| Abstract: | ![]()
Marine microorganisms adapt to their habitat by structural modification of their membrane lipids. This concept is the basis of numerous molecular proxies used for paleoenvironmental reconstruction. Archaeal tetraether lipids from ubiquitous marine planktonic archaea are particularly abundant, well preserved in the sedimentary record and used in several molecular proxies. We here introduce the direct, extraction-free analysis of these compounds in intact sediment core sections using laser desorption ionization (LDI) coupled to Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS). LDI FTICR-MS can detect the target lipids in single submillimeter-sized spots on sediment sections, equivalent to a sample mass in the nanogram range, and could thus pave the way for biomarker-based reconstruction of past environments and ecosystems at subannual to decadal resolution. We demonstrate that ratios of selected archaeal tetraethers acquired by LDI FTICR-MS are highly correlated with values obtained by conventional liquid chromatography/MS protocols. The ratio of the major archaeal lipids, caldarchaeol and crenarchaeol, analyzed in a 6.2-cm intact section of Mediterranean sapropel S1 at 250-µm resolution (∼4-y temporal resolution), provides an unprecedented view of the fine-scale patchiness of sedimentary biomarker distributions and the processes involved in proxy signal formation. Temporal variations of this lipid ratio indicate a strong influence of the ∼200-y de Vries solar cycle on reconstructed sea surface temperatures with possible amplitudes of several degrees, and suggest signal amplification by a complex interplay of ecological and environmental factors. Laser-based biomarker analysis of geological samples has the potential to revolutionize molecular stratigraphic studies of paleoenvironments.Microbial lipids in aquatic sediments reflect phylogeny, environmental conditions, and biogeochemistry of the water column in which they were produced. After sedimentation and because of the persistence of lipid structures in the sedimentary record, the information archived in these lipids remains available on geological time scales. Retrieval of this information from sediments and rocks has increasingly contributed to our understanding of past environments, microbial communities, and biogeochemical processes (e.g., refs. 1–5). Merged with the concept of molecular stratigraphy (2, 6), i.e., the analysis of selected biomarkers in solvent extracts of sediment samples in a stratigraphic framework, unique information can be gleaned regarding the temporal changes of past ecological and environmental conditions in aquatic systems. Because of analytical requirements, the temporal resolution is typically limited by centimeter-scale-sized samples, which, dependent on the depositional setting, tend to integrate time periods of decades to millennia, even in high-sedimentation settings such as the Santa Barbara Basin (e.g., refs. 4, 7, 8). In consequence, our knowledge of the temporal changes of the environmental and ecological history recorded by lipid biomarkers is rather coarse and based on long-term averages of their distributions in the sedimentary record.In this study we seek to extend this approach to ultra-high-resolution molecular stratigraphy. We focused on archaeal glycerol dialkyl glycerol tetraethers (GDGTs), which are produced by planktonic archaeal communities and are ubiquitous and persistent components in marine sediments (e.g., refs. 9, 10) with widely recognized potential for paleoenvironmental studies. The number of cycloalkyl rings in GDGTs (Fig. S1) appears highly sensitive to ecological and environmental factors such as phylogeny (ref. 5 and references therein), temperature (ref. 11 and references therein), or pH (12, 13). This sensitivity of GDGT composition to environmental and ecological factors has driven the development of multiple molecular proxies. Adaptation to temperature has been demonstrated in thermophilic cultures of archaea (e.g., ref. 14) and serves as concept for the reconstruction of paleo sea surface temperatures (SST) in sediments using the TEX86 (tetraether index of 86 carbon atoms) (3), which is based on fossil lipids of planktonic archaea. This proxy has been used to characterize oscillations of SST in different geological episodes (e.g., refs. 8, 15, 16). Complications could arise from additional GDGT sources, e.g., allochthonous inputs of GDGT-bearing soils, lateral transport, in situ production, and/or recycling by sedimentary archaea (cf. refs. 5, 17). Relative GDGT distributions required for proxy calculations are obtained by HPLC atmospheric pressure chemical ionization mass spectrometry (HPLC/APCI-MS) of solvent extracts from gram-sized sediment samples (18, 19).To enhance temporal resolution of GDGT-based proxies, we explored the utility of laser desorption ionization coupled to Fourier transform ion cyclotron resonance mass spectrometry (LDI FTICR-MS). In LDI, the impact of a pulsed laser beam on the sample leads to desorption, vaporization and ionization of the analytes, forming a cloud of charged molecules. An additional matrix is frequently applied to facilitate the generation of ions (matrix assisted laser desorption ionization [MALDI]). A complete understanding of underlying ionization mechanisms has not been achieved yet (20). LDI or MALDI are best known in the field of proteins or peptides and have also been successfully used in lipid research (21). The fact that LDI analysis can generate ions directly from the sample placed on a sample holder without time-consuming wet-chemical pretreatment while producing mass spectra from submillimeter-sized spots (as small as 10 µm) makes this technique particularly attractive for molecular stratigraphy. LDI may allow direct analysis of nanogram-sized samples on the surface of cut, intact sediment cores at ultra-high spatial resolution, equivalent to temporal resolution on the order of months to decades.We aimed to develop a technique that takes advantage of both the exquisite sensitivity and unequivocal molecular information of ultra-high-resolution mass spectrometry by FTICR-MS and the high spatial resolution of LDI within an intact and unaltered sedimentological context. The key steps of validation and implementation included (Fig. S2) (i) the detection of archaeal GDGTs, (ii) verification of results obtained by LDI FTICR-MS by parallel analysis using established HPLC/APCI-MS methods, and (iii) the examination of the first continuous high-resolution GDGT profile from a sediment core section of the eastern Mediterranean sapropel S1, which was deposited under anoxic conditions during the Holocene climatic optimum (HCO; refs. 22, 23). The data thus may provide an unprecedented view of the dynamic variations of both SST and ecological and environmental factors during sapropel formation. |
