The cold microbial majority - marine sulfate-reducing microorganisms

Molecular biology techniques have provided insights into the tremendous genetic diversity, abundance, and distribution of microorganisms on planet Earth. However, we still have a very limited understanding of the metabolic function and thus ecological role of most environmental microorganisms because only a minute fraction of this `microbial majority` is cultivated. Prime examples are sulfate-reducing microorganisms (SRM), ubiquitous inhabitants of anoxic seafloor sediments and key catalysts of the marine sulfur and carbon cycles. Although more than 90% of the seafloor area is exposed to temperatures permanently below 4C, most cultivated SRM are meso- or thermophiles and thus the physiological and genomic features of cold-adapted SRM are poorly characterized. This project aims to fill this gap by using a unique, cultivation-independent approach that combines innovative high-throughput microarray methods and high-resolution single cell techniques to investigate psychrophilic SRM in arctic sediments of the Svalbard archipelago. Based on a 16S rRNA (gene) phylogeography survey of bacteria and archaea, a microarray will be developed for the Svalbard sediment microbiota and applied for identification of psychrophilic SRM that metabolize isotope-labeled substrates supplied at in situ concentrations. The isotope array analyses will reveal (i) the substrate utilization profiles of SRM detected at one sampling site and (ii) the distribution pattern of actively acetate-oxidizing SRM among different Svalbard fjords. These analyses will be complemented by using single cell resolution techniques to quantify the newly identified SRM (by fluorescence in situ hybridization) and to confirm their ecophysiology (by microautoradiography, Raman-microspectroscopy, and/or secondary ion mass spectrometry imaging; NanoSIMS). Finally, by employing targeted single cell genomics approaches where sorting of individual SRM cells is based on their physiology or phylogeny, the genomes of different arctic SRM will be sequenced and analyzed for features that sustain the observed metabolic capabilities under cold temperatures. In summary, this integrated combination of cutting-edge methods has great potential to (i) systematically yield unprecedented insights into the biogeography, ecophysiology, and genetic makeup of a microbial guild that is of global importance in the oceans and (ii) provide a conceptual foundation for the investigation of other uncultivated members of the `microbial majority`.

The ocean floor is for the most part permanently cold (<4C), yet microorganisms are very actively degrading fresh organic matter that sinks down from phytoplankton growth in the water column. Seafloor microorganisms impact global carbon cycling by mineralizing vast quantities of organic matter from pelagic primary production, which is predicted to increase in the Arctic because of diminishing sea ice cover. Up to 50% of available organic carbon in the anoxic marine sediment surface is mineralized by sulfate-reducing microorganisms (SRM), which are thus key players in the oceans sulfur and carbon cycles. However, still little is known about the identity and biology of cold-adapted microorganisms in marine sediments. In this project, we closed knowledge gaps regarding the distribution, substrate use, and genomic composition of SRM and other Arctic seafloor microorganisms that collectively engage in organic carbon degradation. Project highlights include the finding that increased glacier runoff impacts the deep biosphere. Higher sedimentation rates allow ecosystem processes that are typically predominant in surface sediments, such as sulfate reduction, and associated community members to be rapidly buried and also to be maintained at high abundances in deep subsurface sediments. We further found that not all microorganisms that are actively involved in algal biomass degradation, such as acetate-utilizing SRM species, seem to use the substrates for growth and thus an increase in their population size. These different cellular responses of individual species have important implications for the population dynamics of the different functional guild members in marine sediments. We additionally elucidated the identities and functions of several newly discovered microorganisms that are degraders of necromass macromolecules, such as proteins, lipids, and DNA, and provided insights into their genomic-makeup, nutrient sources, and niche partitioning in Arctic marine sediments. For example, members of the order Candidatus Izemoplasmatales are specialized DNA-foragers that have genomes replete with genes for extracellular nucleases and enzymes to use different DNA sub-components.