Fueling Diversity in the Subsurface: Composition and Age of Dissolved Organic Matter in the Critical Zone

Abstract

Surface ecosystems are rapidly changing on a global scale and it is important to understand how this influences aquifers in the subsurface, as groundwater quality is a major concern for future generations. Dissolved organic matter (DOM) contains molecular and isotopic signals from surface-derived inputs as well as from the biotic and abiotic subsurface environment and is therefore ideal to study the connectivity between both environments. We evaluated a 3-year time series of DOM composition using ultrahigh resolution mass spectrometry and age using 14 C accelerator mass spectrometry along a hillslope well transect in the fractured bedrock of the Hainich Critical Zone Exploratory, Germany. We found a wide range of DOM 14 C depletion, from 14 C = −47.9 to 14 C = −782.4, within different zones of the shallow groundwater. The 14 C content of DOM mirrored the connectivity of the aquifers to the surface. The composition of DOM was highly interrelated with its 14 C age. The proportions of surface-derived DOM components decreased with DOM age, whereas microorganismderived DOM components increased. The intensity of surface-sourced DOM signals differed between the wells and likely reflected the hydrological complexity of fracturedrock environments. During recharge, DOM was more enriched in 14 C, contained more surface-derived molecular components and was more diverse. As a potential response to the varying DOM substrate, bacterial 16S rRNA gene analysis revealed community evolution and increased bacterial diversity during recharge. The influx of diverse, surface-derived DOM potentially fueled evolution within the autochthonous bacterial communities, as in contrast to DOM, the bacterial community did not retreat to the initial diversity and community composition during the recession period. Our results demonstrate on the one hand that combined analyses of the composition and age of groundwater DOM strongly contribute to the understanding of interconnections, community evolution and the functioning of subsurface ecosystems and on the other hand that changes in surface ecosystems have an imprint on subsurface ecosystems.

Bolstering fitness via opportunistic CO2fixation: mixotroph dominance in modern groundwater

“…This opportunistic strategy to use autotrophy to fill up their carbon demand allowed them to dominate the microbial community, with generation times almost as short as the strict autotrophs, with 4 days to less than 2 days. Considering the overall low concentrations but high diversity of organic carbon compounds in the groundwater (Benk et al, 2019;Schwab et al, 2019), such a versatile and adaptive strategy seemed to be superior to focusing on one particular lifestyle. In contrast to organisms restricted to a purely heterotrophic lifestyle in cluster IV and V with generation times of up to 8 days, the ability to use CO 2 fixation as a fill-up function for organic carbon proved highly advantageous in the oligotrophic groundwater.…”

“…Second, microbial cells are transported down from the soils, representing another source of microbial carbon (Herrmann et al, 2019). Third, subsurface organic carbon can also be released from sedimentary rocks, which is often characterized by a higher fraction of aromatic and aliphatic functions, similar to organic carbon from marine sediments rather than soil (Benk et al, 2019). The ability of sulfur oxidizers to access all of these carbon sources, and additionally fix CO 2 , should allow them to thrive independent of variations in the organic carbon supply.…”

Combined Use of Diagnostic Fumarate Addition Metabolites and Genes Provides Evidence for Anaerobic Hydrocarbon Biodegradation in Contaminated Groundwater

“…Although H 2 and acetate were not measured in this study, we can speculate that they were formed in uncontaminated groundwater during the decomposition of dissolved organic matter by syntrophic bacteria acting in concert with methanogens. Previous reports describing microbial communities and biogeochemical transformations in pristine groundwater have suggested such interactions stimulated by dissolved organic matter decomposition [ 53 , 54 ].…”

Groundwater bacterial communities evolve over time, exhibiting oscillating similarity patterns in response to recharge

“…CC-BY 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is The copyright holder for this preprint this version posted March 18, 2021. ; https://doi.org/10.1101/2021.03.18.434713 doi: bioRxiv preprint 5 production due to the lack of sunlight, there is little temperature variation, presumably little to no input of surface-derived fresh, easily available organic carbon (Akob and Küsel, 2011;Benk et al, 2019), and groundwater residence time can exceed those of rivers and lakes. It was therefore assumed that groundwater microbial communities would be relatively stable over time (Griebler and Lueders, 2009).…”

“…Unlike limnic and marine systems, groundwater microbiomes have been largely ignored in temporal studies. Subsurface waters are not driven by seasonally varying primary production due to the lack of sunlight, there is little temperature variation, presumably little to no input of surface-derived fresh, easily available organic carbon (Akob and Küsel, 2011; Benk et al, 2019), and groundwater residence time can exceed those of rivers and lakes. It was therefore assumed that groundwater microbial communities would be relatively stable over time (Griebler and Lueders, 2009).…”