Iron Chelation in Soil: Scalable Biotechnology for Accelerating Carbon Dioxide Removal by Enhanced Rock Weathering.

Enhanced rock weathering (EW) is an emerging atmospheric carbon dioxide removal (CDR) strategy being scaled up by the commercial sector. Here, we combine multiomics analyses of belowground microbiomes, laboratory-based dissolution studies, and incubation investigations of soils from field EW trials to build the case for manipulating iron chelators in soil to increase EW efficiency and lower costs. Microbial siderophores are high-affinity, highly selective iron (Fe) chelators that enhance the uptake of Fe from soil minerals into cells. Applying RNA-seq metatranscriptomics and shotgun metagenomics to soils and basalt grains from EW field trials revealed that microbial communities on basalt grains significantly upregulate siderophore biosynthesis gene expression relative to microbiomes of the surrounding soil. Separate in vitro laboratory incubation studies showed that micromolar solutions of siderophores and high-affinity synthetic chelator (ethylenediamine-N,N'-bis-2-hydroxyphenylacetic acid, EDDHA) accelerate EW to increase CDR rates. Building on these findings, we develop a potential biotechnology pathway for accelerating EW using the synthetic Fe-chelator EDDHA that is commonly used in agronomy to alleviate the Fe deficiency in high pH soils. Incubation of EW field trial soils with potassium-EDDHA solutions increased potential CDR rates by up to 2.5-fold by promoting the abiotic dissolution of basalt and upregulating microbial siderophore production to further accelerate weathering reactions. Moreover, EDDHA may alleviate potential Fe limitation of crops due to rising soil pH with EW over time. Initial cost-benefit analysis suggests potassium-EDDHA could lower EW-CDR costs by up to U.S. $77 t CO2 ha-1 to improve EW's competitiveness relative to other CDR strategies.

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.

Chemistry-albedo feedbacks offset up to a third of forestation's CO2 removal benefits.

Forestation is widely proposed for carbon dioxide (CO2) removal, but its impact on climate through changes to atmospheric composition and surface albedo remains relatively unexplored. We assessed these responses using two Earth system models by comparing a scenario with extensive global forest expansion in suitable regions to other plausible futures. We found that forestation increased aerosol scattering and the greenhouse gases methane and ozone following increased biogenic organic emissions. Additionally, forestation decreased surface albedo, which yielded a positive radiative forcing (i.e., warming). This offset up to a third of the negative forcing from the additional CO2 removal under a 4°C warming scenario. However, when forestation was pursued alongside other strategies that achieve the 2°C Paris Agreement target, the offsetting positive forcing was smaller, highlighting the urgency for simultaneous emission reductions.

Initial Validation of a Soil-Based Mass-Balance Approach for Empirical Monitoring of Enhanced Rock Weathering Rates.

Enhanced rock weathering (ERW) is a promising scalable and cost-effective carbon dioxide removal (CDR) strategy with significant environmental and agronomic co-benefits. A major barrier to large-scale implementation of ERW is a robust monitoring, reporting, and verification (MRV) framework. To successfully quantify the amount of carbon dioxide removed by ERW, MRV must be accurate, precise, and cost-effective. Here, we outline a mass-balance-based method in which analysis of the chemical composition of soil samples is used to track in situ silicate rock weathering. We show that signal-to-noise issues of in situ soil analysis can be mitigated by using isotope-dilution mass spectrometry to reduce analytical error. We implement a proof-of-concept experiment demonstrating the method in controlled mesocosms. In our experiment, a basalt rock feedstock is added to soil columns containing the cereal crop Sorghum bicolor at a rate equivalent to 50 t ha-1. Using our approach, we calculate rock weathering corresponding to an average initial CDR value of 1.44 ± 0.27 tCO2eq ha-1 from our experiments after 235 days, within error of an independent estimate calculated using conventional elemental budgeting of reaction products. Our method provides a robust time-integrated estimate of initial CDR, to feed into models that track and validate large-scale carbon removal through ERW.

Improved net carbon budgets in the US Midwest through direct measured impacts of enhanced weathering.

Terrestrial enhanced weathering (EW) through the application of Mg- or Ca-rich rock dust to soil is a negative emission technology with the potential to address impacts of climate change. The effectiveness of EW was tested over 4 years by spreading ground basalt (50 t ha-1 year-1 ) on maize/soybean and miscanthus cropping systems in the Midwest US. The major elements of the carbon budget were quantified through measurements of eddy covariance, soil carbon flux, and biomass. The movement of Mg and Ca to deep soil, released by weathering, balanced by a corresponding alkalinity flux, was used to measure the drawdown of CO2 , where the release of cations from basalt was measured as the ratio of rare earth elements to base cations in the applied rock dust and in the surface soil. Basalt application stimulated peak biomass and net primary production in both cropping systems and caused a small but significant stimulation of soil respiration. Net ecosystem carbon balance (NECB) was strongly negative for maize/soybean (-199 to -453 g C m-2 year-1 ) indicating this system was losing carbon to the atmosphere. Average EW (102 g C m-2 year-1 ) offset carbon loss in the maize/soybean by 23%-42%. NECB of miscanthus was positive (63-129 g C m-2 year-1 ), indicating carbon gain in the system, and EW greatly increased inorganic carbon storage by an additional 234 g C m-2 year-1 . Our analysis indicates a co-deployment of a perennial biofuel crop (miscanthus) with EW leads to major wins-increased harvested yields of 29%-42% with additional carbon dioxide removal (CDR) of 8.6 t CO2 ha-1 year-1 . EW applied to maize/soybean drives a CDR of 3.7 t CO2 ha-1 year-1 , which partially offsets well-established carbon losses from soil from this crop rotation. EW applied in the US Midwest creates measurable improvements to the carbon budgets perennial bioenergy crops and conventional row crops.

Physiological responses to low CO2 over prolonged drought as primers for forest-grassland transitions.

Savannahs dominated by grasses with scattered C3 trees expanded between 24 and 9 million years ago in low latitudes at the expense of forests. Fire, herbivory, drought and the susceptibility of trees to declining atmospheric CO2 concentrations ([CO2]a) are proposed as key drivers of this transition. The role of disturbance is well studied, but physiological arguments are mostly derived from models and palaeorecords, without direct experimental evidence. In replicated comparative experimental trials, we examined the physiological effects of [CO2]a and prolonged drought in a broadleaf forest tree, a savannah tree and a savannah C4 grass. We show that the forest tree was more disadvantaged than either the savannah tree or the C4 grass by the low [CO2]a and increasing aridity. Our experiments provide insights into the role of the intrinsic physiological susceptibility of trees in priming the disturbance-driven transition from forest to savannah in the conditions of the early Miocene.

Legume-microbiome interactions unlock mineral nutrients in regrowing tropical forests.

Legume trees form an abundant and functionally important component of tropical forests worldwide with N2-fixing symbioses linked to enhanced growth and recruitment in early secondary succession. However, it remains unclear how N2-fixers meet the high demands for inorganic nutrients imposed by rapid biomass accumulation on nutrient-poor tropical soils. Here, we show that N2-fixing trees in secondary Neotropical forests triggered twofold higher in situ weathering of fresh primary silicates compared to non-N2-fixing trees and induced locally enhanced nutrient cycling by the soil microbiome community. Shotgun metagenomic data from weathered minerals support the role of enhanced nitrogen and carbon cycling in increasing acidity and weathering. Metagenomic and marker gene analyses further revealed increased microbial potential beneath N2-fixers for anaerobic iron reduction, a process regulating the pool of phosphorus bound to iron-bearing soil minerals. We find that the Fe(III)-reducing gene pool in soil is dominated by acidophilic Acidobacteria, including a highly abundant genus of previously undescribed bacteria, Candidatus Acidoferrum, genus novus. The resulting dependence of the Fe-cycling gene pool to pH determines the high iron-reducing potential encoded in the metagenome of the more acidic soils of N2-fixers and their nonfixing neighbors. We infer that by promoting the activities of a specialized local microbiome through changes in soil pH and C:N ratios, N2-fixing trees can influence the wider biogeochemical functioning of tropical forest ecosystems in a manner that enhances their ability to assimilate and store atmospheric carbon.

Technologies to deliver food and climate security through agriculture.

Agriculture is a major contributor to environmental degradation and climate change. At the same time, a growing human population with changing dietary preferences is driving ever increasing demand for food. The need for urgent reform of agriculture is widely recognized and has resulted in a number of ambitious plans. However, there is credible evidence to suggest that these are unlikely to meet the twin objectives of keeping the increase in global temperature within the target of 2.0 °C above preindustrial levels set out in the Paris Agreement and delivering global food security. Here, we discuss a series of technological options to bring about change in agriculture for delivering food security and providing multiple routes to the removal of CO2 from the atmosphere. These technologies include the use of silicate amendment of soils to sequester atmospheric CO2, agronomy technologies to increase soil organic carbon, and high-yielding resource-efficient crops to deliver increased agricultural yield, thus freeing land that is less suited for intensive cropping for land use practices that will further increase carbon storage. Such alternatives include less intensive regenerative agriculture, afforestation and bioenergy crops coupled with carbon capture and storage technologies.

Phosphate availability and ectomycorrhizal symbiosis with Pinus sylvestris have independent effects on the Paxillus involutus transcriptome.

Many plant species form symbioses with ectomycorrhizal fungi, which help them forage for limiting nutrients in the soil such as inorganic phosphate (Pi). The transcriptional responses to symbiosis and nutrient-limiting conditions in ectomycorrhizal fungal hyphae, however, are largely unknown. An artificial system was developed to study ectomycorrhizal basidiomycete Paxillus involutus growth in symbiosis with its host tree Pinus sylvestris at different Pi concentrations. RNA-seq analysis was performed on P. involutus hyphae growing under Pi-limiting conditions, either in symbiosis or alone. We show that Pi starvation and ectomycorrhizal symbiosis have an independent effect on the P. involutus transcriptome. Notably, low Pi availability induces expression of newly identified putative high-affinity Pi transporter genes, while reducing the expression of putative organic acid transporters. Additionally, low Pi availability induces a close transcriptional interplay between P and N metabolism. GTP-related signalling was found to have a positive effect in the maintenance of ectomycorrhizal symbiosis, whereas multiple putative cytochrome P450 genes were found to be downregulated, unlike arbuscular mycorrhizal fungi. We provide the first evidence of global transcriptional changes induced by low Pi availability and ectomycorrhizal symbiosis in the hyphae of P. involutus, revealing both similarities and differences with better-characterized arbuscular mycorrhizal fungi.

Potential for large-scale CO2 removal via enhanced rock weathering with croplands.

Enhanced silicate rock weathering (ERW), deployable with croplands, has potential use for atmospheric carbon dioxide (CO2) removal (CDR), which is now necessary to mitigate anthropogenic climate change1. ERW also has possible co-benefits for improved food and soil security, and reduced ocean acidification2-4. Here we use an integrated performance modelling approach to make an initial techno-economic assessment for 2050, quantifying how CDR potential and costs vary among nations in relation to business-as-usual energy policies and policies consistent with limiting future warming to 2 degrees Celsius5. China, India, the USA and Brazil have great potential to help achieve average global CDR goals of 0.5 to 2 gigatonnes of carbon dioxide (CO2) per year with extraction costs of approximately US$80-180 per tonne of CO2. These goals and costs are robust, regardless of future energy policies. Deployment within existing croplands offers opportunities to align agriculture and climate policy. However, success will depend upon overcoming political and social inertia to develop regulatory and incentive frameworks. We discuss the challenges and opportunities of ERW deployment, including the potential for excess industrial silicate materials (basalt mine overburden, concrete, and iron and steel slag) to obviate the need for new mining, as well as uncertainties in soil weathering rates and land-ocean transfer of weathered products.

Phylogenomics indicates the "living fossil" Isoetes diversified in the Cenozoic.

The fossil record provides an invaluable insight into the temporal origins of extant lineages of organisms. However, establishing the relationships between fossils and extant lineages can be difficult in groups with low rates of morphological change over time. Molecular dating can potentially circumvent this issue by allowing distant fossils to act as calibration points, but rate variation across large evolutionary scales can bias such analyses. In this study, we apply multiple dating methods to genome-wide datasets to infer the origin of extant species of Isoetes, a group of mostly aquatic and semi-aquatic isoetalean lycopsids, which closely resemble fossil forms dating back to the Triassic. Rate variation observed in chloroplast genomes hampers accurate dating, but genome-wide nuclear markers place the origin of extant diversity within this group in the mid-Paleogene, 45-60 million years ago. Our genomic analyses coupled with a careful evaluation of the fossil record indicate that despite resembling forms from the Triassic, extant Isoetes species do not represent the remnants of an ancient and widespread group, but instead have spread around the globe in the relatively recent past.

Increased yield and CO2 sequestration potential with the C4 cereal Sorghum bicolor cultivated in basaltic rock dust-amended agricultural soil.

Land-based enhanced rock weathering (ERW) is a biogeochemical carbon dioxide removal (CDR) strategy aiming to accelerate natural geological processes of carbon sequestration through application of crushed silicate rocks, such as basalt, to croplands and forested landscapes. However, the efficacy of the approach when undertaken with basalt, and its potential co-benefits for agriculture, require experimental and field evaluation. Here we report that amending a UK clay-loam agricultural soil with a high loading (10 kg/m2 ) of relatively coarse-grained crushed basalt significantly increased the yield (21 ± 9.4%, SE) of the important C4 cereal Sorghum bicolor under controlled environmental conditions, without accumulation of potentially toxic trace elements in the seeds. Yield increases resulted from the basalt treatment after 120 days without P- and K-fertilizer addition. Shoot silicon concentrations also increased significantly (26 ± 5.4%, SE), with potential benefits for crop resistance to biotic and abiotic stress. Elemental budgets indicate substantial release of base cations important for inorganic carbon removal and their accumulation mainly in the soil exchangeable pools. Geochemical reactive transport modelling, constrained by elemental budgets, indicated CO2 sequestration rates of 2-4 t CO2 /ha, 1-5 years after a single application of basaltic rock dust, including via newly formed soil carbonate minerals whose long-term fate requires assessment through field trials. This represents an approximately fourfold increase in carbon capture compared to control plant-soil systems without basalt. Our results build support for ERW deployment as a CDR technique compatible with spreading basalt powder on acidic loamy soils common across millions of hectares of western European and North American agriculture.

Lineage-based functional types: characterising functional diversity to enhance the representation of ecological behaviour in Land Surface Models.

Process-based vegetation models attempt to represent the wide range of trait variation in biomes by grouping ecologically similar species into plant functional types (PFTs). This approach has been successful in representing many aspects of plant physiology and biophysics but struggles to capture biogeographic history and ecological dynamics that determine biome boundaries and plant distributions. Grass-dominated ecosystems are broadly distributed across all vegetated continents and harbour large functional diversity, yet most Land Surface Models (LSMs) summarise grasses into two generic PFTs based primarily on differences between temperate C3 grasses and (sub)tropical C4 grasses. Incorporation of species-level trait variation is an active area of research to enhance the ecological realism of PFTs, which form the basis for vegetation processes and dynamics in LSMs. Using reported measurements, we developed grass functional trait values (physiological, structural, biochemical, anatomical, phenological, and disturbance-related) of dominant lineages to improve LSM representations. Our method is fundamentally different from previous efforts, as it uses phylogenetic relatedness to create lineage-based functional types (LFTs), situated between species-level trait data and PFT-level abstractions, thus providing a realistic representation of functional diversity and opening the door to the development of new vegetation models.

Organellomic data sets confirm a cryptic consensus on (unrooted) land-plant relationships and provide new insights into bryophyte molecular evolution.

PREMISE: Phylogenetic trees of bryophytes provide important evolutionary context for land plants. However, published inferences of overall embryophyte relationships vary considerably. We performed phylogenomic analyses of bryophytes and relatives using both mitochondrial and plastid gene sets, and investigated bryophyte plastome evolution. METHODS: We employed diverse likelihood-based analyses to infer large-scale bryophyte phylogeny for mitochondrial and plastid data sets. We tested for changes in purifying selection in plastid genes of a mycoheterotrophic liverwort (Aneura mirabilis) and a putatively mycoheterotrophic moss (Buxbaumia), and compared 15 bryophyte plastomes for major structural rearrangements. RESULTS: Overall land-plant relationships conflict across analyses, generally weakly. However, an underlying (unrooted) four-taxon tree is consistent across most analyses and published studies. Despite gene coverage patchiness, relationships within mosses, liverworts, and hornworts are largely congruent with previous studies, with plastid results generally better supported. Exclusion of RNA edit sites restores cases of unexpected non-monophyly to monophyly for Takakia and two hornwort genera. Relaxed purifying selection affects multiple plastid genes in mycoheterotrophic Aneura but not Buxbaumia. Plastid genome structure is nearly invariant across bryophytes, but the tufA locus, presumed lost in embryophytes, is unexpectedly retained in several mosses. CONCLUSIONS: A common unrooted tree underlies embryophyte phylogeny, [(liverworts, mosses), (hornworts, vascular plants)]; rooting inconsistency across studies likely reflects substantial distance to algal outgroups. Analyses combining genomic and transcriptomic data may be misled locally for heavily RNA-edited taxa. The Buxbaumia plastome lacks hallmarks of relaxed selection found in mycoheterotrophic Aneura. Autotrophic bryophyte plastomes, including Buxbaumia, hardly vary in overall structure.

Mid-Devonian Archaeopteris Roots Signal Revolutionary Change in Earliest Fossil Forests.

The origin of trees and forests in the Mid Devonian (393-383 Ma) was a turning point in Earth history, marking permanent changes to terrestrial ecology, geochemical cycles, atmospheric CO2 levels, and climate. However, how all these factors interrelate remains largely unknown. From a fossil soil (palaeosol) in the Catskill region near Cairo NY, USA, we report evidence of the oldest forest (mid Givetian) yet identified worldwide. Similar to the famous site at Gilboa, NY, we find treefern-like Eospermatopteris (Cladoxylopsida). However, the environment at Cairo appears to have been periodically drier. Along with a single enigmatic root system potentially belonging to a very early rhizomorphic lycopsid, we see spectacularly extensive root systems here assigned to the lignophyte group containing the genus Archaeopteris. This group appears pivotal to the subsequent evolutionary history of forests due to possession of multiple advanced features and likely relationship to subsequently dominant seed plants. Here we show that Archaeopteris had a highly advanced root system essentially comparable to modern seed plants. This suggests a unique ecological role for the group involving greatly expanded energy and resource utilization, with consequent influence on global processes much greater than expected from tree size or rooting depth alone.

Response of photosynthesis, growth and water relations of a savannah-adapted tree and grass grown across high to low CO2.

BACKGROUND AND AIMS: By the year 2100, atmospheric CO2 concentration ([CO2]a) could reach 800 ppm, having risen from ~200 ppm since the Neogene, beginning ~24 Myr ago. Changing [CO2]a affects plant carbon-water balance, with implications for growth, drought tolerance and vegetation shifts. The evolution of C4 photosynthesis improved plant hydraulic function under low [CO2]a and preluded the establishment of savannahs, characterized by rapid transitions between open C4-dominated grassland with scattered trees and closed forest. Understanding directional vegetation trends in response to environmental change will require modelling. But models are often parameterized with characteristics observed in plants under current climatic conditions, necessitating experimental quantification of the mechanistic underpinnings of plant acclimation to [CO2]a. METHODS: We measured growth, photosynthesis and plant-water relations, within wetting-drying cycles, of a C3 tree (Vachellia karroo, an acacia) and a C4 grass (Eragrostis curvula) grown at 200, 400 or 800 ppm [CO2]a. We investigated the mechanistic linkages between trait responses to [CO2]a under moderate soil drying, and photosynthetic characteristics. KEY RESULTS: For V. karroo, higher [CO2]a increased assimilation, foliar carbon:nitrogen, biomass and leaf starch, but decreased stomatal conductance and root starch. For Eragrostis, higher [CO2]a decreased C:N, did not affect assimilation, biomass or starch, and markedly decreased stomatal conductance. Together, this meant that C4 advantages in efficient water-use over the tree were maintained with rising [CO2]a. CONCLUSIONS: Acacia and Eragrostis acclimated differently to [CO2]a, with implications for their respective responses to water limitation and environmental change. Our findings question the carbon-centric focus on factors limiting assimilation with changing [CO2]a, how they are predicted and their role in determining productivity. We emphasize the continuing importance of water-conserving strategies in the assimilation response of savannah plants to rising [CO2]a.

Impacts of Atmospheric CO2 and Soil Nutritional Value on Plant Responses to Rhizosphere Colonization by Soil Bacteria.

Concerns over rising atmospheric CO2 concentrations have led to growing interest in the effects of global change on plant-microbe interactions. As a primary substrate of plant metabolism, atmospheric CO2 influences below-ground carbon allocation and root exudation chemistry, potentially affecting rhizosphere interactions with beneficial soil microbes. In this study, we have examined the effects of different atmospheric CO2 concentrations on Arabidopsis rhizosphere colonization by the rhizobacterial strain Pseudomonas simiae WCS417 and the saprophytic strain Pseudomonas putida KT2440. Rhizosphere colonization by saprophytic KT2440 was not influenced by sub-ambient (200 ppm) and elevated (1,200 ppm) concentrations of CO2, irrespective of the carbon (C) and nitrogen (N) content of the soil. Conversely, rhizosphere colonization by WCS417 in soil with relatively low C and N content increased from sub-ambient to elevated CO2. Examination of plant responses to WCS417 revealed that plant growth and systemic resistance varied according to atmospheric CO2 concentration and soil-type, ranging from growth promotion with induced susceptibility at sub-ambient CO2, to growth repression with induced resistance at elevated CO2. Collectively, our results demonstrate that the interaction between atmospheric CO2 and soil nutritional status has a profound impact on plant responses to rhizobacteria. We conclude that predictions about plant performance under past and future climate scenarios depend on interactive plant responses to soil nutritional status and rhizobacteria.

Stomatal and non-stomatal limitations in savanna trees and C4 grasses grown at low, ambient and high atmospheric CO2.

By the end of the century, atmospheric CO2 concentration ([CO2]a) could reach 800 ppm, having risen from ∼200 ppm ∼24 Myr ago. Carbon dioxide enters plant leaves through stomata that limit CO2 diffusion and assimilation, imposing stomatal limitation (LS). Other factors limiting assimilation are collectively called non-stomatal limitations (LNS). C4 photosynthesis concentrates CO2 around Rubisco, typically reducing LS. C4-dominated savanna grasslands expanded under low [CO2]a and are metastable ecosystems where the response of trees and C4 grasses to rising [CO2]a will determine shifting vegetation patterns. How LS and LNS differ between savanna trees and C4 grasses under different [CO2]a will govern the responses of CO2 fixation and plant cover to [CO2]a - but quantitative comparisons are lacking. We measured assimilation, within soil wetting-drying cycles, of three C3 trees and three C4 grasses grown at 200, 400 or 800 ppm [CO2]a. Using assimilation-response curves, we resolved LS and LNS and show that rising [CO2]a alleviated LS, particularly for the C3 trees, but LNS was unaffected and remained substantially higher for the grasses across all [CO2]a treatments. Because LNS incurs higher metabolic costs and recovery compared with LS, our findings indicate that C4 grasses will be comparatively disadvantaged as [CO2]a rises.