Mobilized dissolved organic matter provides niche space for prokaryotes in the deep subterranean estuary of a sandy beach

Abstract

A fraction of organic carbon in beach sands is mobilizable as dissolved organic matter (DOM). The molecular composition of this mobilizable DOM and its relation to microbial metabolism is central for biogeochemical processes in beach ecosystems, yet, still poorly understood. To identify these DOM-microbe interactions, we analyzed two continuous 24-m-long sediment cores from the high-energy beach of Spiekeroog Island, Germany. The beach is characterized by a deep subterranean estuary (STE), where sediments are flushed by fresh, saline and brackish water. Even though beach sands are generally low in organic carbon, we found that concentrations of mobilizable DOM from sediments were approximately 16 times higher than the in-situ groundwater concentrations. Ultrahigh-resolution mass spectrometry revealed that the mobilized DOM was enriched in labile compounds, providing a potential source of bioavailable carbon for microbial communities. Cluster analyses identified distinct groups of DOM compounds that correlated with specific prokaryotic taxa and demonstrated that DOM composition influences microbial community differentiation revealed by 16S rRNA gene sequence clustering. Aerobic taxa, including Pseudomonadota and Nitrososphaeria, dominated oxic and redox transition zones and were primarily associated with labile, nitrogen-rich DOM clusters. In contrast, anaerobic taxa such as Chloroflexota and Bathyarchaeia, found in deeper sediments, correlated with more recalcitrant DOM compounds. These findings suggest that mobilized DOM contributes to niche differentiation and thus plays a role in shaping microbial community structures in STE sediments. Variations in DOM composition and redox conditions appear to create distinct ecological niches, enabling different prokaryotic taxa to thrive according to their metabolic capacities and substrate preferences.