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Crump, A. R.

Publications and source records attributed to Crump, A. R..

3 recordsLinked to original sources

Multi omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone

Biogeochemical hotspots are pervasive at terrestrial-aquatic interfaces, particularly within groundwater-surface water mixing zones (hyporheic zones), and they are critical to understanding spatiotemporal variation in biogeochemical cycling. Here, we use multi omic comparisons of hotspots to low-activity sediments to gain mechanistic insight into hyporheic zone organic matter processing. We hypothesized that microbiome structure and function, as described by metagenomics and metaproteomics, would distinguish hotspots from low-activity sediments through a shift towards carbohydrate-utilizing metabolic pathways and elucidate discrete mechanisms governing organic matter processing in each location. We also expected these differences to be reflected in the metabolome, whereby hotspot carbon (C) pools and metabolite transformations therein would be enriched in sugar-associated compounds. In contrast to expectations, we found pronounced phenotypic plasticity in the hyporheic zone microbiome that was denoted by similar microbiome structure, functional potential, and expression across sediments with dissimilar metabolic rates. Instead, diverse nitrogenous metabolites and biochemical transformations characterized hotspots. Metabolomes also corresponded more strongly to aerobic metabolism than bulk C content only (explaining 67% vs. 42% of variation), and bulk C did not improve statistical models based on metabolome composition alone. These results point to organic nitrogen as a significant regulatory factor influencing hyporheic zone organic matter processing. Based on our findings, we propose incorporating knowledge of metabolic pathways associated with different chemical fractions of C pools into ecosystem models will enhance prediction accuracy.

molecular biology

Riparian vegetation limits oxidation of thermodynamically unfavorable bound-carbon stocks along an aquatic interface

In light of increasing terrestrial carbon (C) transport across aquatic boundaries, the mechanisms governing organic carbon (OC) oxidation along terrestrial-aquatic interfaces are crucial to future climate predictions. Here, we investigate the biochemistry, metabolic pathways, and thermodynamics corresponding to OC oxidation in the Columbia River corridor using ultra-high resolution C characterization. We leverage natural vegetative differences to encompass variation in terrestrial C inputs. Our results suggest that decreases in terrestrial C deposition associated with diminished riparian vegetation induce oxidation of physically -bound OC. We also find that contrasting metabolic pathways oxidize OC in the presence and absence of vegetation and--in direct conflict with the priming concept--that inputs of water-soluble and thermodynamically favorable terrestrial OC protects bound-OC from oxidation. In both environments, the most thermodynamically favorable compounds appear to be preferentially oxidized regardless of which OC pool microbiomes metabolize. In turn, we suggest that the extent of riparian vegetation causes sediment microbiomes to locally adapt to oxidize a particular pool of OC, but that common thermodynamic principles govern the oxidation of each pool (i.e., water-soluble or physically-bound). Finally, we propose a mechanistic conceptualization of OC oxidation along terrestrial-aquatic interfaces that can be used to model heterogeneous patterns of OC loss under changing land cover distributions.\n\nKey pointsO_LIRiparian vegetation protects bound-OC stocks\nC_LIO_LIBiochemical processes associated with OC oxidation vary with vegetation conditions\nC_LIO_LICommon thermodynamic principles underlie OC oxidation regardless of vegetation conditions\nC_LI

ecology

Deterministic assembly processes govern seasonal and spatial variation in microbiomes across hydrologically-connected hyporheic zones

Subsurface groundwater-surface water mixing zones (hyporheic zones) have enhanced biogeochemical activity, but assembly processes governing subsurface microbiomes remain a critical uncertainty in understanding hyporheic biogeochemistry. To address this obstacle, we investigated (a) biogeographical patterns in attached and waterborne microbiomes across three hydrologically-connected, physicochemically-distinct zones (inland hyporheic, nearshore hyporheic, and river); (b) assembly processes that generated these patterns; (c) groups of organisms that corresponded to deterministic changes in the environment; and (d) correlations between these groups and hyporheic metabolism. All microbiomes remained dissimilar through time, but consistent presence of similar taxa suggested dispersal and/or common selective pressures among zones. Further, we demonstrated a pronounced impact of deterministic assembly in all microbiomes as well as seasonal shifts from heterotrophic to autotrophic microorganisms associated with increases in groundwater discharge. The abundance of one statistical cluster of organisms increased with active biomass and respiration, revealing organisms that may strongly influence hyporheic biogeochemistry. Based on our results, we propose a conceptualization of hyporheic zone metabolism in which increased organic carbon concentrations during surface water intrusion support heterotrophy, which succumbs to autotrophy under groundwater discharge. These results provide new opportunities to enhance microbially-explicit ecosystem models describing hyporheic zone biogeochemistry and its influence over riverine ecosystem function.\n\nOriginality-Significance StatementSubsurface zones of groundwater and surface water mixing (hyporheic zones) are hotspots of biogeochemical activity and strongly influence carbon, nutrient and contaminant dynamics within riverine ecosystems. Hyporheic zone microbiomes are responsible for up to 95% of riverine ecosystem respiration, yet the ecology of these microbiomes remains poorly understood. While significant progress is being made in the development of microbially-explicit ecosystem models, poor understanding of hyporheic zone microbial ecology impedes development of such models in this critical zone. To fill the knowledge gap, we present a comprehensive analysis of biogeographical patterns in hyporheic microbiomes as well as the ecological processes that govern their composition and function through space and time. Despite pronounced hydrologic connectivity throughout the hyporheic zone--and thus a strong potential for dispersal--we find that ecological selection deterministically governs microbiome composition within local environments, and we identify specific groups of organisms that correspond to seasonal changes in hydrology. Based on our results, we propose a conceptual model for hyporheic zone metabolism in which comparatively high-organic C conditions during surface water intrusion into the hyporheic zone support heterotrophic metabolisms that succumb to autotrophy during time periods of groundwater discharge. These results provide new opportunities to develop microbially-explicit ecosystem models that incorporate the hyporheic zone and its influence over riverine ecosystem function.

ecology