Environmental metabolomes are fundamentally coupled to microbially-linked biogeochemical processes within ecosystems. However, significant gaps exist in our understanding of their spatiotemporal organization, limiting our ability to uncover transferrable principles and predict ecosystem function. We propose that a theoretical paradigm, which integrates concepts from metacommunity ecology, is necessary to reveal underlying mechanisms governing metabolomes. We call this synthesis between ecology and metabolomics ‘meta-metabolome ecology’ and demonstrate its utility using a mass spectrometry dataset. We developed three relational metabolite dendrograms using molecular properties and putative biochemical transformations and performed ecological null modeling. Based upon null modeling results, we show that stochastic processes drove molecular properties while biochemical transformations were structured deterministically. We further suggest that potentially biochemically active metabolites were more deterministically assembled than less active metabolites. Understanding variation in the influences of stochasticity and determinism provides a way to focus attention on which meta-metabolomes and which parts of meta-metabolomes are most likely to be important to consider in mechanistic models. We propose that this paradigm will allow researchers to study the connections between ecological systems and their molecular processes in previously inaccessible detail.

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.

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.

River corridor metabolomes reflect organic matter (OM) processing that drives aquatic biogeochemical cycles. Recent work highlights the power of ultrahigh-resolution mass spectrometry for understanding metabolome composition and river corridor metabolism. However, there have been no studies on the global chemogeography of surface water and sediment metabolomes using ultrahigh-resolution techniques. Here, we describe a community science effort from the Worldwide Hydrobiogeochemistry Observation Network for Dynamic River Systems (WHONDRS) consortium to characterize global metabolomes in surface water and sediment that span multiple stream orders and biomes. We describe the distribution of key aspects of metabolomes including elemental groups, chemical classes, indices, and inferred biochemical transformations. We show that metabolomes significantly differ across surface water and sediment and that surface water metabolomes are more rich and variable. We also use inferred biochemical transformations to identify core metabolic processes shared among surface water and sediment. Finally, we observe significant spatial variation in sediment metabolites between rivers in the eastern and western portions of the contiguous United States. Our work not only provides a basis for understanding global patterns in river corridor biogeochemical cycles but also demonstrates that community science endeavors can enable global research projects that are unfeasible with traditional research models.

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The Worldwide Hydrobiogeochemistry Observation Network for Dynamic River Systems (WHONDRS) aims to galvanize a global community to provide the scientific basis for improved management of dynamic river corridors. WHONDRS is a global research consortium working to understand connections among dynamic hydrology, biogeochemistry, and microbiology in river corridors from local to global scales.

Semiarid ecosystems play a critical role in determining the interannual variability of the global terrestrial carbon sink. Water availability is a critical driver of productivity in semiarid ecosystems, which often alternate between carbon sink/source functioning during wet/dry years. In this study, we investigate how groundwater availability resulting from groundwater‐river water exchange influences net ecosystem exchange of CO2 (NEE), evapotranspiration (ET), and the surface energy balance at two semiarid ecosystems along the Columbia River in central Washington, USA. We examined 1 year of eddy covariance measurements from an upland sagebrush ecosystem primarily fed by rainfall without groundwater access and a riparian grassland ecosystem with groundwater access during the dry season due to lateral groundwater‐river water exchange. The two sites had distinct seasonal patterns of NEE and ET, driven by differences in water availability. While NEE at the upland sagebrush site was strongly constrained by water availability during the dry months, access to groundwater allowed the riparian site to maintain high NEE magnitude and ET during the same dry months. The riparian site had larger annual gross primary productivity than the upland site (612 vs. 424 gC/m2), which was offset by higher ecosystem respiration (558 vs. 363 gC/m2). Thus, the magnitude of the annual NEE at the upland site was larger than that at the riparian site (−62 vs. −54 gC/m2). Our results demonstrate that groundwater access determined by connectivity between groundwater and surface water can be a critical driver of carbon uptake and ET in semiarid ecosystems.