Carbon Limitation Leads to Thermodynamic Regulation of Aerobic Metabolism

Abstract

Organic matter (OM) metabolism in freshwater ecosystems is a critical source of uncertainty in global biogeochemical cycles, yet aquatic OM cycling remains poorly understood. Here, we present the first work to explicitly test OM thermodynamics as a key regulator of aerobic respiration, challenging long-held beliefs that organic carbon and oxygen concentrations are the primary determinants of respiration rates. We pair controlled microcosm experiments with ultrahigh-resolution OM characterization to demonstrate a clear relationship between OM thermodynamic favorability and aerobic respiration under carbon limitation. We also demonstrate a shift in the regulation of aerobic respiration from OM thermodynamics to nitrogen content when carbon is in excess, highlighting a central role for OM thermodynamics in aquatic biogeochemical cycling particularly in carbon-limited ecosystems. Our work therefore illuminates a structural gap in aquatic biogeochemical models and presents a new paradigm in which OM thermodynamics and nitrogen content interactively govern aerobic respiration.. CC-BY-NC-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 made Metabolism of organic matter (OM) in freshwater ecosystems plays a large role in global biogeochemical cycles 1-3 , as freshwater ecosystems emit more than 2 Pg C yr -1 into the atmosphere 4,5 . These emissions are largely dominated by contributions from river corridors 1,5,6 , and within the river corridor, areas of groundwater-surface water mixing (hyporheic zones) have a disproportionate impact on aerobic respiration [7][8][9] . Recent field observations have suggested that OM chemistry, and in particular OM thermodynamics, are key to predicting aerobic respiration in hyporheic zones [10][11][12] . If supported, these observations challenge a widespread paradigm that organic carbon and oxygen concentrations are the primary determinants of aerobic respiration rates and highlight a key source of model uncertainty. Yet, no work has provided direct evidence for OM thermodynamics as a regulator of aerobic respiration in a controlled laboratory environment. Demonstrating this behavior would identify mechanisms that drive field-based phenomena and would enable key properties of OM to be represented in predictive models, thereby contributing to reducing the uncertainty in modeling river corridor biogeochemical cycling 13,14 . microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone.

Disturbance Triggers Non-Linear Microbe-Environment Feedbacks

“…The formulae assignments are part of the processing scripts described in ( 70 ). As in previous work ( 32, 34, 47, 49 ), we followed LaRowe and Van Cappellen ( 71 ), we interpret larger values of ΔG 0 Cox to indicate OM that is thermodynamically less favorable for oxidation by microbes. That is, larger values of ΔG 0 Cox indicate OM that provides less net energy to a microbial cell per oxidation event, assuming all else is equal.…”

“…We infer a causal connection between OM thermodynamics and respiration, potentially triggered by desiccation-driven shifts in OM chemistry and/or microbial physiology. This causal connection is supported by recent work ( 49 ) and the observation of a continuous function between ΔG 0 Cox and respiration rate that transcended experimental treatments. Desiccation therefore likely influences and may even initiate an iterative loop among OM thermodynamics, microbial assembly, and biogeochemistry that underlies cumulative system function.…”

“…As key elements of the inferred system of feedbacks, the links among OM thermodynamic properties, respiration, and desiccation found here are consistent with recent work tied to the same field system. That is, Garayburu-Caruso et al ( 49 ) also showed decreasing aerobic respiration with decreasing favorability for oxidation (i.e., larger values of ΔG 0 Cox ) using sediments sourced ~2 years previously from the same field system. In addition, the impacts of desiccation found here are similar to Goldman et al ( 62 ) after re-inundation.…”

“…Factory calibrated oxygen sensor spots (Part# 200001875, diameter = 0.5 cm, detection limit 15 ppb, 0 – 100 % oxygen; PreSens GmbH, Regensburg, Germany) were adhered to the inner vials of the reactor prior to sediment addition. Detailed description of sensor adhesion and non-destructive measurements of DO consumption using these sensors is provided in Garayburo-Caruso et al ( 49 ). Vials were grouped into six treatment regimes (explained in the previous section) representing inundation-drought transitions.…”

“…From the FTICR-MS data, as in previous work ( 32, 34, 47, 49 ), we followed LaRowe and Van Cappellen ( 71 ) to calculate the Gibbs free energy for the half reaction of organic carbon oxidation under standard conditions (ΔG 0 Cox ). This calculation is based on elemental stoichiometries associated with molecular formulae assigned to individual molecules observed in the FTICR-MS data.…”