Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution.

The transition to a terrestrial environment, termed terrestrialization, is generally regarded as a pivotal event in the evolution and diversification of the land plant flora that changed the surface of our planet. Through phylogenomic studies, a group of streptophyte algae, the Zygnematophyceae, have recently been recognized as the likely sister group to land plants (embryophytes). Here, we report genome sequences and analyses of two early diverging Zygnematophyceae (Spirogloea muscicola gen. nov. and Mesotaenium endlicherianum) that share the same subaerial/terrestrial habitat with the earliest-diverging embryophytes, the bryophytes. We provide evidence that genes (i.e., GRAS and PYR/PYL/RCAR) that increase resistance to biotic and abiotic stresses in land plants, in particular desiccation, originated or expanded in the common ancestor of Zygnematophyceae and embryophytes, and were gained by horizontal gene transfer (HGT) from soil bacteria. These two Zygnematophyceae genomes represent a cornerstone for future studies to understand the underlying molecular mechanism and process of plant terrestrialization.

Positive associations fuel soil biodiversity and ecological networks worldwide.

Microbial interactions are key to maintaining soil biodiversity. However, whether negative or positive associations govern the soil microbial system at a global scale remains virtually unknown, limiting our understanding of how microbes interact to support soil biodiversity and functions. Here, we explored ecological networks among multitrophic soil organisms involving bacteria, protists, fungi, and invertebrates in a global soil survey across 20 regions of the planet and found that positive associations among both pairs and triads of soil taxa governed global soil microbial networks. We further revealed that soil networks with greater levels of positive associations supported larger soil biodiversity and resulted in lower network fragility to withstand potential perturbations of species losses. Our study provides unique evidence of the widespread positive associations between soil organisms and their crucial role in maintaining the multitrophic structure of soil biodiversity worldwide.

Soil moisture decline in China's monsoon loess critical zone: More a result of land-use conversion than climate change.

Soil moisture (SM) is essential for sustaining services from Earth's critical zone, a thin-living skin spanning from the canopy to groundwater. In the Anthropocene epoch, intensive afforestation has remarkably contributed to global greening and certain service improvements, often at the cost of reduced SM. However, attributing the response of SM in deep soil to such human activities is a great challenge because of the scarcity of long-term observations. Here, we present a 37 y (1985 to 2021) analysis of SM dynamics at two scales across China's monsoon loess critical zone. Site-scale data indicate that land-use conversion from arable cropland to forest/grassland caused an 18% increase in SM deficit over 0 to 18 m depth (P < 0.01). Importantly, this SM deficit intensified over time, despite limited climate change influence. Across the Loess Plateau, SM storage in 0 to 10 m layer exhibited a significant decreasing trend from 1985 to 2021, with a turning point in 1999 when starting afforestation. Compared with SM storage before 1999, the relative contributions of climate change and afforestation to SM decline after 1999 were -8% and 108%, respectively. This emphasizes the pronounced impacts of intensifying land-use conversions as the principal catalyst of SM decline. Such a decline shifts 18% of total area into an at-risk status, mainly in the semiarid region, thereby threatening SM security. To mitigate this risk, future land management policies should acknowledge the crucial role of intensifying land-use conversions and their interplay with climate change. This is imperative to ensure SM security and sustain critical zone services.

Negative correlation between soil salinity and soil organic carbon variability.

Soil organic carbon (SOC) is vital for terrestrial ecosystems, affecting biogeochemical processes, and soil health. It is known that soil salinity impacts SOC content, yet the specific direction and magnitude of SOC variability in relation to soil salinity remain poorly understood. Analyzing 43,459 mineral soil samples (SOC < 150 g kg-1) collected across different land covers since 1992, we approximate a soil salinity increase from 1 to 5 dS m-1 in croplands would be associated with a decline in mineral soils SOC from 0.14 g kg-1 above the mean predicted SOC ([Formula: see text] = 18.47 g kg-1) to 0.46 g kg-1 below [Formula: see text] (~-430%), while for noncroplands, such decline is sharper, from 0.96 above [Formula: see text] = 35.96 g kg-1 to 4.99 below [Formula: see text] (~-620%). Although salinity's significance in explaining SOC variability is minor (<6%), we estimate a one SD increase in salinity of topsoil samples (0 to 7 cm) correlates with respective [Formula: see text] declines of ~4.4% and ~9.26%, relative to [Formula: see text] and [Formula: see text]. The [Formula: see text] decline in croplands is greatest in vegetation/cropland mosaics while lands covered with evergreen needle-leaved trees are estimated with the highest [Formula: see text] decline in noncroplands. We identify soil nitrogen, land cover, and precipitation Seasonality Index as the most significant parameters in explaining the SOC's variability. The findings provide insights into SOC dynamics under increased soil salinity, improving understanding of SOC stock responses to land degradation and climate warming.

The evolutionary genomics of adaptation to stress in wild rhizobium bacteria.

Microbiota comprise the bulk of life's diversity, yet we know little about how populations of microbes accumulate adaptive diversity across natural landscapes. Adaptation to stressful soil conditions in plants provides seminal examples of adaptation in response to natural selection via allelic substitution. For microbes symbiotic with plants however, horizontal gene transfer allows for adaptation via gene gain and loss, which could generate fundamentally different evolutionary dynamics. We use comparative genomics and genetics to elucidate the evolutionary mechanisms of adaptation to physiologically stressful serpentine soils in rhizobial bacteria in western North American grasslands. In vitro experiments demonstrate that the presence of a locus of major effect, the nre operon, is necessary and sufficient to confer adaptation to nickel, a heavy metal enriched to toxic levels in serpentine soil, and a major axis of environmental soil chemistry variation. We find discordance between inferred evolutionary histories of the core genome and nreAXY genes, which often reside in putative genomic islands. This suggests that the evolutionary history of this adaptive variant is marked by frequent losses, and/or gains via horizontal acquisition across divergent rhizobium clades. However, different nre alleles confer distinct levels of nickel resistance, suggesting allelic substitution could also play a role in rhizobium adaptation to serpentine soil. These results illustrate that the interplay between evolution via gene gain and loss and evolution via allelic substitution may underlie adaptation in wild soil microbiota. Both processes are important to consider for understanding adaptive diversity in microbes and improving stress-adapted microbial inocula for human use.

Role of atmospheric resonance and land-atmosphere feedbacks as a precursor to the June 2021 Pacific Northwest Heat Dome event.

We demonstrate an indirect, rather than direct, role of quasi-resonant amplification of planetary waves in a summer weather extreme. We find that there was an interplay between a persistent, amplified large-scale atmospheric circulation state and soil moisture feedbacks as a precursor for the June 2021 Pacific Northwest "Heat Dome" event. An extended resonant planetary wave configuration prior to the event created an antecedent soil moisture deficit that amplified lower atmospheric warming through strong nonlinear soil moisture feedbacks, favoring this unprecedented heat event.

Electrostatic coupling and water bridging in adsorption hierarchy of biomolecules at water-clay interfaces.

Clay minerals are implicated in the retention of biomolecules within organic matter in many soil environments. Spectroscopic studies have proposed several mechanisms for biomolecule adsorption on clays. Here, we employ molecular dynamics simulations to investigate these mechanisms in hydrated adsorbate conformations of montmorillonite, a smectite-type clay, with ten biomolecules of varying chemistry and structure, including sugars related to cellulose and hemicellulose, lignin-related phenolic acid, and amino acids with different functional groups. Our molecular modeling captures biomolecule-clay and biomolecule-biomolecule interactions that dictate selectivity and competition in adsorption retention and interlayer nanopore trapping, which we determine experimentally by NMR and X-ray diffraction, respectively. Specific adsorbate structures are important in facilitating the electrostatic attraction and Van der Waals energies underlying the hierarchy in biomolecule adsorption. Stabilized by a network of direct and water-bridged hydrogen bonds, favorable electrostatic interactions drive this hierarchy whereby amino acids with positively charged side chains are preferentially adsorbed on the negatively charged clay surface compared to the sugars and carboxylate-rich aromatics and amino acids. With divalent metal cations, our model adsorbate conformations illustrate hydrated metal cation bridging of carboxylate-containing biomolecules to the clay surface, thus explaining divalent cation-promoted adsorption from our experimental data. Adsorption experiments with a mixture of biomolecules reveal selective inhibition in biomolecule adsorption, which our molecular modeling attributes to electrostatic biomolecule-biomolecule pairing that is more energetically favorable than the biomolecule-clay complex. In sum, our findings highlight chemical and structural features that can inform hypotheses for predicting biomolecule adsorption at water-clay interfaces.

Enhanced weathering in the US Corn Belt delivers carbon removal with agronomic benefits.

Terrestrial enhanced weathering (EW) of silicate rocks, such as crushed basalt, on farmlands is a promising scalable atmospheric carbon dioxide removal (CDR) strategy that urgently requires performance assessment with commercial farming practices. We report findings from a large-scale replicated EW field trial across a typical maize-soybean rotation on an experimental farm in the heart of the United Sates Corn Belt over 4 y (2016 to 2020). We show an average combined loss of major cations (Ca2+ and Mg2+) from crushed basalt applied each fall over 4 y (50 t ha-1 y-1) gave a conservative time-integrated cumulative CDR potential of 10.5 ± 3.8 t CO2 ha-1. Maize and soybean yields increased significantly (P < 0.05) by 12 to 16% with EW following improved soil fertility, decreased soil acidification, and upregulation of root nutrient transport genes. Yield enhancements with EW were achieved with significantly (P < 0.05) increased key micro- and macronutrient concentrations (including potassium, magnesium, manganese, phosphorus, and zinc), thus improving or maintaining crop nutritional status. We observed no significant increase in the content of trace metals in grains of maize or soybean or soil exchangeable pools relative to controls. Our findings suggest that widespread adoption of EW across farming sectors has the potential to contribute significantly to net-zero greenhouse gas emissions goals while simultaneously improving food and soil security.

Reconciling carbon quality with availability predicts temperature sensitivity of global soil carbon mineralization.

Soil organic carbon (SOC) mineralization is a key component of the global carbon cycle. Its temperature sensitivity Q10 (which is defined as the factor of change in mineralization with a 10 °C temperature increase) is crucial for understanding the carbon cycle-climate change feedback but remains uncertain. Here, we demonstrate the universal control of carbon quality-availability tradeoffs on Q10. When carbon availability is not limited, Q10 is controlled by carbon quality; otherwise, substrate availability controls Q10. A model driven by such quality-availability tradeoffs explains 97% of the spatiotemporal variability of Q10 in incubations of soils across the globe and predicts a global Q10 of 2.1 ± 0.4 (mean ± one SD) with higher Q10 in northern high-latitude regions. We further reveal that global Q10 is predominantly governed by the mineralization of high-quality carbon. The work provides a foundation for predicting SOC dynamics under climate and land use changes which may alter soil carbon quality and availability.

Climate forcing controls on carbon terrestrial fluxes during shale weathering.

Climate influences near-surface biogeochemical processes and thereby determines the partitioning of carbon dioxide (CO2) in shale, and yet the controls on carbon (C) weathering fluxes remain poorly constrained. Using a dataset that characterizes biogeochemical responses to climate forcing in shale regolith, we implement a numerical model that describes the effects of water infiltration events, gas exchange, and temperature fluctuations on soil respiration and mineral weathering at a seasonal timescale. Our modeling approach allows us to quantitatively disentangle the controls of transient climate forcing and biogeochemical mechanisms on C partitioning. We find that ~3% of soil CO2 (1.02 mol C/m2/y) is exported to the subsurface during large infiltration events. Here, net atmospheric CO2 drawdown primarily occurs during spring snowmelt, governs the aqueous C exports (61%), and exceeds the CO2 flux generated by pyrite and petrogenic organic matter oxidation (~0.2 mol C/m2/y). We show that shale CO2 consumption results from the temporal coupling between soil microbial respiration and carbonate weathering. This coupling is driven by the impacts of hydrologic fluctuations on fresh organic matter availability and CO2 transport to the weathering front. Diffusion-limited transport of gases under transient hydrological conditions exerts an important control on CO2(g) egress patterns and thus must be considered when inferring soil CO2 drawdown from the gas phase composition. Our findings emphasize the importance of seasonal climate forcing in shaping the net contribution of shale weathering to terrestrial C fluxes and suggest that warmer conditions could reduce the potential for shale weathering to act as a CO2 sink.

Principal role of fungi in soil carbon stabilization during early pedogenesis in the high Arctic.

Climate warming is causing widespread deglaciation and pioneer soil formation over glacial deposits. Melting glaciers expose rocky terrain and glacial till sediment that is relatively low in biomass, oligotrophic, and depleted in nutrients. Following initial colonization by microorganisms, glacial till sediments accumulate organic carbon and nutrients over time. However, the mechanisms driving soil nutrient stabilization during early pedogenesis after glacial retreat remain unclear. Here, we traced amino acid uptake by microorganisms in recently deglaciated high-Arctic soils and show that fungi play a critical role in the initial stabilization of the assimilated carbon. Pioneer basidiomycete yeasts were among the predominant taxa responsible for carbon assimilation, which were associated with overall high amino acid use efficiency and reduced respiration. In intermediate- and late-stage soils, lichenized ascomycete fungi were prevalent, but bacteria increasingly dominated amino acid assimilation, with substantially decreased fungal:bacterial amino acid assimilation ratios and increased respiration. Together, these findings demonstrate that fungi are important drivers of pedogenesis in high-Arctic ecosystems that are currently subject to widespread deglaciation from global warming.

Weaker land-atmosphere coupling in global storm-resolving simulation.

The debate on the sign of the soil moisture-precipitation feedback remains open. On the one hand, studies using global coarse-resolution climate models have found strong positive feedback. However, such models cannot represent convection explicitly. On the other hand, studies using km-scale regional climate models and explicit convection have reported negative feedback. Yet, the large-scale circulation is prescribed in such models. This study revisits the soil moisture-precipitation feedback using global, coupled simulations conducted for 1 y with explicit convection and compares the results to coarse-resolution simulations with parameterized convection. We find significant differences in a majority of points with feedback that is weaker and dominantly negative with explicit convection. The model with explicit convection is more often in a wet regime and prefers the triggering of convection over dry soil in the presence of soil moisture heterogeneity, in contrast to the coarse-resolution model. Further analysis indicates that the feedback not only between soil moisture and evapotranspiration but also between evapotranspiration and precipitation is weaker, in better agreement with observations. Our findings suggest that coarse-resolution models may not be well suited to study aspects of climate change over land such as changes in droughts and heatwaves.

Enumerating soil biodiversity.

Soil is an immense habitat for diverse organisms across the tree of life, but just how many organisms live in soil is surprisingly unknown. Previous efforts to enumerate soil biodiversity consider only certain types of organisms (e.g., animals) or report values for diverse groups without partitioning species that live in soil versus other habitats. Here, we reviewed the biodiversity literature to show that soil is likely home to 59 ± 15% of the species on Earth. We therefore estimate an approximately two times greater soil biodiversity than previous estimates, and we include representatives from the simplest (microbial) to most complex (mammals) organisms. Enchytraeidae have the greatest percentage of species in soil (98.6%), followed by fungi (90%), Plantae (85.5%), and Isoptera (84.2%). Our results demonstrate that soil is the most biodiverse singular habitat. By using this estimate of soil biodiversity, we can more accurately and quantitatively advocate for soil organismal conservation and restoration as a central goal of the Anthropocene.

Restoring particulate and mineral-associated organic carbon through regenerative agriculture.

Sustainability of agricultural production and mitigation of global warming rely on the regeneration of soil organic carbon (SOC), in particulate organic carbon (POC) and mineral-associated organic carbon (MAOC) forms. We conducted a global systematic meta-analysis of the effects of regenerative management practices on SOC, POC, and MAOC in cropland, finding: 1) no-till (NT) and cropping system intensification increase SOC (11.3% and 12.4%, respectively), MAOC (8.5% and 7.1%, respectively), and POC (19.7% and 33.3%, respectively) in topsoil (0 to 20 cm), but not in subsoil (>20 cm); 2) experimental duration, tillage frequency, the intensification type, and rotation diversity moderate the effects of regenerative management; and 3) NT synergized with integrated crop-livestock (ICL) systems to greatly increase POC (38.1%) and cropping intensification synergized with ICL systems to greatly increase MAOC (33.1 to 53.6%). This analysis shows that regenerative agriculture is a key strategy to reduce the soil C deficit inherent to agriculture to promote both soil health and long-term C stabilization.

Potassium jarosite seeding of soils decreases lead and arsenic bioaccessibility: A path toward concomitant remediation.

Soils are common sources of metal(loid) contaminant exposure globally. Lead (Pb) and arsenic (As) are of paramount concern due to detrimental neurological and carcinogenic health effects, respectively. Pb and/or As contaminated soils require remediation, typically leading to excavation, a costly and environmentally damaging practice of removing soil to a central location (e.g., hazardous landfill) that may not be a viable option in low-income countries. Chemical remediation techniques may allow for in situ conversion of soil contaminants to phases that are not easily mobilized upon ingestion; however, effective chemical remediation options are limited. Here, we have successfully tested a soil remediation technology using potted soils that relies on converting soil Pb and As into jarosite-group minerals, such as plumbojarosite (PLJ) and beudantite, possessing exceptionally low bioaccessibility [i.e., solubility at gastric pH conditions (pH 1.5 to 3)]. Across all experiments conducted, all new treatment methods successfully promoted PLJ and/or beudantite conversion, resulting in a proportional decrease in Pb and As bioaccessibility. Increasing temperature resulted in increased conversion to jarosite-group minerals, but addition of potassium (K) jarosite was most critical to Pb and As bioaccessibility decreases. Our methods of K-jarosite treatment yielded <10% Pb and As bioaccessibility compared to unamended soil values of approximately 70% and 60%, respectively. The proposed treatment is a rare dual remediation option that effectively treats soil Pb and As such that potential exposure is considerably reduced. Research presented here lays the foundation for ongoing field application.

Moisture-driven divergence in mineral-associated soil carbon persistence.

Mineral stabilization of soil organic matter is an important regulator of the global carbon (C) cycle. However, the vulnerability of mineral-stabilized organic matter (OM) to climate change is currently unknown. We examined soil profiles from 34 sites across the conterminous USA to investigate how the abundance and persistence of mineral-associated organic C varied with climate at the continental scale. Using a novel combination of radiocarbon and molecular composition measurements, we show that the relationship between the abundance and persistence of mineral-associated organic matter (MAOM) appears to be driven by moisture availability. In wetter climates where precipitation exceeds evapotranspiration, excess moisture leads to deeper and more prolonged periods of wetness, creating conditions which favor greater root abundance and also allow for greater diffusion and interaction of inputs with MAOM. In these humid soils, mineral-associated soil organic C concentration and persistence are strongly linked, whereas this relationship is absent in drier climates. In arid soils, root abundance is lower, and interaction of inputs with mineral surfaces is limited by shallower and briefer periods of moisture, resulting in a disconnect between concentration and persistence. Data suggest a tipping point in the cycling of mineral-associated C at a climate threshold where precipitation equals evaporation. As climate patterns shift, our findings emphasize that divergence in the mechanisms of OM persistence associated with historical climate legacies need to be considered in process-based models.

Whole-soil-profile warming does not change microbial carbon use efficiency in surface and deep soils.

The paucity of investigations of carbon (C) dynamics through the soil profile with warming makes it challenging to evaluate the terrestrial C feedback to climate change. Soil microbes are important engines driving terrestrial biogeochemical cycles; their carbon use efficiency (CUE), defined as the proportion of metabolized organic C allocated to microbial biomass, is a key regulator controlling the fate of soil C. It has been theorized that microbial CUE should decline with warming; however, empirical evidence for this response is scarce, and data from deeper soils are particularly scarce. Here, based on soil samples from a whole-soil-profile warming experiment (0 to 1 m, +4 °C) and 18O tracing approach, we examined the vertical variation of microbial CUE and its response to ~3.3-y experimental warming in an alpine grassland on the Qinghai-Tibetan Plateau. Microbial CUE decreased with soil depth, a trend that was primarily controlled by soil C availability. However, warming had limited effects on microbial CUE regardless of soil depth. Similarly, warming had no significant effect on soil C availability, as characterized by extractable organic C, enzyme-based lignocellulose index, and lignin phenol-based ratios of vanillyls, syringyls, and cinnamyls. Collectively, our work suggests that short-term warming does not alter microbial CUE in either surface or deep soils, and emphasizes the regulatory role of soil C availability on microbial CUE.

Decomposition decreases molecular diversity and ecosystem similarity of soil organic matter.

Soil organic matter (SOM) is comprised of a diverse array of reactive carbon molecules, including hydrophilic and hydrophobic compounds, that impact rates of SOM formation and persistence. Despite clear importance to ecosystem science, little is known about broad-scale controls on SOM diversity and variability in soil. Here, we show that microbial decomposition drives significant variability in the molecular richness and diversity of SOM between soil horizons and across a continental-scale gradient in climate and ecosystem type (arid shrubs, coniferous, deciduous, and mixed forests, grasslands, and tundra sedges). The molecular dissimilarity of SOM was strongly influenced by ecosystem type (hydrophilic compounds: 17%, P < 0.001; hydrophobic compounds: 10% P < 0.001) and soil horizon (hydrophilic compounds: 17%, P < 0.001; hydrophobic compounds: 21%, P < 0.001), as assessed using metabolomic analysis of hydrophilic and hydrophobic metabolites. While the proportion of shared molecular features was significantly higher in the litter layer than subsoil C horizons across ecosystems (12 times and 4 times higher for hydrophilic and hydrophobic compounds, respectively), the proportion of site-specific molecular features nearly doubled from the litter layer to the subsoil horizon, suggesting greater differentiation of compounds after microbial decomposition within each ecosystem. Together, these results suggest that microbial decomposition of plant litter leads to a decrease in SOM α-molecular diversity, yet an increase in ß-molecular diversity across ecosystems. The degree of microbial degradation, determined by the position in the soil profile, exerts a greater control on SOM molecular diversity than environmental factors, such as soil texture, moisture, and ecosystem type.

Hydrogen stable isotope probing of lipids demonstrates slow rates of microbial growth in soil.

The rate at which microorganisms grow and reproduce is fundamental to our understanding of microbial physiology and ecology. While soil microbiologists routinely quantify soil microbial biomass levels and the growth rates of individual taxa in culture, there is a limited understanding of how quickly microbes actually grow in soil. For this work, we posed the simple question: what are the growth rates of soil microorganisms? In this study, we measure these rates in three distinct soil environments using hydrogen-stable isotope probing of lipids with 2H-enriched water. This technique provides a taxa-agnostic quantification of in situ microbial growth from the degree of 2H enrichment of intact polar lipid compounds ascribed to bacteria and fungi. We find that growth rates in soil are quite slow and correspond to average generation times of 14 to 45 d but are also highly variable at the compound-specific level (4 to 402 d), suggesting differential growth rates among community subsets. We observe that low-biomass microbial communities exhibit more rapid growth rates than high-biomass communities, highlighting that biomass quantity alone does not predict microbial productivity in soil. Furthermore, within a given soil, the rates at which specific lipids are being synthesized do not relate to their quantity, suggesting a general decoupling of microbial abundance and growth in soil microbiomes. More generally, we demonstrate the utility of lipid-stable isotope probing for measuring microbial growth rates in soil and highlight the importance of measuring growth rates to complement more standard analyses of soil microbial communities.

A soil fungus confers plant resistance against a phytophagous insect by disrupting the symbiotic role of its gut microbiota.

Plants generate energy flows through natural food webs, driven by competition for resources among organisms, which are part of a complex network of multitrophic interactions. Here, we demonstrate that the interaction between tomato plants and a phytophagous insect is driven by a hidden interplay between their respective microbiotas. Tomato plants colonized by the soil fungus Trichoderma afroharzianum, a beneficial microorganism widely used in agriculture as a biocontrol agent, negatively affects the development and survival of the lepidopteran pest Spodoptera littoralis by altering the larval gut microbiota and its nutritional support to the host. Indeed, experiments aimed to restore the functional microbial community in the gut allow a complete rescue. Our results shed light on a novel role played by a soil microorganism in the modulation of plant-insect interaction, setting the stage for a more comprehensive analysis of the impact that biocontrol agents may have on ecological sustainability of agricultural systems.