Carbon Inputs From Riparian Vegetation Limit Oxidation of Physically Bound Organic Carbon Via Biochemical and Thermodynamic Processes

Abstract

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 ultrahigh‐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 protect 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.

Carbon limitation leads to thermodynamic regulation of aerobic metabolism

“…While our results support previous field observations that emphasize the role of OM thermodynamics in predicting aerobic respiration 11,12 , we uniquely underscore the central role for OM thermodynamics in the metabolism of carbon-limited ecosystems using highly controlled laboratory experiments. A field study by Graham et al 11 showed that thermodynamically favorable OM was preferentially metabolized in sediments across a vegetation gradient. Similarly, Stegen et al 12 highlighted the importance of OM thermodynamics in regulating aerobic respiration within hyporheic zones.…”

“…This study was conducted using sediments from the Columbia River hyporheic zone within the Hanford Site 300 Area (approximately 46° 22’ 15.80”N, 119° 85 16’ 31.52”W) in eastern Washington, USA 10,11,45 . Hyporheic zone sediments were collected in April 2018 at five locations, separated by ~2 m (depth: ~30 cm).…”

“…To test the role OM chemistry as a key regulator of aerobic metabolism, we incubated sediments with thermodynamically distinct N-bearing or N-free OM treatments at concentrations commonly observed in freshwater systems (from 0.3 to 9 mg C L −1 , Supplementary Table 1) 12,24,25 . We inferred carbon limitation at low treatment concentrations (< 3 mg C L −1 ) because sediments were collected from a low carbon area (%C < 0.6 as previously discussed in Graham et al 11 ) with observed C:N < 5 11 which is typically associated with carbon limitation 26,27 . In addition, sediments were pre-processed prior to incubation until dissolved organic carbon concentrations were below instrument detection (see Methods and Supplementary Fig.…”

“…We provide direct evidence for OM thermodynamics in controlling aerobic respiration by demonstrating that thermodynamically-favorable OM supported enhanced respiration in microcosms under carbon limitation. We use the mean Gibbs free energy of the half reaction of organic carbon oxidation under standard conditions as a proxy for thermodynamic favorability throughout this paper, as per LaRowe and Van Cappellen 28 , Graham et al 11 , and Stegen et al 12 . Aerobic respiration was negatively correlated with when OM was amended at low concentrations (Fig.…”

Using Bayesian Networks for Sensitivity Analysis of Complex Biogeochemical Models

“…The river stage in the Columbia River is highly dynamic due to the upstream dam operations (Song et al, 2018). Geochemical and biogeochemical modeling for this system is subject to multiple uncertain factors, such as the permeability field controlled by geological formations and within-formation heterogeneity, river stage and river temperature dynamics under future climate scenarios, reaction network, and associated rates impacted by the abiotic environmental conditions as well as the microbial community that are present in the system (Graham et al, 2017;Stegen et al, 2016Stegen et al, , 2018. Therefore, sensitivity analysis is an essential step for better understanding the model system and implementing efficient strategies to reduce the uncertainty in model predictions.…”