CH4-consuming microorganisms and the formation of carbonate crusts at cold seeps

doi:10.1016/S0012-821X(02)00878-6

Earth and Planetary Science Letters

Volume 203, Issue 1, 15 October 2002, Pages 195-203

https://doi.org/10.1016/S0012-821X(02)00878-6 Get rights and content

Abstract

To understand the role played by microorganisms in the formation of cold seep carbonates, we conducted an integrated microbial, mineralogical and organic geochemical study of methane-related authigenic carbonate crusts formed on eastern Mediterranean mud volcanoes. We show that supersaturation with respect to carbonate minerals is induced by microbial anaerobic oxidation of methane. Combined lipid biomarker analysis and 16S rRNA gene surveys identified a highly diversified methane-consuming archaeal community possibly comprising novel species, implying that the anaerobic oxidation of methane is phylogenetically widespread and directly implicating these organisms in the process of crust precipitation. Moreover, pore-water sulphate gradients produced by co-occurring methane-based sulphate reduction exert the main control on aragonite versus magnesian calcite precipitation. We propose that this may be the dominant mode of carbonate crust formation at cold seeps world-wide, in agreement with aquatic chemistry predictions and explaining carbonate mineralogy.

Introduction

Authigenic carbonate crusts formed at seafloor cold seeps are a sink for methane carbon migrating from depth or released from shallow gas hydrates [1], [2], and thus partly regulate ocean–atmosphere carbon fluxes. Although the association of methane seepage and oxidation with carbonate crust formation is easily established on the basis of carbonate ¹³C depletion, a number of questions regarding carbonate crust formation remain unanswered: the methane-oxidising microorganisms have not been identified and the relative importance of aerobic and anaerobic processes has to be elucidated. Furthermore, a better understanding of how microbial processes affect dissolved inorganic carbon and carbonate–mineral equilibria is needed and controls on authigenic carbonate mineralogy have to be understood.

Growing evidence is being provided by molecular biogeochemical [3], [4], [5] and phylogenetic [6], [7] investigations that anaerobic oxidation of methane, which accounts for most of the methane consumption in marine sediments, is carried out by prokaryotic consortia composed of methanotrophic archaea and sulphate-reducing bacteria. Thiel et al. [8] and Peckmann et al. [9] report on cold seep carbonates that contain such molecular indicators, suggesting that the anaerobic oxidation of methane may play an important role in cold seep carbonate formation. However, the microbial community structure of carbonate crusts has not been described so far and the phylogenetic diversity and spatial variability of the microorganisms involved in their formation are largely unknown. To investigate these aspects, we combined mineralogical and stable isotope studies of authigenic carbonates recovered from eastern Mediterranean mud volcanoes with lipid biomarker analysis, compound-specific carbon isotope measurements and 16S rRNA gene surveys.

Section snippets

Submersible dives and samples

Eastern Mediterranean mud volcanoes form when tectonically over-pressured and methane-charged mud is extruded at the seafloor and re-deposited as mud breccia [10]. Seven such structures at depths between 1600 and 2000 m were explored with the Nautile submersible during the Medinaut cruise of the R/V Nadir in 1998. Their central parts actively release methane to the bottom waters and are covered by carbonate crust pavements up to several decimetres thick [10] (Fig. 1a). These form by

Mineralogy and stable isotope composition of carbonates

The mineralogy of the carbonate crusts was determined by X-ray diffraction of dried and ground subsamples of carbonate crusts. Authigenic (high-Mg) calcite was distinguished from pelagic (low-Mg calcite) on the basis of d values of the (104) diffraction peak which are equal to approximately 2.998 Å and 3.028 Å, respectively [11]. The oxygen and carbon stable isotope compositions of aragonite and high-Mg calcite were measured using a specific procedure to account for the presence of authigenic

Mineralogy and stable isotope composition

Aragonite and high-Mg calcite cements account for up to 82% of the crusts in weight. The carbonate cements are depleted in ¹³C (δ¹³C values of MN16BT2 and MN13BT4 are −28.9‰ and −24.8‰, respectively) indicating that methane is a major source for the carbonate carbon. They are also up to 2.2‰ enriched in ¹⁸O (δ¹⁸O values of MN16BT2 and MN13BT4 are 5.1‰ and 3.5‰, respectively) compared to expected values for aragonite and high-Mg calcite precipitating from modern eastern Mediterranean bottom

Microbial community structure

Scanning electron microscope observations revealed organic matter within the authigenic carbonate mineral matrix (Fig. 1b) that could partly derive from microorganisms involved in the formation of such minerals. To identify these microorganisms, DNA was extracted from the carbonate; this is the first time DNA has been obtained from cold seep carbonate crusts and allowed the microbial community structure to be directly evaluated. Bacterial 16S rRNA gene surveys failed to identify sequences

Lipid biomarker analysis

Lipids were analysed to further evaluate the nature of the microbial communities in the crusts. The lipid extracts of both crusts lack biomarkers diagnostic of aerobic methanotrophic bacteria [19], [20], consistent with the results of the DNA analyses. Instead, they contain a highly diverse set of archaeal biomarkers [12], [21] including diphytanylglycerol diethers (archaeol and sn-2- and sn-3-hydroxyarchaeol), glycerol dibiphytanylglycerol tetraethers, as well as saturated and unsaturated C₂₀

Discussion

In sediments, DNA degrades more rapidly than lipids do. Thus, archaeal lipids and archaeal 16S rRNA genes co-occurring in a carbonate crust may not originate from the same organisms, if the methane flux supporting the archaeal methanotrophic communities is no longer active and the carbonate crust has aged prior to sampling.

Preferential preservation of lipids compared to 16S rRNA genes in crust MN16BT2 seems improbable, though. Both the 16S rRNA sequences (the ANME-1 group) and the ¹³C-depleted

Implications and conclusions

Recent studies show that gas hydrate destabilisation following bottom water temperature increase affected past global climate [34] and could be an important aspect of future climate change. Authigenic carbonates formed at cold seeps are both archives of ancient methane release events as well as carbon sinks that potentially mitigate the climatic impact of such events. The microbial organisms and processes we describe provide new insights into the interpretation of methane release from marine

Acknowledgements

Samples of carbonate crusts were obtained during the French–Dutch Medinaut expedition, an integrated geological, geochemical and biological study of mud volcanism and fluid seepage in the eastern Mediterranean Sea. We thank the officers and crew of the Nadir R/V and the Nautile submersible for their helpful co-operation during seagoing activities. Financial support was provided by the French and Dutch funding organisations, IFREMER and NWO-ALW, respectively. We thank Dr Ellen Hopmans (NIOZ) for

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The formation and burial of authigenic carbonate in marine sediment significantly affect the sedimentary carbon cycle and its isotopic mass balance in geological history. Anaerobic oxidation of methane (AOM) is the primary driver of authigenic carbonate precipitation within the sulfate-methane transition zone (SMTZ). Quantitative estimations of the role of AOM on the authigenic carbonate precipitation and its carbon isotope under non-steady-state processes (e.g., changes in methane fluxes at the bottom sediment, sedimentation rates or organic fluxes in the surface sediment), however, are still limited. In this study, we use geochemical data from porewater (e.g., the concentration of sulfate, calcium, magnesium, strontium, dissolved inorganic carbon, total alkalinity) and solid sediment (e.g., organic matter content, and carbonate content) in different depositional environments of the subtropical Beibu Gulf, South China Sea, combined with a diagenetic reactive-transport modelling approach, to estimate the mineralogy of authigenic carbonate, the relationship between AOM and authigenic carbonate precipitation, and the impact of AOM rate on carbon isotope of sediment carbonate (δ¹³C_Car). The results show that high-Mg carbonates (high-Mg calcite and dolomite) are the main type of authigenic carbonate (∼80%) formed in the methane-bearing sediments, leading to higher porewater Sr²⁺/Ca²⁺ (>0.02) and Mg²⁺/Ca²⁺ (>20) within the SMTZ. Our modelling analysis highlights that the non-steady-state induced by increased methane flux from the underlying sediments can significantly accelerate the authigenic carbonates formation within the SMTZ. Using parametric sensitivity analysis, we observed that even a 1% increase in the authigenic carbonate fraction of sediment carbonates results in significant changes in δ¹³C_Car within the SMTZ (from −1‰ to −2‰), mainly due to lighter carbon isotopes produced by more intensive AOM processes. Noteworthily, the terrestrial-to-marine transition was identified by the sediment and porewater geochemical profiles at site SO-8. Although lower authigenic carbonate precipitation occurs in terrestrial sedimentary environments, the proportion of authigenic carbonate in terrestrial environments (11%) is much higher than that in marine environments (1%), resulting in carbon isotopes of carbonate in terrestrial sediments becoming more negative (−5‰).
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¹: Present address: Organic Geochemistry Unit, School of Geochemistry, University of Bristol, Bristol BS8 1TS, UK.

²: Present address: Department of Biological Sciences, University of Idaho, Moscow, ID 83844-3051, USA.

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CH4-consuming microorganisms and the formation of carbonate crusts at cold seeps

Abstract

Introduction

Section snippets

Submersible dives and samples

Mineralogy and stable isotope composition of carbonates

Mineralogy and stable isotope composition

Microbial community structure

Lipid biomarker analysis

Discussion

Implications and conclusions

Acknowledgements

Methane-derived authigenic carbonates formed by subduction-induced pore-water expulsion along the Oregon/Washington margin

Geol. Soc. Am. Bull.

Authigenic carbonates from the Cascadia subduction zone and their relation to gas hydrate stability

Geology

Archaea mediating anaerobic methane oxidation in deep-sea sediments at cold seeps of the eastern Aleutian subduction zone

Org. Geochem.

Molecular and isotopic analysis of anaerobic methane-oxidising communities in marine sediments

Org. Geochem.

Methane-consuming archaeabacteria in marine sediments

Nature

Comparative analysis of methane-oxidising archaea and sulfate-reducing bacteria in anoxic marine sediments

Appl. Environ. Microbiol.

Molecular signals for anaerobic methane oxidation in Black Sea seep carbonates and a microbial mat

Mar. Chem.

Cold seep deposits of Beauvoisin (Oxfordian; southeastern France) and Marmorito (Miocene; northern Italy): microbially induced authigenic carbonates

Int. J. Earth Sci.

Analysis of intact tetraether lipids in archaeal cell material and sediments by high performance liquid chromatography/atmospheric pressure chemical ionization mass spectrometry

Rap. Commun. Mass Spectrom.

Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediment

Appl. Environ. Microbiol.

Association of marine archaea with the digestive tracts of two marine fish species

Appl. Environ. Microbiol.

Biogeochemical and molecular signatures of anaerobic methane oxidation in a marine sediment

Appl. Environ. Microbiol.

A marine microbial consortium apparently mediating anaerobic oxidation of methane

Nature

CH₄-consuming microorganisms and the formation of carbonate crusts at cold seeps