Soil carbon loss by experimental warming in a tropical forest.

Tropical soils contain one-third of the carbon stored in soils globally1, so destabilization of soil organic matter caused by the warming predicted for tropical regions this century2 could accelerate climate change by releasing additional carbon dioxide (CO2) to the atmosphere3-6. Theory predicts that warming should cause only modest carbon loss from tropical soils relative to those at higher latitudes5,7, but there have been no warming experiments in tropical forests to test this8. Here we show that in situ experimental warming of a lowland tropical forest soil on Barro Colorado Island, Panama, caused an unexpectedly large increase in soil CO2 emissions. Two years of warming of the whole soil profile by four degrees Celsius increased CO2 emissions by 55 per cent compared to soils at ambient temperature. The additional CO2 originated from heterotrophic rather than autotrophic sources, and equated to a loss of 8.2 ± 4.2 (one standard error) tonnes of carbon per hectare per year from the breakdown of soil organic matter. During this time, we detected no acclimation of respiration rates, no thermal compensation or change in the temperature sensitivity of enzyme activities, and no change in microbial carbon-use efficiency. These results demonstrate that soil carbon in tropical forests is highly sensitive to warming, creating a potentially substantial positive feedback to climate change.

Author Correction: Soil carbon loss by experimental warming in a tropical forest.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

New cyclophilin D inhibitor rescues mitochondrial and cognitive function in Alzheimer's disease.

Mitochondrial dysfunction is an early pathological feature of Alzheimer disease and plays a crucial role in the development and progression of Alzheimer's disease. Strategies to rescue mitochondrial function and cognition remain to be explored. Cyclophilin D (CypD), the peptidylprolyl isomerase F (PPIase), is a key component in opening the mitochondrial membrane permeability transition pore, leading to mitochondrial dysfunction and cell death. Blocking membrane permeability transition pore opening by inhibiting CypD activity is a promising therapeutic approach for Alzheimer's disease. However, there is currently no effective CypD inhibitor for Alzheimer's disease, with previous candidates demonstrating high toxicity, poor ability to cross the blood-brain barrier, compromised biocompatibility and low selectivity. Here, we report a new class of non-toxic and biocompatible CypD inhibitor, ebselen, using a conventional PPIase assay to screen a library of ∼2000 FDA-approved drugs with crystallographic analysis of the CypD-ebselen crystal structure (PDB code: 8EJX). More importantly, we assessed the effects of genetic and pharmacological blockade of CypD on Alzheimer's disease mitochondrial and glycolytic bioenergetics in Alzheimer's disease-derived mitochondrial cybrid cells, an ex vivo human sporadic Alzheimer's disease mitochondrial model, and on synaptic function, inflammatory response and learning and memory in Alzheimer's disease mouse models. Inhibition of CypD by ebselen protects against sporadic Alzheimer's disease- and amyloid-ß-induced mitochondrial and glycolytic perturbation, synaptic and cognitive dysfunction, together with suppressing neuroinflammation in the brain of Alzheimer's disease mouse models, which is linked to CypD-related membrane permeability transition pore formation. Thus, CypD inhibitors have the potential to slow the progression of neurodegenerative diseases, including Alzheimer's disease, by boosting mitochondrial bioenergetics and improving synaptic and cognitive function.

Pervasive phosphorus limitation of tree species but not communities in tropical forests.

Phosphorus availability is widely assumed to limit primary productivity in tropical forests, but support for this paradigm is equivocal. Although biogeochemical theory predicts that phosphorus limitation should be prevalent on old, strongly weathered soils, experimental manipulations have failed to detect a consistent response to phosphorus addition in species-rich lowland tropical forests. Here we show, by quantifying the growth of 541 tropical tree species across a steep natural phosphorus gradient in Panama, that phosphorus limitation is widespread at the level of individual species and strengthens markedly below a threshold of two parts per million exchangeable soil phosphate. However, this pervasive species-specific phosphorus limitation does not translate into a community-wide response, because some species grow rapidly on infertile soils despite extremely low phosphorus availability. These results redefine our understanding of nutrient limitation in diverse plant communities and have important implications for attempts to predict the response of tropical forests to environmental change.

Publisher Correction: Pervasive phosphorus limitation of tree species but not communities in tropical forests.

In this Letter, the y axis of the right-hand panel of Fig. 2a was mislabelled 'Phosphomonoesterase' instead of 'Phosphodiesterase'. This error has been corrected online.

Nitrogen deposition accelerates soil carbon sequestration in tropical forests.

Terrestrial ecosystem carbon (C) sequestration plays an important role in ameliorating global climate change. While tropical forests exert a disproportionately large influence on global C cycling, there remains an open question on changes in below-ground soil C stocks with global increases in nitrogen (N) deposition, because N supply often does not constrain the growth of tropical forests. We quantified soil C sequestration through more than a decade of continuous N addition experiment in an N-rich primary tropical forest. Results showed that long-term N additions increased soil C stocks by 7 to 21%, mainly arising from decreased C output fluxes and physical protection mechanisms without changes in the chemical composition of organic matter. A meta-analysis further verified that soil C sequestration induced by excess N inputs is a general phenomenon in tropical forests. Notably, soil N sequestration can keep pace with soil C, based on consistent C/N ratios under N additions. These findings provide empirical evidence that below-ground C sequestration can be stimulated in mature tropical forests under excess N deposition, which has important implications for predicting future terrestrial sinks for both elevated anthropogenic CO2 and N deposition. We further developed a conceptual model hypothesis depicting how soil C sequestration happens under chronic N deposition in N-limited and N-rich ecosystems, suggesting a direction to incorporate N deposition and N cycling into terrestrial C cycle models to improve the predictability on C sink strength as enhanced N deposition spreads from temperate into tropical systems.

Widespread frontoparietal fMRI activity is greatly affected by changes in criterion placement, not discriminability, during recognition memory and visual detection tests.

Widespread frontoparietal activity is consistently observed in recognition memory tests that compare studied ("target") versus unstudied ("nontarget") responses. However, there are conflicting accounts that ascribe various aspects of frontoparietal activity to mnemonic evidence versus decisional processes. According to Signal Detection Theory, recognition judgments require individuals to decide whether the memory strength of an item exceeds an evidence threshold-the decision criterion-for reporting previously studied items. Yet, most fMRI studies fail to manipulate both memory strength and decision criteria, making it difficult to appropriately identify frontoparietal activity associated with each process. In the current experiment, we manipulated both discriminability and decision criteria across recognition memory and visual detection tests during fMRI scanning to assess how frontoparietal activity is affected by each manipulation. Our findings revealed that maintaining a conservative versus liberal decision criterion drastically affects frontoparietal activity in target versus nontarget response contrasts for both recognition memory and visual detection tests. However, manipulations of discriminability showed virtually no differences in frontoparietal activity in target versus nontarget response or item contrasts. Comparing across task domains, we observed similar modulations of frontoparietal activity across criterion conditions, though the recognition memory task revealed larger activations in both magnitude and spatial extent in these contrasts. Nonetheless, there appears to be some domain specificity in frontoparietal activity associated with the maintenance of a conservative versus liberal criterion. We propose that widespread frontoparietal activity observed in target versus nontarget contrasts is largely attributable to response bias where increased activity may reflect inhibition of a prepotent response, which differs depending on whether a person maintains a conservative versus liberal decision criterion.

Breakdown of the growth-mortality trade-off along a soil phosphorus gradient in a diverse tropical forest.

An ecological paradigm predicts that plant species adapted to low resource availability grow slower and live longer than those adapted to high resource availability when growing together. We tested this by using hierarchical Bayesian analysis to quantify variations in growth and mortality of ca 40 000 individual trees from greater than 400 species in response to limiting resources in the tropical forests of Panama. In contrast to theoretical expectations of the growth-mortality paradigm, we find that tropical tree species restricted to low-phosphorus soils simultaneously achieve faster growth rates and lower mortality rates than species restricted to high-phosphorus soils. This result demonstrates that adaptation to phosphorus limitation in diverse plant communities modifies the growth-mortality trade-off, with important implications for understanding long-term ecosystem dynamics.

Structural mechanism of laforin function in glycogen dephosphorylation and lafora disease.

Glycogen is the major mammalian glucose storage cache and is critical for energy homeostasis. Glycogen synthesis in neurons must be tightly controlled due to neuronal sensitivity to perturbations in glycogen metabolism. Lafora disease (LD) is a fatal, congenital, neurodegenerative epilepsy. Mutations in the gene encoding the glycogen phosphatase laforin result in hyperphosphorylated glycogen that forms water-insoluble inclusions called Lafora bodies (LBs). LBs induce neuronal apoptosis and are the causative agent of LD. The mechanism of glycogen dephosphorylation by laforin and dysfunction in LD is unknown. We report the crystal structure of laforin bound to phosphoglucan product, revealing its unique integrated tertiary and quaternary structure. Structure-guided mutagenesis combined with biophysical and biochemical analyses reveal the basis for normal function of laforin in glycogen metabolism. Analyses of LD patient mutations define the mechanism by which subsets of mutations disrupt laforin function. These data provide fundamental insights connecting glycogen metabolism to neurodegenerative disease.

Enhancing Phytate Availability in Soils and Phytate-P Acquisition by Plants: A Review.

Phytate (myo-inositol hexakisphosphate salts) can constitute a large fraction of the organic P in soils. As a more recalcitrant form of soil organic P, up to 51 million metric tons of phytate accumulate in soils annually, corresponding to ∼65% of the P fertilizer application. However, the availability of phytate is limited due to its strong binding to soils via its highly-phosphorylated inositol structure, with sorption capacity being ∼4 times that of orthophosphate in soils. Phosphorus (P) is one of the most limiting macronutrients for agricultural productivity. Given that phosphate rock is a finite resource, coupled with the increasing difficulty in its extraction and geopolitical fragility in supply, it is anticipated that both economic and environmental costs of P fertilizer will greatly increase. Therefore, optimizing the use of soil phytate-P can potentially enhance the economic and environmental sustainability of agriculture production. To increase phytate-P availability in the rhizosphere, plants and microbes have developed strategies to improve phytate solubility and mineralization by secreting mobilizing agents including organic acids and hydrolyzing enzymes including various phytases. Though we have some understanding of phytate availability and phytase activity in soils, the limiting steps for phytate-P acquisition by plants proposed two decades ago remain elusive. Besides, the relative contribution of plant- and microbe-derived phytases, including those from mycorrhizas, in improving phytate-P utilization is poorly understood. Hence, it is important to understand the processes that influence phytate-P acquisition by plants, thereby developing effective molecular biotechnologies to enhance the dynamics of phytate in soil. However, from a practical view, phytate-P acquisition by plants competes with soil P fixation, so the ability of plants to access stable phytate must be evaluated from both a plant and soil perspective. Here, we summarize information on phytate availability in soils and phytate-P acquisition by plants. In addition, agronomic approaches and biotechnological strategies to improve soil phytate-P utilization by plants are discussed, and questions that need further investigation are raised. The information helps to better improve phytate-P utilization by plants, thereby reducing P resource inputs and pollution risks to the wider environment.

Demographic consequences of foraging ecology explain genetic diversification in Neotropical bird species.

Despite evidence that species' traits affect rates of bird diversification, biogeographic studies tend to prioritise earth history in Neotropical bird speciation. Here we compare mitochondrial genetic differentiation among 56 co-distributed Neotropical bird species with varying ecologies. The trait 'diet' best predicted divergence, with plant-dependent species (mostly frugivores and nectivores) showing lower levels of genetic divergence than insectivores or mixed-diet species. We propose that the greater vagility and demographic instability of birds whose diets rely on fruit, seeds, or nectar  known to vary in abundance seasonally and between years  relative to birds that eat primarily insects, drives episodic re-unification of otherwise isolated populations, resetting the divergence 'clock'. Testing this prediction using coalescent simulations, we find that plant-dependent species show stronger signals of recent demographic expansion compared to insectivores or mixed-diet species, consistent with this hypothesis. Our study provides evidence that localised ecological phenomena scale up to generate larger macroevolutionary patterns.

A shift from phenol to silica-based leaf defences during long-term soil and ecosystem development.

The resource availability hypothesis predicts that plants adapted to infertile soils have high levels of anti-herbivore leaf defences. This hypothesis has been mostly explored for secondary metabolites such as phenolics, whereas it remains underexplored for silica-based defences. We determined leaf concentrations of total phenols and silicon (Si) in plants growing along the 2-million-year Jurien Bay chronosequence, exhibiting an extreme gradient of soil fertility. We found that nitrogen (N) limitation on young soils led to a greater expression of phenol-based defences, whereas old, phosphorus (P)-impoverished soils favoured silica-based defences. Both defence types were negatively correlated at the community and individual species level. Our results suggest a trade-off among these two leaf defence strategies based on the strength and type of nutrient limitation, thereby opening up new perspectives for the resource availability hypothesis and plant defence research. This study also highlights the importance of silica-based defences under low P supply.

Temperate Forests Dominated by Arbuscular or Ectomycorrhizal Fungi Are Characterized by Strong Shifts from Saprotrophic to Mycorrhizal Fungi with Increasing Soil Depth.

In temperate and boreal forests, competition for soil resources between free-living saprotrophs and ectomycorrhizal (EcM) fungi has been suggested to restrict saprotrophic fungal dominance to the most superficial organic soil horizons in forests dominated by EcM trees. By contrast, lower niche overlap with arbuscular mycorrhizal (AM) fungi could allow fungal saprotrophs to maintain this dominance into deeper soil horizons in AM-dominated forests. Here we used a natural gradient of adjacent forest patches that were dominated by either AM or EcM trees, or a mixture of both to determine how fungal communities characterized with high-throughput amplicon sequencing change across organic and mineral soil horizons. We found a general shift from saprotrophic to mycorrhizal fungal dominance with increasing soil depth in all forest mycorrhizal types, especially in organic horizons. Vertical changes in soil chemistry, including pH, organic matter, exchangeable cations, and extractable phosphorus, coincided with shifts in fungal community composition. Although fungal communities and soil chemistry differed among adjacent forest mycorrhizal types, variations were stronger within a given soil profile, pointing to the importance of considering horizons when characterizing soil fungal communities. Our results also suggest that in temperate forests, vertical shifts from saprotrophic to mycorrhizal fungi within organic and mineral horizons occur similarly in both ectomycorrhizal and arbuscular mycorrhizal forests.

Methane emissions from tree stems in neotropical peatlands.

Neotropical peatlands emit large amounts of methane (CH4 ) from the soil surface, but fluxes from tree stems in these ecosystems are unknown. In this study we investigated CH4 emissions from five tree species in two forest types common to neotropical lowland peatlands in Panama. Methane from tree stems accounted for up to 30% of net ecosystem CH4 emissions. Peak CH4 fluxes were greater during the wet season when the water table was high and temperatures were lower. Emissions were greatest from the hardwood tree Campnosperma panamensis, but most species acted as emitters, with emissions declining exponentially with height along the stem for all species. Overall, species identity, stem diameter, water level, soil temperature and soil CH4 fluxes explained 54% of the variance in stem CH4 emissions from individual trees. On the landscape level, On the landscape level, the high emissions from C. panamensis forests resulted in that they emitted at 340 kg CH4  d-1 during flooded periods despite their substantially lower areal cover. We conclude that emission from tree stems is an important emission pathway for CH4 flux from Neotropical peatlands, and that these emissions vary strongly with season and forest type.

A rapid ammonium fluoride method to determine the oxygen isotope ratio of available phosphorus in tropical soils.

RATIONALE: The isotopic composition of oxygen bound to phosphorus (δ18 OP value) offers an opportunity to gain insight into P cycling mechanisms. However, there is little information for tropical forest soils, which presents a challenge for δ18 OP measurements due to low available P concentrations. Here we report the use of a rapid ammonium fluoride extraction method (Bray-1) as an alternative to the widely used anion-exchange membrane (AEM) method for quantification of δ18 OP values of available P in tropical forest soils. METHODS: We compared P concentrations and δ18 OP values of available and microbial P determined by AEM and Bray-1 extraction for a series of tropical forest soils from Panama spanning a steep P gradient. This involved an assessment of the influence of extraction conditions, including temperature, extraction time, fumigation time and solution-to-soil ratio, on P concentrations and isotope ratios. RESULTS: Depending on the extraction conditions, Bray-1 P concentrations ranged from 0.2 to 66.3 mg P kg-1 across the soils. Extraction time and temperature had only minor effects on Bray-1 P, but concentrations increased markedly as the solution-to-soil ratio increased. In contrast, extraction conditions did not affect Bray-1 δ18 OP values, indicating that Bray-1 provides a robust measure of the isotopic composition of available soil P. For a relatively high P soil, available and fumigation-released (microbial) δ18 OP values determined by Bray-1 extraction (20‰ and 16‰, respectively) were higher than those determined by the AEM method (18‰ and 12‰, respectively), which we attribute to slightly different P pools extracted by the two methods and/or differences resulting from the longer extraction time needed for the AEM method. CONCLUSIONS: The short extraction time, insensitivity to extraction conditions and smaller mass of soil required to extract sufficient P for isotopic analysis make Bray-1extraction a suitable alternative to the AEM method for the determination of δ18 OP values of available P in tropical soils.

Co-occurring Fungal Functional Groups Respond Differently to Tree Neighborhoods and Soil Properties Across Three Tropical Rainforests in Panama.

Abiotic and biotic drivers of co-occurring fungal functional guilds across regional-scale environmental gradients remain poorly understood. We characterized fungal communities using Illumina sequencing from soil cores collected across three Neotropical rainforests in Panama that vary in soil properties and plant community composition. We classified each fungal OTU into different functional guilds, namely plant pathogens, saprotrophs, arbuscular mycorrhizal (AM), or ectomycorrhizal (ECM). We measured soil properties and nutrients within each core and determined the tree community composition and richness around each sampling core. Canonical correspondence analyses showed that soil pH and moisture were shared potential drivers of fungal communities for all guilds. However, partial the Mantel tests showed different strength of responses of fungal guilds to composition of trees and soils. Plant pathogens and saprotrophs were more strongly correlated with soil properties than with tree composition; ECM fungi showed a stronger correlation with tree composition than with soil properties; and AM fungi were correlated with soil properties, but not with trees. In conclusion, we show that co-occurring fungal guilds respond differently to abiotic and biotic environmental factors, depending on their ecological function. This highlights the joint role that abiotic and biotic factors play in determining composition of fungal communities, including those associated with plant hosts.

Quantifying Uncertainties in Sequential Chemical Extraction of Soil Phosphorus Using XANES Spectroscopy.

Sequential chemical extraction has been widely used to study soil phosphorus (P) dynamics and inform nutrient management, but its efficacy for assigning P into biologically meaningful pools remains unknown. Here, we evaluated the accuracy of the modified Hedley extraction scheme using P K-edge X-ray absorption near-edge structure (XANES) spectroscopy for nine carbonate-free soil samples with diverse chemical and mineralogical properties resulting from different degrees of soil development. For most samples, the extraction markedly overestimated the pool size of calcium-bound P (Ca-P, extracted by 1 M HCl) due to (1) P redistribution during the alkaline extractions (0.5 M NaHCO3 and then 0.1 M NaOH), creating new Ca-P via formation of Ca phosphates between NaOH-desorbed phosphate and exchangeable Ca2+ and/or (2) dissolution of poorly crystalline Fe and Al oxides by 1 M HCl, releasing P occluded by these oxides into solution. The first mechanism may occur in soils rich in well-crystallized minerals and exchangeable Ca2+ regardless of the presence or absence of CaCO3, whereas the second mechanism likely operates in soils rich in poorly crystalline Fe and Al minerals. The overestimation of Ca-P simultaneously caused underestimation of the pools extracted by the alkaline solutions. Our findings identify key edaphic parameters that remarkably influenced the extractions, which will strengthen our understanding of soil P dynamics using this widely accepted procedure.

Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage.

Soil contains more carbon than the atmosphere and vegetation combined. Understanding the mechanisms controlling the accumulation and stability of soil carbon is critical to predicting the Earth's future climate. Recent studies suggest that decomposition of soil organic matter is often limited by nitrogen availability to microbes and that plants, via their fungal symbionts, compete directly with free-living decomposers for nitrogen. Ectomycorrhizal and ericoid mycorrhizal (EEM) fungi produce nitrogen-degrading enzymes, allowing them greater access to organic nitrogen sources than arbuscular mycorrhizal (AM) fungi. This leads to the theoretical prediction that soil carbon storage is greater in ecosystems dominated by EEM fungi than in those dominated by AM fungi. Using global data sets, we show that soil in ecosystems dominated by EEM-associated plants contains 70% more carbon per unit nitrogen than soil in ecosystems dominated by AM-associated plants. The effect of mycorrhizal type on soil carbon is independent of, and of far larger consequence than, the effects of net primary production, temperature, precipitation and soil clay content. Hence the effect of mycorrhizal type on soil carbon content holds at the global scale. This finding links the functional traits of mycorrhizal fungi to carbon storage at ecosystem-to-global scales, suggesting that plant-decomposer competition for nutrients exerts a fundamental control over the terrestrial carbon cycle.

Protecting people with multiple sclerosis through vaccination.

Vaccination is one of the most effective and cost-efficient methods for protecting people with multiple sclerosis (MS) from infections. However, use of vaccines has often been problematic because of misguided concerns that they may exacerbate the disease and/or that some disease-modifying therapies may influence the immune response to immunisations and/or their safety. People with MS risk higher morbidity and mortality from vaccine-preventable infections. It is, therefore, important to address any patient's reluctance to accept vaccination and to provide clear guidance for clinicians on which vaccinations to consider proactively. We have reviewed the current literature and provide recommendations regarding vaccines in adults with MS, including specific advice regarding vaccination safety in patients receiving-or going to receive-disease-modifying therapies, vaccination during pregnancy, pretravel counselling and patient education.

Microbial responses to warming enhance soil carbon loss following translocation across a tropical forest elevation gradient.

Tropical soils contain huge carbon stocks, which climate warming is projected to reduce by stimulating organic matter decomposition, creating a positive feedback that will promote further warming. Models predict that the loss of carbon from warming soils will be mediated by microbial physiology, but no empirical data are available on the response of soil carbon and microbial physiology to warming in tropical forests, which dominate the terrestrial carbon cycle. Here we show that warming caused a considerable loss of soil carbon that was enhanced by associated changes in microbial physiology. By translocating soils across a 3000 m elevation gradient in tropical forest, equivalent to a temperature change of ± 15 °C, we found that soil carbon declined over 5 years by 4% in response to each 1 °C increase in temperature. The total loss of carbon was related to its original quantity and lability, and was enhanced by changes in microbial physiology including increased microbial carbon-use-efficiency, shifts in community composition towards microbial taxa associated with warmer temperatures, and increased activity of hydrolytic enzymes. These findings suggest that microbial feedbacks will cause considerable loss of carbon from tropical forest soils in response to predicted climatic warming this century.