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Molecular-life signatures and organic-matter transformations at the temperature limit of life, IODP Exp. 370

Subject Area Palaeontology
Mineralogy, Petrology and Geochemistry
Term from 2018 to 2021
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 408178672
 
Final Report Year 2021

Final Report Abstract

This project investigated microbial lipid compositions and organic matter transformations along strong thermal gradients in the Nankai Trough. These analyses were performed within the framework of IODP Expedition 370, which was implemented to explore the upper temperature of life of the deep biosphere off Cape Muroto, Nankai Trough, Japan. For this, Site C0023 was established, which is characterized by an extraordinarily high heat flow where temperatures at the sediment-basement interface reach the currently known temperature limit of life at around 120°C. Due to extremely low cell counts, traditional molecular biological techniques were not successful at providing information on the microbial community composition. With this project, we were able to gain meaningful information on the distribution of bacterial and archaeal communities by intact polar lipid analysis down to sediment depths of 827 mbsf (ca. 92°C). Hereby, we detected lipid biomarkers characteristic for sedimentary methanogens and unclassified heterotrophic archaea in the upper half of the core where methane concentrations were highest. This confirms the presence of methanogens in a zone where methane isotope compositions and hydrogenotrophic methanogenesis rates point to biological methane production. The detected archaeal lipids include acyclic glycerol, butanetriol and pentanetriol dialkyl glycerol tetraethers and archaeol with glycosidic headgroups (G-GDGT-0, G-BDGT-0, G-PDGT-0. G-Archaeol). Below 600 mbsf archaeal IPLs reach values that are below detection coinciding with a minimal cell abundance zone. Below this zone G- GDGTs and G-Archaeols are intermittently detected with a spike within the Décollement indicating a potential connection between biomass abundance and lithology. Bacterial lipids at Site C0023 represent a mixture of phospholipids and glycolipids and were detectable down to depths of 515 mbsf. Bacterial IPL concentrations were in a similar range as archaeal IPLs. Even though the detected bacterial lipids are not diagnostic for certain types of organisms their distributions point to a selective adaptation to increasing temperatures and pressure. At 55°C microbial cells strongly decline presumably as a consequence of the collapse of mesophilic communities with increasing temperatures, however, IPL concentrations remain elevated. This spike in IPL over cell concentrations coincides with a rise in endospore concentrations and is likely reflective of a fossil microbial community that lived at these depths before temperatures rose to >50°C. This observation suggests that IPLs in ultra-low biomass environments may provide a timeintegrated signal of present and past benthic life rather than a snapshot of the currently active in situ microbial communities. A stark decline in all detected lipids (intact and core lipids) coincides with the onset of the thermal breakdown of organic matter, but with different reaction rates for different lipids, reflecting their different thermal stabilities. For core lipids a selective preservation of GDGTs with different number of rings is observed with important implications for the application of these compounds as paleoenvironmental proxies. In this project we also tested the hypothesis that the thermal breakdown of organic material provides substantial bioavailable substrates that may directly feed indigenous microbial communities at high temperatures, providing a link between these abiotic and biotic zones. Using hydrous pyrolysis experiments we could confirm the potential for the generation of abiotic substrates, such as methane and acetate that may be used by indigenous microorganism living at elevated temperatures. Our results demonstrate a strong control of temperature on organic matter availability as sediments with a higher thermal overprint generate lower substrate yields, nevertheless, experimentally generated substrate release still mostly exceeded in situ concentrations irrespective of the thermal history. Our findings suggest that cell abundance in the Nankai Trough is not only governed by gradually increasing temperatures, but is a combination of many factors, including lithology, hydrothermal fluid flow and substrate availability.

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