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Final Report Summary - DEEP CARBON FLUX (Energy and carbon food webs of the deep sub-seafloor biosphere)

Vast communities of microorganisms in the sub-seafloor biosphere are responsible for the degradation of deeply buried organic matter (OM) and drive complex metabolic processes of OM mineralization. It remains unknown how the microorganisms subsist at the available energetic limits for life with extremely slow turnover. This project aims to determine the energetic and kinetic controls on the major metabolic processes, in particular the role of small organic acids. These occur in a broad range of concentrations in the pore fluid of recent and old sediments and are key intermediates in the microbial food web. The aim of the DEEP CARBON FLUX project was to develop and apply new and highly sensitive analytical techniques, including 2-dimensional ion chromatography combined with mass spectrometric detection (2D IC-MS). With this new analytical method, combined with measurements of microbial substrate turnover rates, we can analyze both the thermodynamic and the kinetic regulation of predominant microbial processes. The project focused on four systems of study: A) Coastal marine sediment of Aarhus Bay, an easily accessible and intensively studied test site. B) The sediments of the sub-arctic Godhåbsfjord in Southwestern Greenland and the adjacent continental shelf in the Labrador Sea C) The North Pacific where IODP (Integrated Ocean Drilling Program) Expedition 337 drilled approximately 2.5 km deep into sediments harboring several lignite layers. By reaching this depth, expedition 337 set the current depth record in scientific ocean drilling. The low-mature OM encountered here is expected to support diverse microbial communities in spite of over 20 million year age. D) The Baltic Sea where IODP Expedition 347 drilled through several glacial-interglacial sequences with extreme variations in past environmental conditions including OM depleted sedimentary layers.

During the first part of the project, the new analytical method for the analysis of volatile fatty acids (VFAs) in marine pore water samples was successfully developed. The method employs a two dimensional ion chromatography system coupled to a mass spectrometer to quantify the individual acids. In this new approach the first chromatographic dimension is used to separate the VFAs from the inorganic ions in the marine pore water, i.e. chloride and sulfate. The second chromatographic dimension subsequently separates the individual VFAs. Quantification is achieved in a mass spectrometer in the selected ion monitoring mode. The new method enables the quantification of VFAs directly from the marine pore water without the need of further sample pre-treatment and at low detection limits (<0.5 µM).

The newly developed analytical method was used to investigate the pore water concentrations of several VFAs (i.e. formate, acetate, propionate) in the pore water of the drill cores from the four different study sites. We found that the pore water concentrations are surprisingly constant at low concentrations depending on the biochemical zonation of the sediments. In the pore water of sulfate reducing sediments from Arhus Bay, the Godhåbsfjord system and the uppermost layers (0-10 cm) of the sediments in the Baltic Sea, acetate concentrations are balanced around 2-6 µM, formate at 1-4 µM and propionate at approximately 0.5 µM. However, in the deeper methanogenic zones of the Baltic Sea sediments, the concentrations of acetate were slightly higher, but also surprisingly balanced at around 15 - 20 µM. The constant concentrations in the individual biochemical zones show that the VFA concentrations are obviously under the strong control of the microbial communities utilizing these acids as substrates (i.e. sulfate reducers and methanogens). The threshold concentrations, below which acetate is not further depleted by the microbes, differ for the individual biochemical zones and are likely the result of cell physiological constraints of the dominating microbial communities. We used the measured concentrations to calculate the Gibbs energy for the dominant metabolic processes (sulfate reduction and methanogenesis). In the sulfate reduction zones, the energy gained from acetoclastic sulfate reduction decreased with depth from approx. -60 kJ (mol acetate)-1 to -30 kJ (mol acetate)-1. However, the lower energy yield from acetoclastic sulfate reduction at the bottom of the sulfate reduction zone is higher than previously observed for the turnover of hydrogen by sulfate reduction. This shows that thermodynamics alone are not limiting the turnover of VFAs. We used sulfate reduction rates measured by radio tracer incubations to calculate the turnover times of the pore water acetate pool by sulfate reduction and found that the turnover is relatively fast in the range of several hours in the surface-near sediments to 2-3 years at the bottom of the sulfate reduction zones. However, calculated diffusion times of acetate between the individual cells (calculated from cell numbers determined in the sediments) are below one second. This clearly rules out that diffusion is limiting the turnover of VFAs in the sediments. We thus speculate that cell physiological parameter such as membrane transport or activation of the substrates within the cell play an important role in the control of the pore water VFA concentrations and consequently for the available energy from the catabolic reaction. These parameters might be different for individual microbial communities and result in the slightly different VFA pore water concentrations in different biochemical sediment zones.

Water extraction of the deep lignite samples retrieved by IODP Expedition 337 in the North Pacific revealed high contents of format and acetate. Calculation of the energy yield from acetoclastic methanogeneis suggests that acetate is a suitable substrate for methanogenesis in these sediments. The high amounts of extractable VFAs correspond to the high amounts of VFAs chemically bound by ester-functions to the macromolecular organic matrix of the deep coalbeds which were quantified following the application of a selective chemical ester cleavage procedure. These acids represent a long-term reservoir of acetate and formate being released during ongoing geological maturation of the macromolecular organic material.

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