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.

Stream and river systems transport and process substantial amounts of dissolved organic matter (DOM) from terrestrial and aquatic sources to the ocean, with global biogeochemical implications. However, the underlying mechanisms affecting the spatiotemporal organization of DOM composition are under-investigated. To understand the principles governing DOM composition, we leverage the recently proposed synthesis of metacommunity ecology and metabolomics, termed ‘meta-metabolome ecology.’ Applying this novel approach to a freshwater ecosystem, we demonstrated that despite similar molecular properties across metabolomes, metabolite identity significantly diverged due to environmental filtering. We refer to this phenomenon as ‘thermodynamic redundancy,’ which is analogous to the ecological concept of functional redundancy. We suggest that under thermodynamic redundancy, divergent metabolomes can support equivalent biogeochemical function just as divergent ecological communities can support equivalent ecosystem function. As these analyses are performed in additional ecosystems, potentially generalizable principles, like thermodynamic redundancy, can be revealed and provide insight into DOM dynamics.

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.

Biochemical transformations of organic matter (OM) are a primary driver of river corridor biogeochemistry, thereby modulating ecosystem processes at local to global scales. OM transformations are driven by diverse biotic and abiotic processes, but we lack knowledge of how the diversity of those processes varies across river corridors and across surface and subsurface components of river corridors. To fill this gap we quantified the number of putative biotic and abiotic transformations of organic molecules across diverse river corridors using ultra-high resolution mass spectrometry. The number of unique transformations is used here as a proxy for the diversity of biochemical processes underlying observed profiles of organic molecules. For this, we use public data spanning the contiguous United States (ConUS) from the Worldwide Hydrobiogeochemical Observation Network for Dynamic River Systems (WHONDRS) consortium. Our results show that surface water OM had more biotic and abiotic transformations than OM from shallow hyporheic zone sediments (1–3 cm depth). We observed substantially more biotic than abiotic transformations, and the number of biotic and abiotic transformations were highly correlated with each other. We found no relationship between the number of transformations in surface water and sediments, and no meaningful relationships with latitude, longitude, or climate. We also found that the composition of transformations in sediments was not linked with transformation composition in adjacent surface waters. We infer that OM transformations represented in surface water are an integrated signal of diverse processes occurring throughout the upstream catchment. In contrast, OM transformations in sediments likely reflect a narrower range of processes within the sampled volume. This indicates decoupling between surface water and sediment OM, which is surprising given the potential for hydrologic exchange to homogenize OM. We infer that the processes influencing OM transformations and the scales at which they operate diverge between surface water and sediments.

Conceptual frameworks linking microbial community membership, properties, and processes with the environment and emergent function have been proposed but remain untested. Here we refine and test a recent conceptual framework using hyporheic zone sediments exposed to wetting/drying transitions. Throughout the system we found threshold-like responses to the duration of desiccation. Membership of the putatively active community--but not the whole community--responded due to enhanced deterministic selection (an emergent community property). Concurrently, the thermodynamic properties of organic matter became less favorable for oxidation (an environmental component) and respiration decreased (a microbial process). While these responses were step functions of desiccation, we observed continuous monotonic relationships among community assembly, respiration, and organic matter thermodynamics. Placing the results in context of our conceptual framework points to previously unrecognized internal feedbacks that are initiated by disturbance, mediated by thermodynamics, and that cause the impacts of disturbance to be dependent on the history of disturbance.

Rivers receive substantial dissolved organic matter (DOM) input from the land and transport it to the ocean. As DOM travels through watersheds, it undergoes biotic and abiotic transformations that impact biogeochemical cycles and any subsequent CO ₂ release into the atmosphere. While recent research has increased our mechanistic knowledge of DOM composition within watersheds, DOM development across broad spatial distances and within divergent biomes is under investigated. Here, we combined DOM characterization, geochemical analyses, and shotgun metagenomics to analyze samples from seven rivers ranging from the U.S. Pacific Northwest to Berlin, Germany. Initial analyses revealed that many DOM properties were distinguished by river type (e.g., wastewater, headwater) and that geochemistry often explained variation across rivers. At a global scale, analyses rooted in meta-metabolome ecology indicated that DOM was structured overwhelmingly by deterministic selection. When controlling for scale, however, analyses indicated that ecological assembly dynamics were again partially structured by river type. Finally, microbial analyses revealed that many riverine microbes from our systems shared core metabolic functional potential while differing in peripheral capabilities in across the rivers. Further analysis of the carbon degradation potential for recovered metagenomically assembled genomes indicated that the sampled rivers had strong taxonomically conserved niche differentiation and that carbon degradation potential diversity was significantly related to organic matter diversity. Together, these results help us uncover interconnections between the development of DOM, riverine geochemistry, and microbial functional potential.