Carbon limitation leads to thermodynamic regulation of aerobic metabolism

Abstract

13Organic matter (OM) metabolism in freshwater ecosystems is a critical source of uncertainty in 14 global biogeochemical cycles, yet aquatic OM cycling remains poorly understood. Here, we 15 present the first work to explicitly test OM thermodynamics as a key regulator of aerobic 16 respiration, challenging long-held beliefs that organic carbon and oxygen concentrations are the 17 primary determinants of respiration rates. We pair controlled microcosm experiments with 18 ultrahigh-resolution OM characterization to demonstrate a clear relationship between OM 19 thermodynamic favorability and aerobic respiration under carbon limitation. We also 20 demonstrate a shift in the regulation of aerobic respiration from OM thermodynamics to nitrogen 21 content when carbon is in excess, highlighting a central role for OM thermodynamics in aquatic 22 biogeochemical cycling particularly in carbon-limited ecosystems. Our work therefore 23 illuminates a structural gap in aquatic biogeochemical models and presents a new paradigm in 24 which OM thermodynamics and nitrogen content interactively govern aerobic respiration. 25 26 27 3 Metabolism of organic matter (OM) in freshwater ecosystems plays a large role in global 28 biogeochemical cycles 1-3 , as freshwater ecosystems emit more than 2 Pg C yr -1 into the 29 atmosphere 4,5 . These emissions are largely dominated by contributions from river corridors 1,5,6 , 30 and within the river corridor, areas of groundwater-surface water mixing (hyporheic zones) have 31 a disproportionate impact on aerobic respiration 7-9 . Recent field observations have suggested that 32 OM chemistry, and in particular OM thermodynamics, are key to predicting aerobic respiration 33 in hyporheic zones 10-12 . If supported, these observations challenge a widespread paradigm that 34 organic carbon and oxygen concentrations are the primary determinants of aerobic respiration 35 rates and highlight a key source of model uncertainty. Yet, no work has provided direct evidence 36 for OM thermodynamics as a regulator of aerobic respiration in a controlled laboratory 37 environment. Demonstrating this behavior would identify mechanisms that drive field-based 38 phenomena and would enable key properties of OM to be represented in predictive models, 39 thereby contributing to reducing the uncertainty in modeling river corridor biogeochemical 40 cycling 13,14 . 41We use highly controlled aerobic microcosms, non-invasive dissolved oxygen consumption 42 rates, and ultrahigh-resolution OM characterization to investigate the role of OM chemistry in 43 determining aerobic respiration in hyporheic zone sediments. Based on field observations 10-12 , 44 we hypothesized that OM chemistry, including thermodynamic favorability and nitrogen (N) 45 content, would regulate aerobic respiration. Historically, investigations of thermodynamic 46 constraints on microbial metabolism have primarily focused on oxidation-reduction reactions 47 premise that using oxygen as the terminal electron acceptor provides sufficient energy ...

Representing Organic Matter Thermodynamics in Biogeochemical Reactions via Substrate-Explicit Modeling

“…This result challenges classical theories that use the concentrations of bulk substrate pools (such as organic carbon and oxygen) as the sole driving factors of aerobic respiration, notably excluding the influence of OM chemistry on biogeochemistry. The substrate-explicit model is built upon recent experimental studies that reveal a close relationship between OM thermodynamics and aerobic respiration (Graham et al, 2017;Graham et al, 2018;Garayburu-Caruso et al, 2020). Our test cases are broadly consistent with the conclusions of these studies, indicating a need to revise classic theory via incorporation of OM thermodynamics into our understanding and modeling of aerobic respiration.…”

“…For example, a present paradigm in environmental science views aerobic respiration rates as being primarily determined by kinetics (i.e., organic carbon (OC) and oxygen concentrations). However, recent field and laboratory studies suggest that OM thermodynamics can be a main driver of aerobic respiration (Graham et al, 2017;Graham et al, 2018;Stegen et al, 2018b;Garayburu-Caruso et al, 2020). Conventional lumped biogeochemical models are not completely effective for addressing this issue because the thermodynamic properties of substrates are a function of chemical composition of compounds constituting OM pools.…”

Using metacommunity ecology to understand environmental metabolomes

“…Importantly, data collected using an FTICR-MS will include information about any ionizable compound, not just those associated with biological systems 61 . Despite this potential limitation, previous studies have demonstrated that this type of data still contains biogeochemically relevant information 1,2,4,16,17 . Therefore, the three dendrograms described above can resolve the potential relationships between molecular formula based upon a point of view, which is agnostic to a molecular formula's source (MCD), a point of view which encompasses a putative biochemical point of view (TD), and an integrated view (TWCD).…”

“…nvironmental metabolomics enables the investigation of the metabolic processes and interactions occurring within an ecosystem and can provide deep insight into ongoing biogeochemical cycles [1][2][3][4] . High-resolution mass spectrometric techniques, like Orbitrap-MS, Fourier transform ion cyclotron resonance MS (FTICR-MS), and ion mobility spectrometry MS (IMS-MS), among others have allowed researchers to investigate the individual carbon compounds that constitute natural organic matter (NOM) 1,[5][6][7] .…”

“…For example, differential abilities across taxa to scavenge nutrients can lead to a deterministic change in community structure through time 25 . Similarly, individual metabolites within metabolite assemblages will undergo fluctuations in production rate (analogous to birth rate) and degradation rate (analogous to death rate), driven by abiotic or biotic transformations 1,4,11,26 . Distinct from biological systems, however, metabolite 'death' is inherently coupled to metabolite 'birth' as one metabolite is transformed into another.…”