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DOE OSTI2025

The Emergence and Promise of Functional Chemogeography of Organic Matter

Organisms in ecosystems continuously release a myriad of organic matter molecules that undergo microbial and abiotic transformation, processes that critically influence carbon storage and climate feedbacks. Yet, a systematic understanding of what determines the transformation and persistence of organic matter across spatiotemporal scales remains elusive. We propose an emerging framework, termed “functional chemogeography,” to understand transformation and persistence of organic matter based on the chemical traits of molecules. This framework extends beyond a sole focus on intrinsic traits, which remain relatively constant across spatiotemporal scales, to emphasize extrinsic traits such as biochemical transformations and environmental responses, which vary spatiotemporally and are shaped by both intrinsic traits and the environment. When upscaled to the assemblage level using functional diversity indices, these extrinsic traits reveal a significant, and in some cases superior, capacity than intrinsic traits to explain biogeochemical processes, as demonstrated through a case study of dissolved organic matter in China's lakes. In conclusion, by integrating trait-based perspectives into predictive models, this framework helps bridge chemical complexity with ecosystem biogeochemistry, thereby advancing our ability to predict the fate of global organic carbon under environmental change.

chemical traits↗

DOE OSTI2026

Correlational selection and genetic architecture shape the evolution of the leaf economics spectrum in a perennial grass

The generality of the worldwide leaf economics spectrum (LES) has made it a pillar of trait-based ecological research. Yet, few studies have examined the processes shaping the evolution of the LES within species, in part, because most species occupy only a small portion of the LES. Here, to address this gap, we took advantage of the distinct leaf economics strategies present in different ecotypes of the phenotypically diverse perennial grass Panicum virgatum (switchgrass) to generate a genetic mapping population, which we planted in common gardens at three sites spanning 12 degrees of latitude in the central United States. With this genetic mapping population, we evaluated two potentially interacting causes of LES evolution: 1) genetic architecture, where multiple traits are influenced by either the same gene (pleiotropy) or by genes in close physical proximity (genetic linkage), and 2) correlational selection, where selection acts on traits in combination rather than in isolation. We found that shared genetic architecture influenced covariation between photosynthetic rate (A MASS ) and leaf nitrogen (N MASS ) and between A MASS and leaf mass per area (LMA). We also found that correlational selection favored the trait combinations predicted by the LES (e.g., high LMA with low N MASS or low LMA with high N MASS ) and disfavored other, mismatched trait combinations at two of the three sites. Together, these results demonstrate how the evolution of an integrated LES within species can arise from multiple evolutionary causes.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Drought impacts on microbial trait distribution and feedback to soil carbon cycling

Abstract Quantifying the impact of drought on microbial processes and its consequences for soil carbon cycling is hindered by the lack of underlying mechanistic understanding. Therefore, there is a need to scale up the physiological response to changing water status from individual soil microbes to collective communities across different ecosystems. Here we propose the use of a framework that incorporates trait‐based ecology to link drought‐impacted microbial processes to rates of soil carbon decomposition and stabilisation. We briefly synthesise existing knowledge on the effects of drought on microbial physiology at the individual to community scale, before integrating this understanding within a framework incorporating life‐history strategy, ecological strategy and biochemistry. This framework highlights a dynamic allocation to high yield (Y), resource acquisition (A) and stress tolerance (S) pathways as environmental conditions change. Y‐A‐S strategies represent sets of traits that tend to correlate due to physiological or evolutionary trade‐offs. This framework enables assessment of microbial processes along two key environmental gradients of water and resource availability, both of which are constrained by drought. The variable chemistry of biomass and necromass produced under different physiological strategies in response to drying–rewetting impacts organic matter decomposition and stabilisation in soils, and should also be considered when quantifying soil carbon balance. We highlight that diversion of resources away from microbial growth can alter soil organic matter chemistry and its persistence depending on the kind of microbial compounds produced. To advance such a framework, we highlight avenues of research that would enable the further identification and quantification of traits linked to Y‐A‐S strategies and the physiological outcomes at the community level under drought and rewetting, and conclude by hypothesising how ecosystem‐level changes might feedback on to the soil carbon cycle. A scalable understanding of microbial drought‐response mechanisms affecting soil carbon cycling will transform the way microbial physiology is represented in ecosystem studies. Read the free Plain Language Summary for this article on the Journal blog.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2026

Divergent trait controls on soluble sugars and starch underlie global strategies of tree carbohydrate storage

Nonstructural carbohydrate (NSC) stores buffer tree metabolism, osmotic regulation, and defense, thereby mediating tolerance and survival under climate extremes. Yet, the functional and evolutionary determinants of interspecific variation in NSC remain elusive, limiting understanding and prediction of forest carbon allocation and mortality under global change. Here, we present a cross-species synthesis of NSC concentrations across multiple organs for 281 woody species from 102 mixed forest communities worldwide, where we quantified species-specific deviations from community means to disentangle intrinsic trait effects from environmental and methodological variation. We found phylogenetic signals in NSC deviations, with coniferous gymnosperms and evergreen species consistently maintaining lower stem soluble sugars and starch concentrations than co-occurring angiosperms and deciduous species, respectively. A global pattern emerged where greater stomatal sensitivity to leaf water potential was associated with declines in the relative concentrations of both sugars and starch. In contrast, xylem hydraulic safety traits showed weak and organ-dependent relationships with NSC concentrations. Sugars increased with photosynthetic capacity and declined with wood density, whereas starch showed the reverse pattern, which aligned with the distinct functional-metabolic roles of sugars and starch. By integrating trait-based ecology with a community-centered framework, our study provides global evidence that stomatal regulation, photosynthetic capacity, specific leaf area, and wood density jointly govern interspecific NSC variation, through contrasting effects on sugars and starch. These are among the most broadly measured traits globally, thus the emergent carbohydrate–trait relationships can have broad applications toward understanding and predicting forest growth and survival under climate change.

tropic system↗

DOE OSTI2025

Microbiome Adaptation Could Amplify Modeled Projections of Global Soil Carbon Loss With Climate Warming

Warming alters soil microbial traits through ecological and evolutionary processes, directly influencing the decomposition of organic matter, which significantly affects global soil carbon emissions. Yet, soil carbon models largely ignore these processes and their implications for global responses to warming. Here, we incorporate eco-evolutionary theory into a mechanistic model describing microbial soil carbon decomposition to address the question of whether such processes could have consequential effects on climate carbon feedbacks globally. We assume that a key trait of microbes, their resource allocation to production of exoenzymes (which facilitate decomposition of organic matter)—is optimized to environmental temperatures by natural selection. We find that eco-evolutionary optimization results in microbes allocating more resources to enzyme production under warming. When applied at the global scale, eco-evolutionary optimization enhances the biological realism of soil carbon models and significantly amplifies global soil carbon loss by 2100. Our results highlight the significant potential of microbial eco-evolutionary responses to influence carbon cycle feedbacks to climate change, and motivate an urgent need for more comprehensive data to accurately quantify the adaptive potential of microbiomes in response to climate change.

Biodiversity & Conservation↗

DOE OSTI2023

Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems

Soil fungi belonging to different functional guilds, such as saprotrophs, pathogens, and mycorrhizal symbionts, play key roles in forest ecosystems. To date, no study has compared the actual gene expression of these guilds in different forest soils. We used metatranscriptomics to study the competition for organic resources by these fungal groups in boreal, temperate, and Mediterranean forest soils. Using a dedicated mRNA annotation pipeline combined with the JGI MycoCosm database, we compared the transcripts of these three fungal guilds, targeting enzymes involved in C- and N mobilization from plant and microbial cell walls. Genes encoding enzymes involved in the degradation of plant cell walls were expressed at a higher level in saprotrophic fungi than in ectomycorrhizal and pathogenic fungi. However, ectomycorrhizal and saprotrophic fungi showed similarly high expression levels of genes encoding enzymes involved in fungal cell wall degradation. Transcripts for N-related transporters were more highly expressed in ectomycorrhizal fungi than in other groups. Here, we showed that ectomycorrhizal and saprotrophic fungi compete for N in soil organic matter, suggesting that their interactions could decelerate C cycling. Metatranscriptomics provides a unique tool to test controversial ecological hypotheses and to better understand the underlying ecological processes involved in soil functioning and carbon stabilization.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Conditional filamentation as an adaptive trait of bacteria and its ecological significance in soils

Bacteria can regulate cell morphology in response to environmental conditions, altering their physiological and metabolic characteristics to improve survival. Conditional filamentation, in which cells suspend division while continuing lateral growth, is a strategy with a range of adaptive benefits. Here, we review the causes and consequences of conditional filamentation with respect to bacterial physiology, ecology and evolution. We describe four major benefits from conditional filamentation: stress tolerance, surface colonization, gradient spanning and the facilitation of biotic interactions. Adopting a filamentous growth habit involves fitness trade-offs which are also examined. We focus on the role of conditional filamentation in soil habitats, where filamentous morphotypes are highly prevalent and where environmental heterogeneity can benefit a conditional response. Here, to illustrate the use of information presented in our review, we tested the conditions regulating filamentation by the forest soil isolate Paraburkholderia elongata 5N T . Filamentation by P. elongata was induced at elevated phosphate concentrations, and was associated with the accumulation of intracellular polyphosphate, highlighting the role of filamentation in a phosphate-solubilizing bacterium. Conditional filamentation enables bacteria to optimize their growth and metabolism in environments that are highly variable, a trait that can impact succession, symbioses, and biogeochemistry in soil environments.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Deep ocean metagenomes provide insight into the metabolic architecture of bathypelagic microbial communities

The deep sea, the largest ocean’s compartment, drives planetary-scale biogeochemical cycling. Yet, the functional exploration of its microbial communities lags far behind other environments. Here we analyze 58 metagenomes from tropical and subtropical deep oceans to generate the Malaspina Gene Database. Free-living or particle-attached lifestyles drive functional differences in bathypelagic prokaryotic communities, regardless of their biogeography. Ammonia and CO oxidation pathways are enriched in the free-living microbial communities and dissimilatory nitrate reduction to ammonium and H 2 oxidation pathways in the particle-attached, while the Calvin Benson-Bassham cycle is the most prevalent inorganic carbon fixation pathway in both size fractions. Reconstruction of the Malaspina Deep Metagenome-Assembled Genomes reveals unique non-cyanobacterial diazotrophic bacteria and chemolithoautotrophic prokaryotes. The widespread potential to grow both autotrophically and heterotrophically suggests that mixotrophy is an ecologically relevant trait in the deep ocean. These results expand our understanding of the functional microbial structure and metabolic capabilities of the largest Earth aquatic ecosystem.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Organizing principles for vegetation dynamics

Understanding vegetation dynamics is very challenging because of the multitude of contributing processes at 64widely different spatial and temporal scales. In this Perspective we propose that understanding of vegetation dynamics can be improved, permitting better predictions, based on organizing principles that constrain plant and ecosystem be haviour: natural selection, self-organization, and entropy maximization. Although these ideas are increasingly used,a limited common understanding of their theoretical basis has prevented their full potential to be realized. We explain the power of natural selection-based optimality to predict photosynthesis and carbon allocation responses to multiple environmental drivers, and how individual plasticity leads to the predictable self-organization of forest canopies. We show how models of natural selection acting on a few key traits can generate realistic plant communities, and how entropy maximization can distinguish between stochastic and deterministic drivers of vegetation patterns. In combination with empirical exploration of patterns in plant functional variation, these principles can accelerate the development of dynamic vegetation models as well as trait-based ecology resting on strengthened theoretical and empirical foundations.

Geosciences↗

DOE OSTI2023

Codon Optimization Improves the Prediction of Xylose Metabolism from Gene Content in Budding Yeasts

Xylose is the second most abundant monomeric sugar in plant biomass. Consequently, xylose catabolism is an ecologically important trait for saprotrophic organisms, as well as a fundamentally important trait for industries that hope to convert plant mass to renewable fuels and other bioproducts using microbial metabolism. Although common across fungi, xylose catabolism is rare within Saccharomycotina, the subphylum that contains most industrially relevant fermentative yeast species. The genomes of several yeasts unable to consume xylose have been previously reported to contain the full set of genes in the XYL pathway, suggesting the absence of a gene–trait correlation for xylose metabolism. Here, we measured growth on xylose and systematically identified XYL pathway orthologs across the genomes of 332 budding yeast species. Although the XYL pathway coevolved with xylose metabolism, we found that pathway presence only predicted xylose catabolism about half of the time, demonstrating that a complete XYL pathway is necessary, but not sufficient, for xylose catabolism. We also found that XYL1 copy number was positively correlated, after phylogenetic correction, with xylose utilization. We then quantified codon usage bias of XYL genes and found that XYL3 codon optimization was significantly higher, after phylogenetic correction, in species able to consume xylose. Finally, we showed that codon optimization of XYL2 was positively correlated, after phylogenetic correction, with growth rates in xylose medium. We conclude that gene content alone is a weak predictor of xylose metabolism and that using codon optimization enhances the prediction of xylose metabolism from yeast genome sequence data.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Leaf angle as a leaf and canopy trait: Rejuvenating its role in ecology with new technology

Abstract Life on Earth depends on the conversion of solar energy to chemical energy by plants through photosynthesis. A fundamental challenge in optimizing photosynthesis is to adjust leaf angles to efficiently use the intercepted sunlight under the constraints of heat stress, water loss and competition. Despite the importance of leaf angle, until recently, we have lacked data and frameworks to describe and predict leaf angle dynamics and their impacts on leaves to the globe. We review the role of leaf angle in studies of ecophysiology, ecosystem ecology and earth system science, and highlight the essential yet understudied role of leaf angle as an ecological strategy to regulate plant carbon–water–energy nexus and to bridge leaf, canopy and earth system processes. Using two models, we show that leaf angle variations have significant impacts on not only canopy‐scale photosynthesis, energy balance and water use efficiency but also light competition within the forest canopy. New techniques to measure leaf angles are emerging, opening opportunities to understand the rarely‐measured intraspecific, interspecific, seasonal and interannual variations of leaf angles and their implications to plant biology and earth system science. We conclude by proposing three directions for future research.

Yang, Xi↗

DOE OSTI2020

Whole genome resequencing reveals genomic regions associated with thermal adaptation in redband trout

Abstract Adaptation to local environments involves evolution of ecologically important traits and underlying physiological processes. Here, we used low coverage whole‐genome resequencing (lcWGR) on individuals to identify genome regions involved in thermal adaptation in wild redband trout Oncorhynchus mykiss gairdneri , a subspecies of rainbow trout that inhabits ecosystems ranging from cold montane forests to high elevation deserts. This study includes allele frequency‐based analyses for selective sweeps among populations, followed by multiple association tests for specific sets of phenotypes measured under thermal stress (acute and chronic survival/mortality; high or low cardiac performance groups). Depending on the groups in each set of analyses, sequencing reads covered 43%–75% of the genome at ≥15× and each analysis included millions of SNPs across the genome. In tests for selective sweeps among populations, a total of six chromosomal regions were significant. The further association tests for specific phenotypes revealed that the region on chromosome 4 was consistently the most significant and contains the cerk gene (ceramide kinase). This study provides insight into a potential genetic mechanism of local thermal adaptation and suggests c erk may be an important candidate gene. However, further validation of this cerk gene is necessary to determine if the association with cardiac performance results in a functional role to influence thermal performance when exposed to high water temperatures and hypoxic conditions.

Chen, Zhongqi↗

DOE OSTI2021

Evolution of pathogen tolerance and emerging infections: A missing experimental paradigm

Researchers worldwide are repeatedly warning us against future zoonotic diseases resulting from humankind’s insurgence into natural ecosystems. The same zoonotic pathogens that cause severe infections in a human host frequently fail to produce any disease outcome in their natural hosts. What precise features of the immune system enable natural reservoirs to carry these pathogens so efficiently? To understand these effects, we highlight the importance of tracing the evolutionary basis of pathogen tolerance in reservoir hosts, while drawing implications from their diverse physiological and life-history traits, and ecological contexts of host-pathogen interactions. Long-term co-evolution might allow reservoir hosts to modulate immunity and evolve tolerance to zoonotic pathogens, increasing their circulation and infectious period. Such processes can also create a genetically diverse pathogen pool by allowing more mutations and genetic exchanges between circulating strains, thereby harboring rare alive-on-arrival variants with extended infectivity to new hosts (i.e., spillover). Finally, we end by underscoring the indispensability of a large multidisciplinary empirical framework to explore the proposed link between evolved tolerance, pathogen prevalence, and spillover in the wild.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Fine-Root Ecology Database (FRED): A Global Collection of Root Trait Data with Coincident Site, Vegetation, Edaphic, and Climatic Data, Version 3.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2022

What are mycorrhizal traits?

Traits are inherent properties of organisms, but how are they defined for organismal networks such as mycorrhizal symbioses? Mycorrhizal symbioses are complex and diverse belowground symbioses between plants and fungi that have proved challenging to fit into a unified and coherent trait framework. Here we propose an inclusive mycorrhizal trait framework that classifies traits as morphological, physiological, and phenological features that have functional implications for the symbiosis. We further classify mycorrhizal traits by location – plant, fungus, or the symbiosis – which highlights new questions in trait-based mycorrhizal ecology designed to charge and challenge the scientific community. This new framework is an opportunity for researchers to interrogate their data to identify novel insights and gaps in our understanding of mycorrhizal symbioses.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2026

Fine-Root Ecology Database (FRED): A Global Collection of Root Trait Data with Coincident Site, Vegetation, Edaphic, and Climatic Data, Version 4.

To address the need for a centralized root trait database, we compiled the Fine-Root Ecology Database (FRED) from published and unpublished data sources. We have continued to add to the FRED database since the release of FRED 1.0 in 2017, followed by 2.0 in 2018, and 3.0 in 2021. This new release of FRED 4.0 now has 213,941 observations of 238 root traits, for a combined total of roughly 3.4 million data fields for root traits and ancillary data together. FRED 4.0 has 39.8% more root trait observations than FRED 3.0 and a 34.4% increase in unique data sources. This release of FRED 4.0 also includes significant increases in geographic regions that have long been underrepresented in global datasets, notably in the tropical low latitudes. Ancillary data on associated site, vegetation, edaphic, and climatic conditions from across the globe have also increased concurrently with root trait observations. FRED is focused on fine roots (traditionally defined as roots less than 2 mm in diameter), as coarse roots are studied using different methodology, often at very different scales, and have different traits and trait interpretations. Despite this fine-root focus, FRED accepts data collected from roots of all sizes and contains observations of many root classes including coarse roots. Data collection will continue for the foreseeable future. The FRED4_Entire_Database_2026.csv file is the flat csv data file for FRED 4.0, and the FRED4_dd.csv file is the data dictionary of all columns available in FRED, including column IDs, column names, definitions, and unit (where applicable).

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements

In the context of a recent massive increase in research on plant root functions and their impact on the environment, root ecologists currently face many important challenges to keep on generating cutting-edge, meaningful and integrated knowledge. Consideration of the below-ground components in plant and ecosystem studies has been consistently called for in recent decades, but methodology is disparate and sometimes inappropriate. This handbook, based on the collective effort of a large team of experts, will improve trait comparisons across studies and integration of information across databases by providing standardised methods and controlled vocabularies. It is meant to be used not only as starting point by students and scientists who desire working on below-ground ecosystems, but also by experts for consolidating and broadening their views on multiple aspects of root ecology. Beyond the classical compilation of measurement protocols, we have synthesised recommendations from the literature to provide key background knowledge useful for: (1) defining below-ground plant entities and giving keys for their meaningful dissection, classification and naming beyond the classical fine-root vs coarse-root approach; (2) considering the specificity of root research to produce sound laboratory and field data; (3) describing typical, but overlooked steps for studying roots (e.g. root handling, cleaning and storage); and (4) gathering metadata necessary for the interpretation of results and their reuse. Most importantly, all root traits have been introduced with some degree of ecological context that will be a foundation for understanding their ecological meaning, their typical use and uncertainties, and some methodological and conceptual perspectives for future research. Considering all of this, we urge readers not to solely extract protocol recommendations for trait measurements from this work, but to take a moment to read and reflect on the extensive information contained in this broader guide to root ecology, including sections I–VII and the many introductions to each section and root trait description. Finally, it is critical to understand that a major aim of this guide is to help break down barriers between the many subdisciplines of root ecology and ecophysiology, broaden researchers’ views on the multiple aspects of root study and create favourable conditions for the inception of comprehensive experiments on the role of roots in plant and ecosystem functioning.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Phylogenomic structure and speciation in an emerging model: the Sphagnum magellanicum complex (Bryophyta)

Sphagnum magellanicum is one of two Sphagnum species for which a reference-quality genome exists to facilitate research in ecological genomics. Phylogenetic and comparative genomic analyses were conducted based on resequencing data from 48 samples and RADseq analyses based on 187 samples. Here, we report that there are four clades/species within the S. magellanicum complex in eastern North America and that the reference genome belongs to Sphagnum divinum . The species exhibit tens of thousands (RADseq) to millions (resequencing) of fixed nucleotide differences. Two species, however, referred to informally as S. diabolicum and S. magni because they have not been formally described, are differentiated by only 100 (RADseq) to 1000 (resequencing) of differences. Introgression among species in the complex is demonstrated using D-statistics and f 4 ratios. One ecologically important functional trait, tissue decomposability, which underlies peat (carbon) accumulation, does not differ between segregates in the S. magellanicum complex, although previous research showed that many closely related Sphagnum species have evolved differences in decomposability/carbon sequestration. Phylogenetic resolution and more accurate species delimitation in the S. magellanicum complex substantially increase the value of this group for studying the early evolutionary stages of climate adaptation and ecological evolution more broadly.

59 BASIC BIOLOGICAL SCIENCES↗