A New Angle on How Roots Acclimate to Sporadic Rainfall.

Root architecture critically influences a plant's ability to forage for nutrients and water in soil. In this issue of Cell, Ogura et al. (2019) report a new regulatory gene and elegant molecular mechanism that links auxin-dependent root-angle regulation with improved plant fitness under variable rainfall conditions.

The Soil-Borne Legacy.

Plants greatly rely on their root microbiome for uptake of nutrients and protection against stresses. Recent studies have uncovered the involvement of plant stress responses in the assembly of plant-beneficial microbiomes. To facilitate durable crop production, deciphering the driving forces that shape the microbiome is crucial.

Developmental Responses to Water and Salinity in Root Systems.

Roots provide the primary mechanism that plants use to absorb water and nutrients from their environment. These functions are dependent on developmental mechanisms that direct root growth and branching into regions of soil where these resources are relatively abundant. Water is the most limiting factor for plant growth, and its availability is determined by the weather, soil structure, and salinity. In this review, we define the developmental pathways that regulate the direction of growth and branching pattern of the root system, which together determine the expanse of soil from which a plant can access water. The ability of plants to regulate development in response to the spatial distribution of water is a focus of many recent studies and provides a model for understanding how biological systems utilize positional cues to affect signaling and morphogenesis. A better understanding of these processes will inform approaches to improve crop water use efficiency to more sustainably feed a growing population.

The lung fibroblast as "soil fertilizer" in breast cancer metastasis.

Fibroblasts strongly impact tumor progression, but whether they prime the pre-metastatic niche is poorly understood. In this issue of Immunity, Gong and Li et al. identify lung-specific immunosuppressive fibroblasts, which are hijacked by breast cancer cells to facilitate metastasis.

A unified explanation for the morphology of raised peatlands.

Raised peatlands, or bogs, are gently mounded landforms that are composed entirely of organic matter1-4 and store the most carbon per area of any terrestrial ecosystem5. The shapes of bogs are critically important because their domed morphology4,6,7 accounts for much of the carbon that bogs store and determines how they will respond to interventions8,9 to stop greenhouse gas emissions and fires after anthropogenic drainage10-13. However, a general theory to infer the morphology of bogs is still lacking4,6,7. Here we show that an equation based on the processes universal to bogs explains their morphology across biomes, from Alaska, through the tropics, to New Zealand. In contrast to earlier models of bog morphology that attempted to describe only long-term equilibrium shapes4,6,7 and were, therefore, inapplicable to most bogs14-16, our approach makes no such assumption and makes it possible to infer full shapes of bogs from a sample of elevations, such as a single elevation transect. Our findings provide a foundation for quantitative inference about the morphology, hydrology and carbon storage of bogs through Earth's history, as well as a basis for planning natural climate solutions by rewetting damaged bogs around the world.

Amazon forest biogeography predicts resilience and vulnerability to drought.

Amazonia contains the most extensive tropical forests on Earth, but Amazon carbon sinks of atmospheric CO2 are declining, as deforestation and climate-change-associated droughts1-4 threaten to push these forests past a tipping point towards collapse5-8. Forests exhibit complex drought responses, indicating both resilience (photosynthetic greening) and vulnerability (browning and tree mortality), that are difficult to explain by climate variation alone9-17. Here we combine remotely sensed photosynthetic indices with ground-measured tree demography to identify mechanisms underlying drought resilience/vulnerability in different intact forest ecotopes18,19 (defined by water-table depth, soil fertility and texture, and vegetation characteristics). In higher-fertility southern Amazonia, drought response was structured by water-table depth, with resilient greening in shallow-water-table forests (where greater water availability heightened response to excess sunlight), contrasting with vulnerability (browning and excess tree mortality) over deeper water tables. Notably, the resilience of shallow-water-table forest weakened as drought lengthened. By contrast, lower-fertility northern Amazonia, with slower-growing but hardier trees (or, alternatively, tall forests, with deep-rooted water access), supported more-drought-resilient forests independent of water-table depth. This functional biogeography of drought response provides a framework for conservation decisions and improved predictions of heterogeneous forest responses to future climate changes, warning that Amazonia's most productive forests are also at greatest risk, and that longer/more frequent droughts are undermining multiple ecohydrological strategies and capacities for Amazon forest resilience.

Unlocking bacterial potential to reduce farmland N2O emissions.

Farmed soils contribute substantially to global warming by emitting N2O (ref. 1), and mitigation has proved difficult2. Several microbial nitrogen transformations produce N2O, but the only biological sink for N2O is the enzyme NosZ, catalysing the reduction of N2O to N2 (ref. 3). Although strengthening the NosZ activity in soils would reduce N2O emissions, such bioengineering of the soil microbiota is considered challenging4,5. However, we have developed a technology to achieve this, using organic waste as a substrate and vector for N2O-respiring bacteria selected for their capacity to thrive in soil6-8. Here we have analysed the biokinetics of N2O reduction by our most promising N2O-respiring bacterium, Cloacibacterium sp. CB-01, its survival in soil and its effect on N2O emissions in field experiments. Fertilization with waste from biogas production, in which CB-01 had grown aerobically to about 6 × 109 cells per millilitre, reduced N2O emissions by 50-95%, depending on soil type. The strong and long-lasting effect of CB-01 is ascribed to its tenacity in soil, rather than its biokinetic parameters, which were inferior to those of other strains of N2O-respiring bacteria. Scaling our data up to the European level, we find that national anthropogenic N2O emissions could be reduced by 5-20%, and more if including other organic wastes. This opens an avenue for cost-effective reduction of N2O emissions for which other mitigation options are lacking at present.

Microbial competition for phosphorus limits the CO2 response of a mature forest.

The capacity for terrestrial ecosystems to sequester additional carbon (C) with rising CO2 concentrations depends on soil nutrient availability1,2. Previous evidence suggested that mature forests growing on phosphorus (P)-deprived soils had limited capacity to sequester extra biomass under elevated CO2 (refs. 3-6), but uncertainty about ecosystem P cycling and its CO2 response represents a crucial bottleneck for mechanistic prediction of the land C sink under climate change7. Here, by compiling the first comprehensive P budget for a P-limited mature forest exposed to elevated CO2, we show a high likelihood that P captured by soil microorganisms constrains ecosystem P recycling and availability for plant uptake. Trees used P efficiently, but microbial pre-emption of mineralized soil P seemed to limit the capacity of trees for increased P uptake and assimilation under elevated CO2 and, therefore, their capacity to sequester extra C. Plant strategies to stimulate microbial P cycling and plant P uptake, such as increasing rhizosphere C release to soil, will probably be necessary for P-limited forests to increase C capture into new biomass. Our results identify the key mechanisms by which P availability limits CO2 fertilization of tree growth and will guide the development of Earth system models to predict future long-term C storage.

An engineered enzyme embedded into PLA to make self-biodegradable plastic.

Plastic production reached 400 million tons in 2022 (ref. 1), with packaging and single-use plastics accounting for a substantial amount of this2. The resulting waste ends up in landfills, incineration or the environment, contributing to environmental pollution3. Shifting to biodegradable and compostable plastics is increasingly being considered as an efficient waste-management alternative4. Although polylactide (PLA) is the most widely used biosourced polymer5, its biodegradation rate under home-compost and soil conditions remains low6-8. Here we present a PLA-based plastic in which an optimized enzyme is embedded to ensure rapid biodegradation and compostability at room temperature, using a scalable industrial process. First, an 80-fold activity enhancement was achieved through structure-based rational engineering of a new hyperthermostable PLA hydrolase. Second, the enzyme was uniformly dispersed within the PLA matrix by means of a masterbatch-based melt extrusion process. The liquid enzyme formulation was incorporated in polycaprolactone, a low-melting-temperature polymer, through melt extrusion at 70 °C, forming an 'enzymated' polycaprolactone masterbatch. Masterbatch pellets were integrated into PLA by melt extrusion at 160 °C, producing an enzymated PLA film (0.02% w/w enzyme) that fully disintegrated under home-compost conditions within 20-24 weeks, meeting home-composting standards. The mechanical and degradation properties of the enzymated film were compatible with industrial packaging applications, and they remained intact during long-term storage. This innovative material not only opens new avenues for composters and biomethane production but also provides a feasible industrial solution for PLA degradation.

Environmental drivers of increased ecosystem respiration in a warming tundra.

Arctic and alpine tundra ecosystems are large reservoirs of organic carbon1,2. Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere3,4. The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain5-7. This hampers the accuracy of global land carbon-climate feedback projections7,8. Here we synthesize 136 datasets from 56 open-top chamber in situ warming experiments located at 28 arctic and alpine tundra sites which have been running for less than 1 year up to 25 years. We show that a mean rise of 1.4 °C [confidence interval (CI) 0.9-2.0 °C] in air and 0.4 °C [CI 0.2-0.7 °C] in soil temperature results in an increase in growing season ecosystem respiration by 30% [CI 22-38%] (n = 136). Our findings indicate that the stimulation of ecosystem respiration was due to increases in both plant-related and microbial respiration (n = 9) and continued for at least 25 years (n = 136). The magnitude of the warming effects on respiration was driven by variation in warming-induced changes in local soil conditions, that is, changes in total nitrogen concentration and pH and by context-dependent spatial variation in these conditions, in particular total nitrogen concentration and the carbon:nitrogen ratio. Tundra sites with stronger nitrogen limitations and sites in which warming had stimulated plant and microbial nutrient turnover seemed particularly sensitive in their respiration response to warming. The results highlight the importance of local soil conditions and warming-induced changes therein for future climatic impacts on respiration.

Fertilizer management for global ammonia emission reduction.

Crop production is a large source of atmospheric ammonia (NH3), which poses risks to air quality, human health and ecosystems1-5. However, estimating global NH3 emissions from croplands is subject to uncertainties because of data limitations, thereby limiting the accurate identification of mitigation options and efficacy4,5. Here we develop a machine learning model for generating crop-specific and spatially explicit NH3 emission factors globally (5-arcmin resolution) based on a compiled dataset of field observations. We show that global NH3 emissions from rice, wheat and maize fields in 2018 were 4.3 ± 1.0 Tg N yr-1, lower than previous estimates that did not fully consider fertilizer management practices6-9. Furthermore, spatially optimizing fertilizer management, as guided by the machine learning model, has the potential to reduce the NH3 emissions by about 38% (1.6 ± 0.4 Tg N yr-1) without altering total fertilizer nitrogen inputs. Specifically, we estimate potential NH3 emissions reductions of 47% (44-56%) for rice, 27% (24-28%) for maize and 26% (20-28%) for wheat cultivation, respectively. Under future climate change scenarios, we estimate that NH3 emissions could increase by 4.0 ± 2.7% under SSP1-2.6 and 5.5 ± 5.7% under SSP5-8.5 by 2030-2060. However, targeted fertilizer management has the potential to mitigate these increases.

Rainforest transformation reallocates energy from green to brown food webs.

Terrestrial animal biodiversity is increasingly being lost because of land-use change1,2. However, functional and energetic consequences aboveground and belowground and across trophic levels in megadiverse tropical ecosystems remain largely unknown. To fill this gap, we assessed changes in energy fluxes across 'green' aboveground (canopy arthropods and birds) and 'brown' belowground (soil arthropods and earthworms) animal food webs in tropical rainforests and plantations in Sumatra, Indonesia. Our results showed that most of the energy in rainforests is channelled to the belowground animal food web. Oil palm and rubber plantations had similar or, in the case of rubber agroforest, higher total animal energy fluxes compared to rainforest but the key energetic nodes were distinctly different: in rainforest more than 90% of the total animal energy flux was channelled by arthropods in soil and canopy, whereas in plantations more than 50% of the energy was allocated to annelids (earthworms). Land-use change led to a consistent decline in multitrophic energy flux aboveground, whereas belowground food webs responded with reduced energy flux to higher trophic levels, down to -90%, and with shifts from slow (fungal) to fast (bacterial) energy channels and from faeces production towards consumption of soil organic matter. This coincides with previously reported soil carbon stock depletion3. Here we show that well-documented animal biodiversity declines with tropical land-use change4-6 are associated with vast energetic and functional restructuring in food webs across aboveground and belowground ecosystem compartments.

The development of terrestrial ecosystems emerging after glacier retreat.

The global retreat of glaciers is dramatically altering mountain and high-latitude landscapes, with new ecosystems developing from apparently barren substrates1-4. The study of these emerging ecosystems is critical to understanding how climate change interacts with microhabitat and biotic communities and determines the future of ice-free terrains1,5. Here, using a comprehensive characterization of ecosystems (soil properties, microclimate, productivity and biodiversity by environmental DNA metabarcoding6) across 46 proglacial landscapes worldwide, we found that all the environmental properties change with time since glaciers retreated, and that temperature modulates the accumulation of soil nutrients. The richness of bacteria, fungi, plants and animals increases with time since deglaciation, but their temporal patterns differ. Microorganisms colonized most rapidly in the first decades after glacier retreat, whereas most macroorganisms took longer. Increased habitat suitability, growing complexity of biotic interactions and temporal colonization all contribute to the increase in biodiversity over time. These processes also modify community composition for all the groups of organisms. Plant communities show positive links with all other biodiversity components and have a key role in ecosystem development. These unifying patterns provide new insights into the early dynamics of deglaciated terrains and highlight the need for integrated surveillance of their multiple environmental properties5.

Tree diversity increases decadal forest soil carbon and nitrogen accrual.

Increasing soil carbon and nitrogen storage can help mitigate climate change and sustain soil fertility1,2. A large number of biodiversity-manipulation experiments collectively suggest that high plant diversity increases soil carbon and nitrogen stocks3,4. It remains debated, however, whether such conclusions hold in natural ecosystems5-12. Here we analyse Canada's National Forest Inventory (NFI) database with the help of structural equation modelling (SEM) to explore the relationship between tree diversity and soil carbon and nitrogen accumulation in natural forests. We find that greater tree diversity is associated with higher soil carbon and nitrogen accumulation, validating inferences from biodiversity-manipulation experiments. Specifically, on a decadal scale, increasing species evenness from its minimum to maximum value increases soil carbon and nitrogen in the organic horizon by 30% and 42%, whereas increasing functional diversity enhances soil carbon and nitrogen in the mineral horizon by 32% and 50%, respectively. Our results highlight that conserving and promoting functionally diverse forests could promote soil carbon and nitrogen storage, enhancing both carbon sink capacity and soil nitrogen fertility.

Microbial carbon use efficiency promotes global soil carbon storage.

Soils store more carbon than other terrestrial ecosystems1,2. How soil organic carbon (SOC) forms and persists remains uncertain1,3, which makes it challenging to understand how it will respond to climatic change3,4. It has been suggested that soil microorganisms play an important role in SOC formation, preservation and loss5-7. Although microorganisms affect the accumulation and loss of soil organic matter through many pathways4,6,8-11, microbial carbon use efficiency (CUE) is an integrative metric that can capture the balance of these processes12,13. Although CUE has the potential to act as a predictor of variation in SOC storage, the role of CUE in SOC persistence remains unresolved7,14,15. Here we examine the relationship between CUE and the preservation of SOC, and interactions with climate, vegetation and edaphic properties, using a combination of global-scale datasets, a microbial-process explicit model, data assimilation, deep learning and meta-analysis. We find that CUE is at least four times as important as other evaluated factors, such as carbon input, decomposition or vertical transport, in determining SOC storage and its spatial variation across the globe. In addition, CUE shows a positive correlation with SOC content. Our findings point to microbial CUE as a major determinant of global SOC storage. Understanding the microbial processes underlying CUE and their environmental dependence may help the prediction of SOC feedback to a changing climate.

Net greenhouse gas balance of fibre wood plantation on peat in Indonesia.

Tropical peatlands cycle and store large amounts of carbon in their soil and biomass1-5. Climate and land-use change alters greenhouse gas (GHG) fluxes of tropical peatlands, but the magnitude of these changes remains highly uncertain6-19. Here we measure net ecosystem exchanges of carbon dioxide, methane and soil nitrous oxide fluxes between October 2016 and May 2022 from Acacia crassicarpa plantation, degraded forest and intact forest within the same peat landscape, representing land-cover-change trajectories in Sumatra, Indonesia. This allows us to present a full plantation rotation GHG flux balance in a fibre wood plantation on peatland. We find that the Acacia plantation has lower GHG emissions than the degraded site with a similar average groundwater level (GWL), despite more intensive land use. The GHG emissions from the Acacia plantation over a full plantation rotation (35.2 ± 4.7 tCO2-eq ha-1 year-1, average ± standard deviation) were around two times higher than those from the intact forest (20.3 ± 3.7 tCO2-eq ha-1 year-1), but only half of the current Intergovernmental Panel on Climate Change (IPCC) Tier 1 emission factor (EF)20 for this land use. Our results can help to reduce the uncertainty in GHG emissions estimates, provide an estimate of the impact of land-use change on tropical peat and develop science-based peatland management practices as nature-based climate solutions.

Cost-effective mitigation of nitrogen pollution from global croplands.

Cropland is a main source of global nitrogen pollution1,2. Mitigating nitrogen pollution from global croplands is a grand challenge because of the nature of non-point-source pollution from millions of farms and the constraints to implementing pollution-reduction measures, such as lack of financial resources and limited nitrogen-management knowledge of farmers3. Here we synthesize 1,521 field observations worldwide and identify 11 key measures that can reduce nitrogen losses from croplands to air and water by 30-70%, while increasing crop yield and nitrogen use efficiency (NUE) by 10-30% and 10-80%, respectively. Overall, adoption of this package of measures on global croplands would allow the production of 17 ± 3 Tg (1012 g) more crop nitrogen (20% increase) with 22 ± 4 Tg less nitrogen fertilizer used (21% reduction) and 26 ± 5 Tg less nitrogen pollution (32% reduction) to the environment for the considered base year of 2015. These changes could gain a global societal benefit of 476 ± 123 billion US dollars (USD) for food supply, human health, ecosystems and climate, with net mitigation costs of only 19 ± 5 billion USD, of which 15 ± 4 billion USD fertilizer saving offsets 44% of the gross mitigation cost. To mitigate nitrogen pollution from croplands in the future, innovative policies such as a nitrogen credit system (NCS) could be implemented to select, incentivize and, where necessary, subsidize the adoption of these measures.

Agricultural pesticide land budget and river discharge to oceans.

Pesticides are ubiquitous environmental pollutants negatively affecting ecosystem and human health1,2. About 3 Tg of pesticides are used annually in agriculture to protect crops3. How much of these pesticides remain on land and reach the aquifer or the ocean is uncertain. Monitoring their environmental fate is challenging, and a detailed picture of their mobility in time and space is largely missing4. Here, we develop a process-based model accounting for the hydrology and biogeochemistry of the 92 most used agricultural pesticide active substances to assess their pathways through the principal catchments of the world and draw a near-present picture of the global land and river budgets, including discharge to oceans. Of the 0.94 Tg net annual pesticide input in 2015 used in this study, 82% is biologically degraded, 10% remains as residue in soil and 7.2% leaches below the root zone. Rivers receive 0.73 Gg of pesticides from their drainage at a rate of 10 to more than 100 kg yr-1 km-1. By contrast to their fate in soil, only 1.1% of pesticides entering rivers are degraded along streams, exceeding safety levels (concentrations >1 µg l-1) in more than 13,000 km of river length, with 0.71 Gg of pesticide active ingredients released to oceans every year. Herbicides represent the prevalent pesticide residue on both land (72%) and river outlets (62%).

Autonomous self-burying seed carriers for aerial seeding.

Aerial seeding can quickly cover large and physically inaccessible areas1 to improve soil quality and scavenge residual nitrogen in agriculture2, and for postfire reforestation3-5 and wildland restoration6,7. However, it suffers from low germination rates, due to the direct exposure of unburied seeds to harsh sunlight, wind and granivorous birds, as well as undesirable air humidity and temperature1,8,9. Here, inspired by Erodium seeds10-14, we design and fabricate self-drilling seed carriers, turning wood veneer into highly stiff (about 4.9 GPa when dry, and about 1.3 GPa when wet) and hygromorphic bending or coiling actuators with an extremely large bending curvature (1,854 m-1), 45 times larger than the values in the literature15-18. Our three-tailed carrier has an 80% drilling success rate on flat land after two triggering cycles, due to the beneficial resting angle (25°-30°) of its tail anchoring, whereas the natural Erodium seed's success rate is 0%. Our carriers can carry payloads of various sizes and contents including biofertilizers and plant seeds as large as those of whitebark pine, which are about 11 mm in length and about 72 mg. We compare data from experiments and numerical simulation to elucidate the curvature transformation and actuation mechanisms to guide the design and optimization of the seed carriers. Our system will improve the effectiveness of aerial seeding to relieve agricultural and environmental stresses, and has potential applications in energy harvesting, soft robotics and sustainable buildings.

Landscape dynamics and the Phanerozoic diversification of the biosphere.

The long-term diversification of the biosphere responds to changes in the physical environment. Yet, over the continents, the nearly monotonic expansion of life started later in the early part of the Phanerozoic eon1 than the expansion in the marine realm, where instead the number of genera waxed and waned over time2. A comprehensive evaluation of the changes in the geodynamic and climatic forcing fails to provide a unified theory for the long-term pattern of evolution of life on Earth. Here we couple climate and plate tectonics models to numerically reconstruct the evolution of the Earth's landscape over the entire Phanerozoic eon, which we then compare to palaeo-diversity datasets from marine animal and land plant genera. Our results indicate that biodiversity is strongly reliant on landscape dynamics, which at all times determine the carrying capacity of both the continental domain and the oceanic domain. In the oceans, diversity closely adjusted to the riverine sedimentary flux that provides nutrients for primary production. On land, plant expansion was hampered by poor edaphic conditions until widespread endorheic basins resurfaced continents with a sedimentary cover that facilitated the development of soil-dependent rooted flora, and the increasing variety of the landscape additionally promoted their development.