Jonathan R. Leake

Epiparasitic plants specialized on arbuscular mycorrhizal fungi

Over 400 non-photosynthetic species from 10 families of vascular plants obtain their carbon from fungi and are thus defined as myco-heterotrophs. Many of these plants are epiparasitic on green plants from which they obtain carbon by ‘cheating’ shared mycorrhizal fungi. Epiparasitic plants examined to date depend on ectomycorrhizal fungi for carbon transfer and exhibit exceptional specificity for these fungi, but for most myco-heterotrophs neither the identity of the fungi nor the sources of their carbon are known. Because many myco-heterotrophs grow in forests dominated by plants associated with arbuscular mycorrhizal fungi (AMF; phylum Glomeromycota), we proposed that epiparasitism would occur also between plants linked by AMF. On a global scale AMF form the most widespread mycorrhizae, thus the ability of plants to cheat this symbiosis would be highly significant. We analysed mycorrhizae from three populations of Arachnitis uniflora (Corsiaceae, Monocotyledonae), five Voyria species and one Voyriella species (Gentianaceae, Dicotyledonae), and neighbouring green plants. Here we show that non-photosynthetic plants associate with AMF and can display the characteristic specificity of epiparasites. This suggests that AMF mediate significant inter-plant carbon transfer in nature.

Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm

The dramatic decline in atmospheric CO2 evidenced by proxy data during the Devonian (416.0-359.2 Ma) and the gradual decline from the Cretaceous (145.5-65.5 Ma) onwards have been linked to the spread of deeply rooted trees and the rise of angiosperms, respectively. But this paradigm overlooks the coevolution of roots with the major groups of symbiotic fungal partners that have dominated terrestrial ecosystems throughout Earth history. The colonization of land by plants was coincident with the rise of arbuscular mycorrhizal fungi (AMF),while the Cenozoic (c. 65.5-0 Ma) witnessed the rise of ectomycorrhizal fungi (EMF) that associate with both gymnosperm and angiosperm tree roots. Here, we critically review evidence for the influence of AMF and EMF on mineral weathering processes. We show that the key weathering processes underpinning the current paradigm and ascribed to plants are actually driven by the combined activities of roots and mycorrhizal fungi. Fuelled by substantial amounts of recent photosynthate transported from shoots to roots, these fungi form extensive mycelial networks which extend into soil actively foraging for nutrients by altering minerals through the acidification of the immediate root environment. EMF aggressively weather minerals through the additional mechanism of releasing low molecular weight organic chelators. Rates of biotic weathering might therefore be more usefully conceptualized as being fundamentally controlled by the biomass, surface area of contact, and capacity of roots and their mycorrhizal fungal partners to interact physically and chemically with minerals. All of these activities are ultimately controlled by rates of carbon-energy supply from photosynthetic organisms. The weathering functions in leading carbon cycle models require experiments and field studies of evolutionary grades of plants with appropriate mycorrhizal associations. Representation of the coevolution of roots and fungi in geochemical carbon cycle models is required to further our understanding of the role of the biota in Earths CO2 and climate history.

Changes in soil microbial biomass and microbial activities in response to 7 years simulated pollutant nitrogen deposition on a heathland and two grasslands

Abstract The effects of 7 years simulated pollutant nitrogen (N) deposition on soil microbial biomass C (Cmic), soil phosphomonoesterase (PME) activity and utilisation of carbon (C) and organic N and phosphorus (P) sources by soil bacteria are reported for a heathland, an acidic grassland and a calcareous grassland. N additions increased Cmic in the heathland, decreased it in the acid grassland, and had no effect in the calcareous grassland. These effects mirrored the changes in plant cover, indicating close-coupling of plant and microbial responses to chronic N additions. In the heathland, PME activity generally rose with each increment of N addition while in the acid grassland, PME activity significantly increased only in the 14 g N m−2 y−1 (ammonium nitrate) treatment. In the calcareous grassland, PME activity was highly correlated with KCl extractable N (R2 = 0.71), indicating increased PME activity in response to increasing N saturation. At all three sites, PME activity per mg Cmic was greater in plots receiving N inputs, reflecting greater P limitation. In the heathland, N treatments caused a 3-fold increase in the utilisation rate of C and organic N substrates in BIOLOG plates, whereas utilisation of organic P substrates rose 10-fold in response to 8 g N m−2 y−1 and 18-fold in response to 12 g N m−2 y−1. In the acid grassland, utilisation of the C sources decreased in response to the N treatments. The results demonstrate that long-term chronic inputs of pollutant N can significantly increase microbial biomass and activity in N-limited heathland ecosystems, but may reduce microbial biomass and microbial activity in P-limited grasslands.

Plant-driven fungal weathering: Early stages of mineral alteration at the nanometer scale

Plant-driven fungal weathering is a major pathway of soil formation, yet the precise mechanism by which mycorrhiza alter minerals is poorly understood. Here we report the first direct in situ observations of the effects of a soil fungus on the surface of a mineral over which it grew in a controlled experiment. An ectomycorrhizal fungus was grown in symbiosis with a tree seedling so that individual hyphae expanded across the surface of a biotite flake over a period of three months. Ultramicroscopic and spectroscopic analysis of the fungus-biotite interfaces revealed intimate fungal-mineral attachment, biomechanical forcing, altered interlayer spacings, substantial depletion of potassium (~50 nm depth), oxidation of the biotite Fe(II), and the formation of vermiculite and clusters of Fe(III) oxides. Our study demonstrates the biomechanical-chemical alteration interplay at the fungus-biotite interface at the nanometer scale. Specifically, the weathering process is initiated by physical distortion of the lattice structure of biotite within 1 μm of the attached fungal hypha. Only subsequently does the distorted volume become chemically altered through dissolution and oxidation reactions that lead to mineral neoformation.

Base cation depletion, eutrophication and acidification of species-rich grasslands in response to long-term simulated nitrogen deposition

Pollutant nitrogen deposition effects on soil and foliar element concentrations were investigated in acidic and limestone grasslands, located in one of the most nitrogen and acid rain polluted regions of the UK, using plots treated for 8-10 years with 35-140 kg N ha(-2)y(-1) as NH(4)NO(3). Historic data suggests both grasslands have acidified over the past 50 years. Nitrogen deposition treatments caused the grassland soils to lose 23-35% of their total available bases (Ca, Mg, K, and Na) and they became acidified by 0.2-0.4 pH units. Aluminium, iron and manganese were mobilised and taken up by limestone grassland forbs and were translocated down the acid grassland soil. Mineral nitrogen availability increased in both grasslands and many species showed foliar N enrichment. This study provides the first definitive evidence that nitrogen deposition depletes base cations from grassland soils. The resulting acidification, metal mobilisation and eutrophication are implicated in driving floristic changes.

Chitin as a nitrogen source for mycorrhizal fungi

Three ericoid and two ectomycorrhizal fungi were tested for their abilities to utilize chitin as a sole source of nitrogen. All of the ericoid fungi readily degraded chitin. The ecto-fungi, in contrast, used it only sparingly. The results extend the range of polymeric N sources known to be utilized by mycorrhizal fungi and imply that some mycorrhizal fungi may be involved in recycling of N from this structural component of hyphal walls in soil. The possible role of chitinase activity in influencing fungal interactions in heathland ecosystems is discu

Twelve testable hypotheses on the geobiology of weathering

Critical Zone (CZ) research investigates the chemical, physical, and biological processes that modulate the Earths surface. Here, we advance 12 hypotheses that must be tested to improve our understanding of the CZ: (1) Solar-to-chemical conversion of energy by plants regulates flows of carbon, water, and nutrients through plant-microbe soil networks, thereby controlling the location and extent of biological weathering. (2) Biological stoichiometry drives changes in mineral stoichiometry and distribution through weathering. (3) On landscapes experiencing little erosion, biology drives weathering during initial succession, whereas weathering drives biology over the long term. (4) In eroding landscapes, weathering-front advance at depth is coupled to surface denudation via biotic processes. (5) Biology shapes the topography of the Critical Zone. (6) The impact of climate forcing on denudation rates in natural systems can be predicted from models incorporating biogeochemical reaction rates and geomorphological transport laws. (7) Rising global temperatures will increase carbon losses from the Critical Zone. (8) Rising atmospheric P(CO2) will increase rates and extents of mineral weathering in soils. (9) Riverine solute fluxes will respond to changes in climate primarily due to changes in water fluxes and secondarily through changes in biologically mediated weathering. (10) Land use change will impact Critical Zone processes and exports more than climate change. (11) In many severely altered settings, restoration of hydrological processes is possible in decades or less, whereas restoration of biodiversity and biogeochemical processes requires longer timescales. (12) Biogeochemical properties impart thresholds or tipping points beyond which rapid and irreversible losses of ecosystem health, function, and services can occur.

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2

The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that Glomeromycota formed the sole ancestral plant–fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO2 concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon-for-nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid-Palaeozoic (1500 ppm) and near-contemporary (440 ppm) CO2 concentrations using isotope tracers, and analysed cytological differences in plant–fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort–Mucoromycotina symbiosis is mutualistic and mycorrhiza-like, but differs from liverwort–Glomeromycota symbiosis in maintaining functional efficiency of carbon-for-nutrient exchange between partners across CO2 concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild-collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO2, we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis.

Bryophyte physiological responses to, and recovery from, long‐term nitrogen deposition and phosphorus fertilisation in acidic grassland

Atmospheric nitrogen deposition can cause major declines in bryophyte abundance yet the physiological basis for such declines is not fully understood. Bryophyte physiological responses may also be sensitive bioindicators of both the impacts of, and recovery from, N deposition. Here, responses of tissue nutrients (nitrogen (N), phosphorus (P) and potassium (K): NPK), N and P metabolism enzymes (nitrate reductase and phosphomonoesterase), photosynthetic pigments, chlorophyll fluorescence, sclerophylly and percentage cover of two common bryophytes (Pseudoscleropodium purum and Rhytidiadelphus squarrosus) to long-term (11 yr) enhanced N deposition (+3.5 and +14 g N m(-2) yr(-1)) are reported in factorial combination with P addition. Recovery of responses 22 months after treatment cessation were also assessed. Enhanced N deposition caused up to 90% loss of bryophyte cover but no recovery was observed. Phosphomonoesterase activity and tissue N:P ratios increased up to threefold in response to N loading and showed clear recovery, particularly in P. purum. Smaller responses and recovery were also seen in all chlorophyll fluorescence measurements and altered photosynthetic pigment composition. The P limitation of growth appears to be a key mechanism driving bryophyte loss along with damage to photosystem II. Physiological measurements are more sensitive than measurements of abundance as bioindicators of N deposition impact and of recovery in particular.

Organic carbon hidden in urban ecosystems

Urbanization is widely presumed to degrade ecosystem services, but empirical evidence is now challenging these assumptions. We report the first city-wide organic carbon (OC) budget for vegetation and soils, including under impervious surfaces. Urban soil OC storage was significantly greater than in regional agricultural land at equivalent soil depths, however there was no significant difference in storage between soils sampled beneath urban greenspaces and impervious surfaces, at equivalent depths. For a typical U.K. city, total OC storage was 17.6 kg m−2 across the entire urban area (assuming 0 kg m−2 under 15% of land covered by buildings). The majority of OC (82%) was held in soils, with 13% found under impervious surfaces, and 18% stored in vegetation. We reveal that assumptions underpinning current national estimates of ecosystem OC stocks, as required by Kyoto Protocol signatories, are not robust and are likely to have seriously underestimated the contributions of urban areas.