Thaumarchaeota in Marine Sediments

Marine sediments host the largest reservoir of organic carbon in the world as well as a huge number of microorganisms. These complex microbial communities and their associated metabolic activities have a profound impact on global biogeochemical cycles. Understanding their structure and function is crucial for predicting the fate of carbon and other essential elements in the marine system. However, the vast majority of subsurface microorganisms are poorly characterized and their physiological activities remain unknown. One of the most widespread and abundant microbial groups in oceanic sediments are thaumarchaeota, a phylum of archaea formerly referred to as mesophilic crenarchaeota. Thaumarchaeota in aerobic environments, i.e. in the oceanic plankton and in soils and freshwater are capable of aerobic ammonia oxidation and therefore contribute to global nitrogen cycling by performing the first step in nitrification. While the metabolism of thaumarchaeota in marine sediments is unknown, their metabolic activities are expected to be different and probably more versatile since they reside in large numbers in anaerobic horizons of the deep sediments. In this study we will investigate the genomic potential of different thaumarchaeotal clades that typically occur in marine sediments and we will also attempt to cultivate and physiologically characterize representatives of them. Our study builds on an earlier intense investigation of two highly stratified marine sediment cores from the ultra-slow spreading ridge of the North Atlantic (PNAS 2012, 109(42):E2846-55). The 3 m cores exhibited an unusually strong and compressed geochemical layering allowing us to find quantitative correlations between the sediment geochemistry and changes in the microbial communities. Eight out of 15 horizons in these cores were dominated by thaumarchaeota of various subclades typical for deep marine sediments. Samples from these horizons will be used in this project to directly extract DNA for metagenomic investigations and to extract cells for cell sorting and subsequent single cell genomics. In parallel we will set up a variety of enrichments based on the geochemical context data available. Along the project, genomic information will feed into the cultivation strategies and enrichment cultures will in turn be used as starting material for single cell genomics. In addition isotopic studies on actively growing archaeal enrichments will be performed using NanoSIMS imaging (nano secondary ion mass spectrometry) to investigate the assimilation of substrates by certain archaeal clades. Comparative genomic studies of thaumarchaeota from marine sediments will be performed to tackle their specific genomic and physiological adaptations and their evolutionary relationship with other thaumarchaeota and related archaeal clades. Our study will provide insights into the physiological and metabolic potential, genetic setup and evolution of one of the most widespread and abundant, but very little studied microbial groups on this planet.

Marine sediments host the largest reservoir of organic carbon in the world as well as a huge number of microorganisms. These complex microbial communities and their associated metabolic activities have a profound impact on global biogeochemical cycles. Understanding their structure and function is crucial for predicting the fate of carbon and other essential elements in the marine system. Yet, relatively little is known about the activity and adaptations of these microorganisms. In this project we have reconstructed the genomes of archaea from the phylum Thaumarchaeota which are abundant in deep sea sediments. We analyzed samples from the ultra slow spreading ridge in the North Atlantic and from the abyssal plains, i.e. some of the deepest spots in the Pacific Ocean. The eleven reconstructed genomes give information about three different clades that evolved independently, probably from marine and shallow sediment ancestors, respectively. They are all capable of ammonia oxidation like their relatives from marine pelagic oceans and shallow sediments, freshwater or soil. However, they show specific metabolic adaptations and repair mechanisms that allow them to cope with the extreme conditions of the deep ocean, in particular nutrient limitation and high hydrostatic pressure. This includes the capacity to scavenge fermentation products and amino acids from the environment which might support them in saving metabolic energy, and simultaneously implicate them in the global carbon pool turnover in previously undetected ways. In addition, specific capacities to maintain intracellular ion concentrations and extra genes for repair of their genetic material allows these organisms to thrive in such extreme deep sea environments. By reconstructing the ancestors of the different ammonia oxidizing lineages of thaumarchaeota, we demonstrate that this group evolved from an aerobic ancestor in hot springs and by adaptative radiation formed an impressively widespread microbial clade on Earth with all organisms thriving from the same energy metabolism, i.e. by oxidizing ammonia to nitrite and fixing inorganic carbon thus contributing to the nitrogen and carbon cycling on global scales.