Elsevier

Organic Geochemistry

Volume 41, Issue 4, April 2010, Pages 414-426
Organic Geochemistry

Biomarker indicators for anaerobic oxidizers of methane in brackish-marine sediments with diffusive methane fluxes

https://doi.org/10.1016/j.orggeochem.2009.09.009Get rights and content

Abstract

The anaerobic oxidation of methane (AOM) is a major methane sink in marine sediments and plays a crucial role in mitigating methane fluxes to the overlying water column. We investigated biomarker distributions and compound specific isotopic signatures in sediments from sites on the Northern European continental margin that are characterized by a diffusive flux of methane. At all sites, the organic matter (OM) is predominantly derived from terrestrial higher plants, with subordinate abundances of algal biomarkers, but biomarkers for archaea and bacteria are also present. The co-occurrence of the archaeal lipids archaeol, sn-2-hydroxyarchaeol and 2,6,10,15,19-pentamethylicosane (PMI) with non-isoprenoidal glycerol diethers inferred to derive from sulfate-reducing bacteria (SRB) is similar to microbial biomarker assemblages observed at cold seeps. The archaeal and inferred SRB biomarker concentrations typically reach maxima close to the sulfate-methane transition zone (SMTZ), where archaeal biomarkers are depleted in 13C. The 16S rRNA gene sequences from the SMTZ of the Aarhus Bay sediment core indicate the occurrence of ANME-1 archaea, consistent with inferences derived from biomarker distributions. The observations suggest that AOM in these diffusive settings is mediated by consortia of archaea and bacteria similar to those found at many seep and methane hydrate sites around the world.

Introduction

Continental shelf settings are highly productive areas (Berger et al., 1989) and represent ca. 80% of the total carbon accumulation in the ocean (Wollast, 1991, Ver et al., 1999). Degradation of OM that becomes buried in continental shelf sediments ultimately leads to the formation of methane. Despite extensive production in marine sediments, most of the upward moving methane never reaches the overlying water column because a large proportion is oxidized in the subsurface, primarily in the anoxic region of the sediment so that, on a global scale, the oceans are only minor contributors of methane to the atmosphere (Reeburgh, 2007).

The anaerobic oxidation of methane (AOM) and the microorganisms mediating this transformation have been studied extensively, particularly in sediments from cold seeps and methane hydrate settings (Knittel and Boetius, 2009). Biogeochemical studies demonstrate that AOM is mediated by distinct groups of archaea called ANME that are phylogenetically related to methanogens (Hinrichs et al., 1999, Orphan et al., 2002, Knittel et al., 2005). They frequently occur in association with sulfate-reducing bacteria (SRB; Boetius et al., 2000, Orphan et al., 2001, Orphan et al., 2002, Michaelis et al., 2002, Knittel et al., 2005, Niemann et al., 2006) but can also occur as mono-specific aggregates and single cells (Orphan et al., 2002, Knittel et al., 2005, Treude et al., 2005).

One approach widely adopted in investigations of the microbial ecology of cold seeps is the determination of the distribution and carbon isotopic composition of lipid biomarkers diagnostic for certain groups of microorganisms. Unlike Eukarya and Bacteria, Archaea contain ether-bound membrane lipids with isoprenoid carbon skeletons rather than ester linked alkyl lipids (De Rosa and Gambacorta, 1988). Isoprenoid ether lipids or their degradation products have been reported in diverse environments (Hoefs et al., 1997, DeLong et al., 1998, Schouten et al., 1998) and have been useful in studying archaeal communities in cold seeps (Hinrichs et al., 1999, Pancost et al., 2000, Pancost et al., 2001a, Niemann et al., 2005). In zones of AOM, ether lipids are frequently accompanied (Elvert et al., 2000, Bian et al., 2001) by the irregular isoprenoid hydrocarbons PMI (2,6,10,15,19-pentamethylicosane) and crocetane (2,6,11,15-tetramethylhexadecane). Archaeal lipid biomarkers in the AOM zone often co-occur with bacterially-derived compounds such as branched fatty acids characteristic of SRB (Boetius et al., 2000, Pancost et al., 2000, Hinrichs and Boetius, 2002) and non-isoprenoidal ether lipids (Pancost et al., 2001b, Hinrichs and Boetius, 2002). In these settings, the uptake of 13C-depleted methane by microbial consortia is expressed as highly 13C-depleted archaeal and bacterial biomarkers.

Biomarker concentrations and isotopic signatures at cold seeps are correlated with AOM and sulfate reduction (SR) rates. Maximum biomarker concentrations and minimum δ13C values generally occur at sites with the highest AOM and SR rates and the highest consortium biomass (Elvert et al., 2005). In AOM settings characterized by a diffusive source of methane, the lipid biomarker approach has been adopted in only a few cases (Bian et al., 2001, Biddle et al., 2006, Parkes et al., 2007), partly because a high input of allochthonous OM tends to obscure the occurrence of biomarkers derived from organisms involved in AOM. The EU-funded METROL (Methane Flux Control in Ocean Margin Sediments) program has been investigating methane fluxes in sediments from European ocean margin settings, including Aarhus Bay, the Kattegat, the Skagerrak and Western Baltic Sea sediments. In this study, detailed lipid biomarker and pore water analyses, as well as DNA analysis and rate measurements of AOM and SR, were carried out on a sediment core from Aarhus Bay. These were then compared with biomarker distributions and pore water geochemistry at various sites within the Skagerrak, the Kattegat and the Western Baltic Sea.

Section snippets

Sites and sampling

Sediments from the eastern part of the North Sea (Skagerrak), the transition connection between the North Sea and the Baltic Sea (the Kattegat and Aarhus Bay), the western Baltic Sea, and methane-derived authigenic carbonates from a methane seep within the Kattegat (Fig. 1, Table 1) were retrieved as part of the METROL project. Two parallel gravity cores were collected from each site; one was used to analyze geochemical parameters and biogeochemical reaction rates, while the second was used for

Sediment pore water geochemistry

Fig. 2a shows sulfate and methane pore water profiles and Fig. 2b the rates of sulfate reduction and AOM in Aarhus Bay sediment (core 173 GC). It should be noted that about 10 cm of the top sediment was lost using gravity coring and that the vertical scale shows depth in the GC core rather than depth below the sediment surface. Methane concentration <0.1 μmol cm−3 was measured throughout the top 175 cm. Pore water sulfate concentration decreased with depth over this section from 20 mM to <1 mM. Below

Discussion

Archaeal and bacterial biomarkers in the European Margin sediments investigated here are also ubiquitous in AOM settings such as cold seeps and sediments associated with methane hydrates. In fact, such a distribution of archaeal and SRB lipids is now an integral component of the characterization of modern and ancient cold seeps. However, biomarker concentrations are highly variable, both among the cores investigated here and relative to settings characterized by an advective methane supply.

Conclusions

The distributions of archaeal and bacterial biomarkers in our sediments are similar to those found in cold seep and methane hydrate settings, suggesting that similar organisms mediate AOM in these diverse settings; for the Aarhus Bay setting, this is supported by the occurrence of highly 13C-depleted archaeal lipid biomarkers and ANME-1 gene sequences at the SMTZ. However, distributions and carbon isotopic compositions suggest that AOM-mediating organisms are not the sole sources of the

Acknowledgements

We thank the anonymous reviewers for constructive comments which helped improve the manuscript. The work was carried out as part of the METROL project of the 5th Framework Program and funded by the European Commission. A. A. was supported by a Marie Curie Fellowship for Early Stage Research Training (EST) through the BIOTRACS program, funded by the EU under the FP6 protocol. We thank all of the scientific members of METROL, particularly B.B. Jørgensen and C. Borowski. We acknowledge B. Cragg

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