Divergent microbial communities in groundwater and overlying soils exhibit functional redundancy for plant-polysaccharide degradation

Light driven primary production by plants is the main source of biomass in terrestrial ecosystems. But also in subsurface habitats like aquifers, life is fueled largely by this plant-derived biomass. Here, we investigate the degradation of plant-derived polysaccharides in a groundwater microbiome to identify the microbial key players involved, and compare them to those from soil of the groundwater recharge area. We quantified the activities of enzymes degrading the abundant plant polymers starch, cellulose and hemicellulose in oligotrophic groundwater samples, despite the low cell numbers present. Normalized to 16S rRNA gene copy numbers, these activities were only one order of magnitude lower than in soil. Stimulation of the groundwater microbiome with either starch or cellulose and hemicellulose led to changes of the enzymatic activity ratios, indicating autochthonous production of enzymes in response to the plant polymers. Furthermore, DNA stable isotope probing with C-13 labelled plant polymers allowed us to identify microbes involved in the degradation of these compounds. In (hemi)cellulose microcosms, Bacteroidia and Candidatus Parcubacteria were active, while the active community in starch microcosms mostly comprised Candidatus Saccharibacteria, Cytophagia, and Actinobacteria. Not a single one of the active OTUs was also found to be labelled in soil microcosms. This indicates that the degradation of plant-derived polysaccharides in groundwater is driven by organisms completely distinct from those active in soil. The involvement of members of the candidate phyla Cand. Parcubacteria and Cand. Saccharibacteria, organisms known to be abundant in groundwater, in plant-derived organic matter degradation might strongly impact subsurface carbon cycling.