Vanessa A. Garayburu-Caruso's research while affiliated with Pacific Northwest National Laboratory and other places

Despite the explosion of soil metagenomic data, we lack a synthesized understanding of patterns in the distribution and functions of soil microorganisms. These patterns are critical to predictions of soil microbiome responses to climate change and resulting feedbacks that regulate greenhouse gas release from soils. To address this gap, we assay 1,512 manually curated soil metagenomes using complementary annotation databases, read-based taxonomy, and machine learning to extract multidimensional genomic fingerprints of global soil microbiomes. Our objective is to uncover novel biogeographical patterns of soil microbiomes across environmental factors and ecological biomes with high molecular resolution. We reveal shifts in the potential for (i) microbial nutrient acquisition across pH gradients; (ii) stress-, transport-, and redox-based processes across changes in soil bulk density; and (iii) greenhouse gas emissions across biomes. We also use an unsupervised approach to reveal a collection of soils with distinct genomic signatures, characterized by coordinated changes in soil organic carbon, nitrogen, and cation exchange capacity and in bulk density and clay content that may ultimately reflect soil environments with high microbial activity. Genomic fingerprints for these soils highlight the importance of resource scavenging, plant-microbe interactions, fungi, and heterotrophic metabolisms. Across all analyses, we observed phylogenetic coherence in soil microbiomes—more closely related microorganisms tended to move congruently in response to soil factors. Collectively, the genomic fingerprints uncovered here present a basis for global patterns in the microbial mechanisms underlying soil biogeochemistry and help beget tractable microbial reaction networks for incorporation into process-based models of soil carbon and nutrient cycling. IMPORTANCE We address a critical gap in our understanding of soil microorganisms and their functions, which have a profound impact on our environment. We analyzed 1,512 global soils with advanced analytics to create detailed genetic profiles (fingerprints) of soil microbiomes. Our work reveals novel patterns in how microorganisms are distributed across different soil environments. For instance, we discovered shifts in microbial potential to acquire nutrients in relation to soil acidity, as well as changes in stress responses and potential greenhouse gas emissions linked to soil structure. We also identified soils with putative high activity that had unique genomic characteristics surrounding resource acquisition, plant-microbe interactions, and fungal activity. Finally, we observed that closely related microorganisms tend to respond in similar ways to changes in their surroundings. Our work is a significant step toward comprehending the intricate world of soil microorganisms and its role in the global climate.

Organic matter (OM) composition plays a central role in microbial respiration of dissolved organic matter and subsequent biogeochemical reactions. Here, a direct connection of organic carbon chemistry and thermodynamics to reactive transport simulators has been achieved through the newly developed Lambda-PFLOTRAN workflow tool that succinctly incorporates carbon chemistry data generated from Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS) into reaction networks to simulate organic matter degradation and the resulting biogeochemistry. Lambda-PFLOTRAN is a python-based workflow, executed through a Jupyter Notebook interface, that digests raw FTICR-MS data, develops a representative reaction network based on substrate-explicit thermodynamic modeling (also termed lambda modeling due to its key thermodynamic parameter λ used therein), and completes a biogeochemical simulation with the open source, reactive flow and transport code PFLOTRAN. The workflow consists of the following five steps: configuration, thermodynamic (lambda) analysis, sensitivity analysis, parameter estimation, and simulation output and visualization. Two test cases are provided to demonstrate the functionality of the Lambda-PFLOTRAN workflow. The first test case uses laboratory incubation data of temporal oxygen depletion to fit lambda parameters (i.e., maximum utilization rate and microbial carrying capacity). A slightly more complex second test case fits multiple lambda formulation and soil organic matter release parameters to temporal greenhouse gas generation measured during a soil incubation. Overall, the Lambda-PFLOTRAN workflow facilitates upscaling by using molecular-scale characterization to inform biogeochemical processes occurring at larger scales.

Quantifying the relative influence of factors and processes controlling riverine ecosystem function is essential to predicting future conditions under global change. Dissolved organic matter (DOM) is a fundamental component of riverine ecosystems that fuels microbial food webs, influences nutrient and light availability, and represents a significant carbon flux globally. The heterogeneous nature of DOM molecular composition and its propensity for interaction (i.e., functional diversity) can characterize riverine ecosystem function across spatiotemporal scales. To investigate fundamental drivers of DOM diversity, we collected seasonal water samples from 42 nested locations within five watersheds spanning multiple watershed sizes (~5 to 30,000 km) across the United States. Patterns in DOM molecular diversity and putative biochemical transformations derived from high-resolution mass spectrometry were assessed across gradients of explanatory variables associated with watershed characteristics (e.g., watershed area, water residence time, land cover). We found that putative biochemical transformations were more strongly related to explanatory variables across watersheds than common bulk DOM parameters and that watershed area, surface water residence time and derived Damköhler numbers representing DOM reactivity timescales were strong predictors of DOM diversity. The data also indicate that catchment-specific land cover factors can significantly influence DOM diversity in diverging directions. Overall, the results highlight the importance of considering water residence time and land cover when interpreting longitudinal patterns in DOM chemistry and the continued challenge of identifying generalizable drivers that are transferable across watershed and regional scales for application in Earth system models. This work also introduces a Findable Accessible Interoperable Reusable (FAIR) dataset (>300 samples) to the community for future syntheses.

Areas where groundwater and surface water mix (i.e., hyporheic zones, HZ) contribute substantially to stream ecosystem respiration (ERtot). We rely on reactive transport models to understand HZ respiration at large scales; however, model outputs have not been evaluated with field estimates of ERtot. Here we evaluate the degree to which spatial variation in model-predicted HZ respiration can explain spatial variation in field-estimated ERtot across 32 sites in the Yakima River basin (YRB). We find that predicted HZ respiration did not explain spatial variation in ERtot. We hypothesize that ERtot is influenced by processes that integrate contributions from sediments, such as benthic algae, submerged macrophytes, and shallow HZ. Our results indicate that sediment-associated processes hydrologically connected to the active channel are primary drivers of spatial variation in ERtot in the YRB. We encourage conceptual and physical models of stream ERtot to integrate shallow hyporheic exchange with sediment associated primary production.

River sediment microbial respiration is a key indicator of ecosystem functioning and the biogeochemical fluxes across this critical zone link surface and subsurface waters. As such, there is tremendous interest in measuring and mapping these respiration rates. Respiration observations are expensive and labor intensive; there is limited data available to the community. An open science, collaborative initiative is collecting samples for respiration rate analysis and multi-scale metadata; this evolving data set is being used for making machine learning (ML) predictions at unsampled sites to help inform continued community engagement. However, it is a challenge to find an optimum configuration for ML models to work with this feature-rich (i.e. 100+ possible input variables) data set. Here, we present results from a two-tiered approach to managing the analysis of this complex data set: 1) a stacked ensemble of models that automatically optimizes hyperparameters and manages the training of many models and 2) feature permutation importance to detect the most important features in the models. The major elements of this workflow are modular, portable, open, and cloud-based thus making this implementation a potential template for other applications. The models developed here predict that sediment organic matter chemistry is one of the most important features for predicting sediment respiration rate. Other larger-scale, important features fall into the categories of climatic, ecological, geological, and fluvial settings. Leveraging these larger-scale features to generate data-driven estimates of river sediment respiration rates reveals spatially consistent but heterogeneous patterns across the river network of the Columbia River Basin.

The hyporheic zone is a hotspot for biogeochemical cycling where interactions with mineral metals preserve the release and biodegradation of organic matter (OM). A small fraction of OM can still be exchanged between localized sediments and the overlying water column, and recent evidence suggests there exists a longitudinal structuring in sediment dissolved OM (DOM) chemistry across the continental United States (CONUS). In this study, we tested a hypothesis that water extractable sediment DOM chemistry could be explained by sediment metal contents and integrative watershed scale features at the CONUS scale. Crowdsourced samples were characterized for high resolution mass spectrometry and coupled with sediment metals determined via x‐ray fluorescence as well as with land cover and soil elemental information obtained from national databases. Our results highlight weak relationships between DOM chemistry and elemental composition at the CONUS scale indicating limited transferability of organo‐metal linkages into multi‐scale hydrobiogeochemical models.

Advancing our understanding of dissolved organic matter (DOM) chemistry in aquatic systems necessitates the integration of data streams from multiple analytical platforms. Some measurements require pretreatment with solid phase extraction (SPE), while others are performed directly on whole water samples. Evidence has suggested that SPE will be biased against select DOM fractions, leading to concerns over the ability to establish data linkages across platforms with variable needs for SPE pretreatment, such as those from optical measurements and those that provide high‐resolution molecular information. Here, we directly addressed this concern by assessing the impact of SPE on DOM optical properties through excitation–emission matrices with parallel factor analysis (PARAFAC) for 47 samples across a stream network within a single watershed reflective of variable DOM sources. PARAFAC data was further paired with molecular information obtained by Fourier transform ion cyclotron resonance mass spectrometry (FTICR‐MS). A comparison of PARAFAC models first revealed no systematic qualitative differences in major components between whole water DOM and DOM isolated by SPE (SPE‐DOM); however, quantitative biases against select components were observed. Further linkages with FTICR‐MS data revealed that the molecular fingerprint associated with each PARAFAC component was consistent between the whole water DOM and SPE‐DOM. Our results suggest that bulk scale linkages across these analytical platforms could be inferred irrespective of the observed quantitative biases resulting from SPE for samples within this example watershed. This work represents a key step toward the systematic evaluation of linkages between optical and high‐resolution mass spectrometry datasets in freshwater lotic environments.

Aerobic respiration of organic matter is a key metabolic process influencing carbon (C) biogeochemistry in aquatic ecosystems. Anthropogenic and environmental perturbations to stream ecosystem metabolism can have deleterious effects on downstream water quality. Various environmental features of rivers also influence stream metabolism, including physical (e.g., discharge, light, flow regimes) and chemical factors (nutrients, organic matter) and watershed characteristics (e.g., stream size or drainage area, land use). The relative proportion of surface water contact with benthic sediments has been considered the primary driver of ecosystem processes, including ecosystem respiration (ER). While aquatic ecosystem respiration occurs in the water column (ERwc) and in benthic sediments—including surficial and subsurface sediments (ERsed)—ERsed has long been assumed to be the primary contributor to whole-river ecosystem respiration (ERtot). Recent studies show, however, that somewhere along the river continuum (e.g., 5th–9th order), rivers transition from being dominated by benthic processes to being dominated by water column processes. Yet few metabolism studies have parsed contributions from the water column (ERwc) to ERtot, making it difficult to evaluate the relative magnitude and importance of ERwc across the river continuum and across biomes. In this study, we used the Yakima River basin, Washington, USA, to increase our understanding of basin-scale variation in ERwc. We collected ERwc data and water chemistry samples in triplicate at 47 sites in the Yakima River basin distributed across Strahler stream orders 2–7 and different hydrological and biophysical settings during summer baseflow conditions in 2021. We found that observed ERwc rates were consistently slow throughout the basin during baseflow conditions, ranging from −0.11–0.03 mg O2 L⁻1 d⁻1, and were generally at the very slow end of the range of published ERwc literature values. When compared to reach-scale ERtot rates predicted for rivers across the conterminous United States (CONUS), the very slow ERwc rates we observed throughout the Yakima River basin indicate that ERwc is likely a small component of ERtot in this basin. Despite these slow rates, ERwc nonetheless shows spatial variation across the Yakima River basin that was well explained by watershed characteristics and water chemistry. Multiple linear regression model results show that nitrate (NO3-N), dissolved organic carbon (DOC), and temperature together explained 41.5 % of the spatial variation in ERwc. Supporting the findings of other studies, we found that ERwc increased linearly with increasing NO3-N, increasing DOC, and increasing temperature. We hypothesize that low concentrations of nutrients, DOC, and low temperatures in the water column, coupled with low TSS concentrations, likely contribute to the slow ERwc rates observed throughout the Yakima River basin. Because ERtot measurements integrate contributions from water column respiration and sediment-associated respiration (ERsed), estimating ERtot in cold, clear, low nutrient rivers like those in the Yakima River basin with very slow ERwc will essentially measure contributions from ERsed.