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Microbial life under extreme energy limitation

Final Report Summary - MICROENERGY (Microbial life under extreme energy limitation)

Half of all prokaryotic microorganisms in the ocean subsist in the deep subsurface seabed with a mean cellular energy flux that is orders of magnitude below anything studied in laboratory cultures so far. Yet, these microorganisms drive major processes in the geosphere and control element cycles that affect hydrocarbon reservoirs, ocean chemistry, and global climate on geological time scales. The main objective of MICROENERGY was to understand the basic functions of these anaerobic communities buried in the seabed and subsisting at the energetic limits of life.

Life in Slow Motion. From data on organic carbon mineralization in marine sediments and from the size of microbial communities responsible for this mineralization we calculated that subsurface microorganisms must live in slow motion with extremely low metabolic rates and with generation times of years to thousands of years. We confirmed this astonishing result by an independent approach, using a molecular clock driven by the spontaneous conversion between L- and D-amino acids (racemization). By that approach, we determined the age of dead microbial biomass and modeled the turnover time of the living biomass. Analyses of endospores in the same sediments show that spore formation is not the main solution to long-term dormancy. Endospores are, however, highly resistant and disperse throughout the ocean to ultimately become buried in the seabed and survive for hundreds of years.

A World of Archaea. Archaea are abundant in the anoxic seabed, yet their metabolic functions were largely unknown. We discovered a systematic shift from total bacterial predominance in surface sediment to equal abundance of archaea and bacteria in the subsurface, a shift apparently caused by the influence of burrowing macrofauna. By cell extraction, cell sorting, and single-cell genome sequencing we could, for the first time, determine the genetic potential of several unknown bacteria and archaea. Some cells belonged to the globally most abundant archaea in marine sediments (MCG, now called Bathyarchaeota) and were found to specialize on extracellular peptide hydrolysis and uptake, a previously unknown function among marine mesophilic archaea. By deep metagenomic sequencing we showed that the newly discovered, deeply-branching group of Asgard archaea with relations to the origin of eukaryotic cells live in the seabed.

How are Processes Controlled? The relative contribution of different physiological groups to the total subsurface communities appears to be controlled by the fraction of free energy allocated to them during the degradation of buried organic matter. By detailed analyses of the substrates and products of microbial metabolism we estimated the potential energetic or kinetic limitation of metabolic rates. The concentrations of intermediates in the anaerobic degradation pathways show surprising little variation between sites or with depth and age. The consumers of these organic acids clearly exert a strong control on their concentration although their turnover time may vary from hours to years.

Shallow Gas: Hot-Spots of Methane Production. We combined pore water analyses from multiple sediment cores with seismo-acoustic transects to model the controls on shallow gas accumulations in marine sediments and to map the hotspots of subsurface methane flux. We discovered a positive feed-back whereby small changes in the sulfate-methane transition are enhanced in much stronger changes in the overall methane production. We could also demonstrate a methane-dependent iron reduction in the deep sub-seafloor of the Baltic Sea. We have now compiled a comprehensive geochemical database on methane and are working on a new global budget of the seabed methane cycle.