, A., Bak, F., and Liesack, W.: Disproportionation of inorganic sulfur compounds by the sulfate-reducing bacterium Desulfocapsa thiozymogenes gen nov, sp nov, Arch. Microbiol., 166, 184–192, 1996.

Jørgensen, B. B.: A comparison of methods for the quantification of bacterial sulphate reduction in coastal marine sediments. I. Measurements with radiotracer techniques, Geomicrob. J., 1, 11–27, 1978.

Jørgensen, B. B. and Boetius, A.: Feast and famine – microbial life in the deep-sea bed, Nat. Rev. Microbiol., 5, 770–781, 2007.

Joye, S. B., Boetius, A., Orcutt, B. N., Montoya, J. P., Schulz, H. N., Erickson, M. J., and Lugo, S. K.: The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps, Chem. Geol., 205, 219–238, 2004.

Juniper, S. K., Tunnicliffe, V., and Southward, E. C.: Hydrothermal Vents in Turbidite Sediments on a Northeast Pacific Spreading Center – Organisms and Substratum at an Ocean Drilling Site, Can. J. Zool., 70, 1792–1809, 1992.

Kniemeyer, O., Musat, F., Sievert, S. M., Knittel, K., Wilkes, H., Blumenberg, M., Michaelis, W., Classen, A., Bolm, C., Joye, S. B., and Widdel, F.: Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria, Nature, 449, 898–901, 2007.

Knittel, K., Boetius, A., Lemke, A., Eilers, H., Lochte, K., Pfannkuche, O., Linke, P., and Amann, R.: Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia margin, Oregon), Geomicrob. J., 20, 269–294, 2003.

Knittel, K., Lösekann, T., Boetius, A., Kort, R., and Amann, R.: Diversity and distribution of methanotrophic archaea at cold seeps, Appl. Environ. Microb., 71, 467–479, 2005.

Knittel, K. and Boetius, A.: Anaerobic Oxidation of Methane: Progress with an Unknown Process, Annu. Rev. Microbiol., 63, 311–334, https://doi.org/10.1146/annurev.micro.61.080706.093130, 2009.

Kolb, B. and Ettre, L. S.: Static Headspace-Gas Chromatography: Theory and Practice, Wiley-Interscience, New Jersey, 376 pp., 2005.

Larter, S. and di Primio, R.: Effects of biodegradation on oil and gas field PVT properties and the origin of oil rimmed gas accumulations, Org. Geochem., 36, 299–310, https://doi.org/10.1016/j.orggeochem.2004.07.015, 2005.

Lösekann, T., Knittel, K., Nadalig, T., Fuchs, B., Niemann, H., Boetius, A., and Amann, R.: Diversity and Abundance of Aerobic and Anaerobic Methane Oxidizers at the Haakon Mosby Mud Volcano, Barents Sea, Appl. Environ. Microb., 73, 3348–3362, 2007.

Lollar, B. S., Frape, S. K., Weise, S. M., Fritz, P., Macko, S. A., and Welhan, J. A.: Abiogenic Methanogenesis in Crystalline Rocks, Geochim. Cosmochim. Ac., 57, 5087–5097, 1993.

Niemann, H., Elvert, M., Hovland, M., Orcutt, B., Judd, A., Suck, I., Gutt, J., Joye, S., Damm, E., Finster, K., and Boetius, A.: Methane emission and consumption at a North Sea gas seep (Tommeliten area), Biogeosciences, 2, 335–351, 2005.

Niemann, H., Duarte, J., Hensen, C., Omoregie, E., Magalhaes, V. H., Elvert, M., Pinheiro, L. M., Kopf, A., and Boetius, A.: Microbial methane turnover at mud volcanoes of the Gulf of Cadiz, Geochim. Cosmochim. Ac., 70, 5336–5355, 2006a.

Niemann, H., Lösekann, T., de Beer, D., Elvert, M., Nadalig, T., Knittel, K., Amann, R., Sauter, E. J., Schlüter, M., Klages, M., Foucher, J. P., and Boetius, A.: Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink, Nature, 443, 854–858, 2006b.

Olu-Le Roy, K., Caprais, J. C., Fifis, A., Fabri, M. C., Galeron, J., Budzinsky, H., Le Menach, K., Khripounoff, A., Ondreas, H., and Sibuet, M.: Cold-seep assemblages on a giant pockmark off West Africa: spatial patterns and environmental control, Mar. Ecol. Evol. Persp., 28, 115–130, https://doi.org/10.1111/j.1439-0485.2006.00145.x, 2007.

Omoregie, E. O., Mastalerz, V., de Lange, G., Straub, K. L., Kappler, A., Roy, H., Stadnitskaia, A., Foucher, J. P., and Boetius, A.: Biogeochemistry and community composition of iron- and sulfur-precipitating microbial mats at the Chefren mud volcano (Nile Deep Sea fan, Eastern Mediterranean), Appl. Environ. Microb., 74, 3198–3215, 2008.

Omoregie, E. O., Niemann, H., Mastalerz, V., de Lange, G., Stadnitskaia, A., Mascle, J., Foucher, J. P., and Boetius, A.: Microbial methane oxidation and sulfate reduction at cold seeps of the deep Eastern Mediterranean Sea, Mar. Geol., 261, 114–127, 2009.

Orphan, V. J., Hinrichs, K. U., Ussler, W., Paull, C. K., Taylor, L. T., Sylva, S. P., Hayes, J. M., and Delong, E. F.: Comparative analysis of methane-oxidizing archaea and sulfate- reducing bacteria in anoxic marine sediments, Appl. Environ. Microb., 67, 1922–1934, 2001.

Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D., and DeLong, E. F.: Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments, P. Nat. Acad. Sci. USA., 99, 7663–7668, 2002.

Pernthaler, A., Dekas, A. E., Brown, C. T., Goffredi, S. K., Embaye, T., and Orphan, V. J.: Diverse syntrophic partnerships from-deep-sea methane vents revealed by direct cell capture and metagenomics, P. Nat. Acad. Sci. USA., 105, 7052–7057, https://doi.org/10.1073/pnas.0711303105, 2008.

Rabus, R., Hansen, T. A., and Widdel, F.: Dissimilatory Sulfate- and Sulfur-Reducing Prokaryotes, in: The Prokayotes, edited by: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E., Springer, Berlin, 659–768, 2006.

Rack, W. and Rott, H.: Pattern of retreat and disintegration of the Larsen B ice shelf, Antarctic Peninsula, Ann. Glaciol., 39, 505–510, 2004.

Raghoebarsing, A. A., Pol, A., van de Pas-Schoonen, K. T., Smolders, A. J. P., Ettwig, K. F., Rijpstra, W. I. C., Schouten, S., Damste, J. S. S., Op den Camp, H. J. M., Jetten, M. S. M., and Strous, M.: A microbial consortium couples anaerobic methane oxidation to denitrification, Nature, 440, 918–921, 2006.

Reeburgh, W. S.: Oceanic methane biogeochemistry, Chem. Rev., 107, 486–513, 2007.

Rott, H., Skvarca, P., and Nagler, T.: Rapid collapse of northern Larsen Ice Shelf, Antarctica, Science, 271, 788–792, 1996.

Roussel, E. G., Sauvadet, A. L., Allard, J., Chaduteau, C., Richard, P., Bonavita, M. A. C., and Chaumillon, E.: Archaeal Methane Cycling Communities Associated with Gassy Subsurface Sediments of Marennes-Oleron Bay (France), Geomicrob. J., 26, 31–43, https://doi.org/10.1080/01490450802599284, 2009.

Rutgers Van der Loeff, M. M., Meadows, P. S., and Allen, J. A.: Oxygen in Pore Waters of Deep-Sea Sediments, Philos. T. Roy. Soc. A, 331, 69–84, 1990.

Sahling, H., Rickert, D., Lee, R. W., Linke, P., and Suess, E.: Macrofaunal community structure and sulfide flux at gas hydrate deposits from the Cascadia convergent margin, NE Pacific, Mar. Ecol.-Prog. Ser., 231, 121–138, 2002.

Sahling, H., Wallmann, K., Dählmann, A., Schmaljohann, R., and Petersen, S.: The physicochemical habitat of Sclerolinum sp at Hook Ridge hydrothernial vent, Bransfield Strait, Antarctica, Limnol. Oceanogr., 50, 598–606, 2005.

Sahling, H., Bohrmann, G., Spiess, V., Bialas, J., Breitzke, M., Ivanov, M., Kasten, S., Krastel, S., and Schneider, R. R.: Pockmarks in the northern Congo Fan area, SW Africa: Complex seafloor features shaped by fluid flow. Mar. Geol., 249, 206–225, 2008.

Sauter, E. J., Muyakshin, S. I., Charlou, J. L., Schlüter, M., Boetius, A., Jerosch, K., Damm, E., Foucher, J. P., and Klages, M.: Methane discharge from a deep-sea submarine mud volcano into the upper water column by gas hydrate-coated methane bubbles, Earth Planet. Sci. Lett., 243, 354–365, 2006.

Schrenk, M. O., Kelley, D. S., Delaney, J. R., and Baross, J. A.: Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney, Appl. Environ. Microb., 69, 3580–3592, 2003.

Schulz, H. and Zabel, M.: Marine Geochemistry, 2 ed., Springer, 574 pp., 2006.

Seeberg-Elverfeldt, J., Schlüter, M., Feseker, T., and Kölling, M.: Rhizon sampling of porewaters near the sediment-water interface of aquatic systems, Limnol. Oceanogr.-Meth., 3, 361–371, 2005.

Shepherd, A., Wingham, D., Payne, T., and Skvarca, P.: Larsen ice shelf has progressively thinned, Science, 302, 856–859, 2003.

Small, H., Stevens, T. S., and Bauman, W. C.: Novel Ion-Exchange Chromatographic Method Using Conductimetric Detection, Anal. Chem., 47, 1801–1809, 1975.

Stadnitskaia, A., Ivanov, M. K., Blinova, V., Kreulen, R., and van Weering, T. C. E.: Molecular and carbon isotopic variability of hydrocarbon gases from mud volcanoes in the Gulf of Cadiz, NE Atlantic, Mar. Petrol. Geol., 23, 281–296, 2006.

Teske, A., Hinrichs, K. U., Edgcomb, V., Gomez, A. D., Kysela, D., Sylva, S. P., Sogin, M. L., and Jannasch, H. W.: Microbial diversity of hydrothermal sediments in the Guaymas Basin: Evidence for anaerobic methanotrophic communities, Appl. Environ. Microb., 68, 1994–2007, 2002.

Torres, M. E., McManus, J., Hammond, D. E., de Angelis, M. A., Heeschen, K. U., Colbert, S. L., Tryon, M. D., Brown, K. M., and Suess, E.: Fluid and chemical fluxes in and out of sediments hosting methane hydrate deposits on Hydrate Ridge, OR, I: Hydrological provinces, Earth Planet. Sci. Lett., 201, 525–540, 2002.

Treude, T., Boetius, A., Knittel, K., Wallmann, K., and Jørgensen, B. B.: Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific Ocean, Mar. Ecol.-Prog. Ser., 264, 1–14, 2003.

von Damm, K. L., Oosting, S. E., Kozlowski, R., Buttermore, L. G., Colodner, D. C., Edmonds, H. N., Edmond, J. M., and Grebmeier, J. M.: Evolution of East Pacific Rise hydrothermal vent fluids following a volcanic eruption, Nature, 375, 47–50, 1995.

Webster, G., Yarram, L., Freese, E., Köster, J., Sass, H., Parkes, R. J., and Weightman, A. J.: Distribution of candidate division JS1 and other Bacteria in tidal sediments of the German Wadden Sea using targeted 16S rRNA gene PCR-DGGE, FEMS Microbiol. Ecol., 62, 78–89, 2007.

Wegener, G., Shovitri, M., Knittel, K., Niemann, H., Hovland, M., and Boetius, A.: Biogeochemical processes and microbial diversity of the Gullfaks and Tommeliten methane seeps (Northern North Sea), Biogeosciences, 5, 1127–1144, 2008.

Whiticar, M. J.: Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane, Chem. Geol., 161, 291–314, 1999.

Widdel, F.: Anaerobic hydrocarbon-degrading microorganisms – an overview., in: Handbook of Hydrocarbon and Lipid Microbiology, edited by: Timmis, K. N., Springer Verlag, Berlin, in press, 2009.

Wirsen, C. O., Sievert, S. M., Cavanaugh, C. M., Molyneaux, S. J., Ahmad, A., Taylor, L. T., DeLong, E. F., and Taylor, C. D.: Characterization of an Autotrophic Sulfide-Oxidizing Marine Arcobacter sp. That Produces Filamentous Sulfur, Appl. Environ. Microb., 68, 316–325, https://doi.org/10.1128/aem.68.1.316-325.2002, 2002.

Zhou, J. Z., Bruns, M. A., and Tiedje, J. M.: DNA recovery from soils of diverse composition, Appl. Environ. Microb., 62, 316–322, 1996.