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Despite the widely observed predominance of Cand. Patescibacteria in subsurface communities, their input source and ecophysiology are poorly understood. Here we study mechanisms of the formation of a groundwater microbiome and the subsequent differentiation of Cand. Patescibacteria. In the Hainich Critical Zone Exploratory, Germany, we trace the input of microorganisms from forested soils of preferential recharge areas through fractured aquifers along a 5.4 km hillslope well transect. Cand. Patescibacteria were preferentially mobilized from soils and constituted 66% of species-level OTUs shared between seepage and shallow groundwater. These OTUs, mostly related to Cand. Kaiserbacteraceae, Cand. Nomurabacteraceae, and unclassified UBA9983 at the family level, represented a relative abundance of 71.4% of the Cand. Patescibacteria community at the shallowest groundwater well, and still 44.4% at the end of the transect. Several Cand. Patescibacteria subclass-level groups exhibited preferences for different conditions in the two aquifer assemblages investigated: Cand. Kaiserbacteraceae surprisingly showed positive correlations with oxygen concentrations, while Cand. Nomurabacteraceae were negatively correlated. Co-occurrence network analysis revealed a central role of Cand. Patescibacteria in the groundwater microbial communities and pointed to potential associations with specific organisms, including abundant autotrophic taxa involved in nitrogen, sulfur and iron cycling. Strong associations among Cand. Patescibacteria themselves further suggested that for many groups within this phylum, distribution was mainly driven by conditions commonly supporting a fermentative life style without direct dependence on specific hosts. We propose that import from soil, and community differentiation driven by hydrochemical conditions, including the availability of organic resources and potential hosts, determine the success of Cand. Patescibacteria in groundwater environments.

Across a landscape, aquatic-terrestrial interfaces within and between ecosystems are hotspots of organic matter (OM) mineralization. These interfaces are characterized by sharp spatio-temporal changes in environmental conditions, which affect OM properties and thus control OM mineralization and other transformation processes. Consequently, the extent of OM movement at and across aquatic-terrestrial interfaces is crucial in determining OM turnover and carbon (C) cycling at the landscape scale. Here, we propose expanding current concepts in aquatic and terrestrial ecosystem sciences to comprehensively evaluate OM turnover at the landscape scale. We focus on three main concepts toward explaining OM turnover at the landscape scale: the landscape spatio-temporal context, OM turnover described by priming and ecological stoichiometry, and anthropogenic effects as a disruptor of natural OM transfer magnitudes and pathways. A conceptual framework is introduced that allows for discussing the disparities in spatial and temporal scales of OM transfer, changes in environmental conditions, ecosystem connectivity, and microbial–substrate interactions. The potential relevance of priming effects in both terrestrial and aquatic systems is addressed. For terrestrial systems, we hypothesize that the interplay between the influx of OM and its corresponding elemental composition and the elemental demand of the microbial communities – stoichiometric question – may alleviate spatial and metabolic thresholds. In comparison, substrate level OM dynamics may be substantially different in aquatic systems due to matrix effects that accentuate the role of abiotic conditions, substrate quality, and microbial community dynamics. We highlight the disproportionate impact anthropogenic activities can have on OM cycling across the landscape including reversing natural OM flows through the landscape, disrupting ecosystem connectivity, and nutrient additions that cascade across the landscape. This knowledge is crucial for a better understanding of OM cycling in a landscape context, in particular since terrestrial and aquatic compartments may respond differently to the ongoing changes in climate, land use, and other anthropogenic interferences.

The formation of Fe(III) oxides in natural environments occurs in the presence of natural organic matter (OM), resulting in the formation of OM–mineral complexes that form through adsorption or coprecipitation processes. Thus, microbial Fe(III) reduction in natural environments most often occurs in the presence of OM–mineral complexes rather than pure Fe(III) minerals. This study investigated to what extent does the content of adsorbed or coprecipitated OM on ferrihydrite influence the rate of Fe(III) reduction by Shewanella oneidensis MR-1, a model Fe(III)-reducing microorganism, in comparison to a microbial consortium extracted from the acidic, Fe-rich Schlöppnerbrunnen fen. We found that increased OM content led to increased rates of microbial Fe(III) reduction by S. oneidensis MR-1 in contrast to earlier findings with the model organism Geobacter bremensis. Ferrihydrite–OM coprecipitates were reduced slightly faster than ferrihydrites with adsorbed OM. Surprisingly, the complex microbial consortia stimulated by a mixture of electrons donors (lactate, acetate, and glucose) mimics S. oneidensis under the same experimental Fe(III)-reducing conditions suggesting similar mechanisms of electron transfer whether or not the OM is adsorbed or coprecipitated to the mineral surfaces. We also followed potential shifts of the microbial community during the incubation via 16S rRNA gene sequence analyses to determine variations due to the presence of adsorbed or coprecipitated OM–ferrihydrite complexes in contrast to pure ferrihydrite. Community profile analyses showed no enrichment of typical model Fe(III)-reducing bacteria, such as Shewanella or Geobacter sp., but an enrichment of fermenters (e.g., Enterobacteria) during pure ferrihydrite incubations which are known to use Fe(III) as an electron sink. Instead, OM–mineral complexes favored the enrichment of microbes including Desulfobacteria and Pelosinus sp., both of which can utilize lactate and acetate as an electron donor under Fe(III)-reducing conditions. In summary, this study shows that increasing concentrations of OM in OM–mineral complexes determines microbial Fe(III) reduction rates and shapes the microbial community structure involved in the reductive dissolution of ferrihydrite. Similarities observed between the complex Fe(III)-reducing microbial consortia and the model Fe(III)-reducer S. oneidensis MR-1 suggest electron-shuttling mechanisms dominate in OM-rich environments, including soils, sediments, and fens, where natural OM interacts with Fe(III) oxides during mineral formation.