Isolation and identification of arbuscular mycorrhizal fungi from an abandoned uranium mine and their role in soil-to-plant transfer of radionuclides and metals.

Arbuscular mycorrhizal fungi were recovered from soil samples from the naturally radioactive soil at the long-abandoned South Terras uranium mine in Cornwall, UK. Species of Rhizophagus, Claroideoglomus, Paraglomus, Septoglomus, and Ambispora were recovered, and pot cultures from all except Ambispora were established. Cultures were identified to species level using morphological observation and rRNA gene sequencing combined with phylogenetic analysis. These cultures were used in pot experiments designed with a compartmentalised system to assess the contribution of fungal hyphae to the accumulation of essential elements, such as copper and zinc, and non-essential elements, such as lead, arsenic, thorium, and uranium into root and shoot tissues of Plantago lanceolata. The results indicated that none of the treatments had any positive or negative impact on shoot and root biomass. However, Rhizophagus irregularis treatments showed higher accumulation of copper and zinc in shoots, while R. irregularis and Septoglomus constrictum enhanced arsenic accumulation in roots. Moreover, R. irregularis increased uranium concentration in roots and shoots of the P. lanceolata plant. This study provides useful insight into fungal-plant interactions that determine metal and radionuclide transfer from soil into the biosphere at contaminated sites such as mine workings.

Geochemistry and microbiology of tropical serpentine soils in the Santa Elena Ophiolite, a landscape-biogeographical approach.

The Santa Elena Ophiolite is a well-studied ultramafic system in Costa Rica mainly comprised of peridotites. Here, tropical climatic conditions promote active laterite formation processes, but the biogeochemistry of the resulting serpentine soils is still poorly understood. The aim of this study was to characterize the soil geochemical composition and microbial community of contrasting landscapes in the area, as the foundation to start exploring the biogeochemistry of metals occurring there. The soils were confirmed as Ni-rich serpentine soils but differed depending on their geographical location within the ophiolite area, showing three serpentine soil types. Weathering processes resulted in mountain soils rich in trace metals such as cobalt, manganese and nickel. The lowlands showed geochemical variations despite sharing similar landscapes: the inner ophiolite lowland soils were more like the surrounding mountain soils rather than the north lowland soils at the border of the ophiolite area, and within the same riparian basin, concentrations of trace metals were higher downstream towards the mangrove area. Microbial community composition reflected the differences in geochemical composition of soils and revealed potential geomicrobiological inputs to local metal biogeochemistry: iron redox cycling bacteria were more abundant in the mountain soils, while more manganese-oxidizing bacteria were found in the lowlands, with the highest relative abundance in the mangrove areas. The fundamental ecological associations recorded in the serpentine soils of the Santa Elena Peninsula, and its potential as a serpentinization endemism hotspot, demonstrate that is a model site to study the biogeochemistry, geomicrobiology and ecology of tropical serpentine areas.

Do trade-offs govern plant species' responses to different global change treatments?

Plants are subject to trade-offs among growth strategies such that adaptations for optimal growth in one condition can preclude optimal growth in another. Thus, we predicted that a plant species that responds positively to one global change treatment would be less likely than average to respond positively to another treatment, particularly for pairs of treatments that favor distinct traits. We examined plant species' abundances in 39 global change experiments manipulating two or more of the following: CO2 , nitrogen, phosphorus, water, temperature, or disturbance. Overall, the directional response of a species to one treatment was 13% more likely than expected to oppose its response to a another single-factor treatment. This tendency was detectable across the global data set, but held little predictive power for individual treatment combinations or within individual experiments. Although trade-offs in the ability to respond to different global change treatments exert discernible global effects, other forces obscure their influence in local communities.

Towards a microbial process-based understanding of the resilience of peatland ecosystem service provisioning - A research agenda.

Peatlands are wetland ecosystems with great significance as natural habitats and as major global carbon stores. They have been subject to widespread exploitation and degradation with resulting losses in characteristic biota and ecosystem functions such as climate regulation. More recently, large-scale programmes have been established to restore peatland ecosystems and the various services they provide to society. Despite significant progress in peatland science and restoration practice, we lack a process-based understanding of how soil microbiota influence peatland functioning and mediate the resilience and recovery of ecosystem services, to perturbations associated with land use and climate change. We argue that there is a need to: in the short-term, characterise peatland microbial communities across a range of spatial and temporal scales and develop an improved understanding of the links between peatland habitat, ecological functions and microbial processes; in the medium term, define what a successfully restored 'target' peatland microbiome looks like for key carbon cycle related ecosystem services and develop microbial-based monitoring tools for assessing restoration needs; and in the longer term, to use this knowledge to influence restoration practices and assess progress on the trajectory towards 'intact' peatland status. Rapid advances in genetic characterisation of the structure and functions of microbial communities offer the potential for transformative progress in these areas, but the scale and speed of methodological and conceptual advances in studying ecosystem functions is a challenge for peatland scientists. Advances in this area require multidisciplinary collaborations between peatland scientists, data scientists and microbiologists and ultimately, collaboration with the modelling community. Developing a process-based understanding of the resilience and recovery of peatlands to perturbations, such as climate extremes, fires, and drainage, will be key to meeting climate targets and delivering ecosystem services cost effectively.

Organic complexation of U(VI) in reducing soils at a natural analogue site: Implications for uranium transport.

Understanding the long-term fate, stability, and bioavailability of uranium (U) in the environment is important for the management of nuclear legacy sites and radioactive wastes. Analysis of U behavior at natural analogue sites permits evaluation of U biogeochemistry under conditions more representative of long-term equilibrium. Here, we have used bulk geochemical and microbial community analysis of soils, coupled with X-ray absorption spectroscopy and µ-focus X-ray fluorescence mapping, to gain a mechanistic understanding of the fate of U transported into an organic-rich soil from a pitchblende vein at the UK Needle's Eye Natural Analogue site. U is highly enriched in the Needle's Eye soils (∼1600 mg kg-1). We show that this enrichment is largely controlled by U(VI) complexation with soil organic matter and not U(VI) bioreduction. Instead, organic-associated U(VI) seems to remain stable under microbially-mediated Fe(III)-reducing conditions. U(IV) (as non-crystalline U(IV)) was only observed at greater depths at the site (>25 cm); the soil here was comparatively mineral-rich, organic-poor, and sulfate-reducing/methanogenic. Furthermore, nanocrystalline UO2, an alternative product of U(VI) reduction in soils, was not observed at the site, and U did not appear to be associated with Fe-bearing minerals. Organic-rich soils appear to have the potential to impede U groundwater transport, irrespective of ambient redox conditions.

A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants.

We report a previously undescribed member of the Helotiales that is superabundant in soils at two maritime Antarctic islands under Antarctic Hairgrass (Deschampsia antarctica Desv.). High throughput sequencing showed that up to 92% of DNA reads, and 68% of RNA reads, in soils from the islands were accounted for by the fungus. Sequencing of the large subunit region of ribosomal (r)DNA places the fungus close to the Pezizellaceae, Porodiplodiaceae, and Sclerotiniaceae, with analyses of internal transcribed spacer regions of rDNA indicating that it has affinities to previously unnamed soil and root fungi from alpine, cool temperate and Low Arctic regions. The fungus was found to be most frequent in soils containing C aged to 1,000-1,200 years before present. The relative abundances of its DNA and RNA reads were positively associated with soil carbon and nitrogen concentrations and δ13C values, with the relative abundance of its DNA being negatively associated with soil pH value. An isolate of the fungus produces flask-shaped phialides with a pronounced venter bearing masses of conidia measuring 4.5-6(7) × 1.8-2.5 µm, suggestive of anamorphic Chalara. Enzymatic studies indicate that the isolate strongly synthesizes the extracellular enzyme acid phosphatase, and also exhibits alkaline phosphatase and naphthol-AS-BI-phosphohydrolase activities. Ecophysiological measurements indicate optimal hyphal growth of the isolate at a pH of 4.2-4.5 and a water potential of -0.66 MPa. The isolate is a psychrotroph, exhibiting measureable hyphal growth at -2°C, optimal hyphal extension rate at 15°C and negligible growth at 25°C. It is proposed that the rising temperatures that are predicted to occur in maritime Antarctica later this century will increase the growth rate of the fungus, with the potential loss of ancient C from soils. Analyses using the GlobalFungi Database indicate that the fungus is present in cold, acidic soils on all continents. We advocate further studies to identify whether it is superabundant in soils under D. antarctica elsewhere in maritime Antarctica, and for further isolates to be obtained so that the species can be formally described.

Endemic and cosmopolitan fungal taxa exhibit differential abundances in total and active communities of Antarctic soils.

Our understanding of the diversity and community dynamics of soil fungi has increased greatly through the use of DNA-based identification. Community characterization of metabolically active communities via RNA sequencing has previously revealed differences between 'active' and 'total' fungal communities, which may be influenced by the persistence of DNA from nonactive components. However, it is not known how fungal traits influence their prevalence in these contrasting community profiles. In this study, we coextracted DNA and RNA from soil collected from three Antarctic islands to test for differences between total and active soil fungal communities. By matching these geographically isolated fungi against a global dataset of soil fungi, we show that widely dispersed taxa are often more abundant in the total community, whilst taxa restricted to Antarctica are more likely to have higher abundance in the active community. In addition, we find that active communities have lower richness, and show a reduction in the abundance of the most dominant fungi, whilst there are consistent differences in the abundances of certain taxonomic groups between the total and active communities. These results suggest that the views of soil fungal communities offered by DNA- and RNA-based characterization differ in predictable ways.

Multiple environmental factors influence 238U, 232Th and 226Ra bioaccumulation in arbuscular mycorrhizal-associated plants.

Ecological consequences of low-dose radioactivity from natural sources or radioactive waste are important to understand but knowledge gaps still remain. In particular, the soil transfer and bioaccumulation of radionuclides into plant roots is poorly studied. Furthermore, better knowledge of arbuscular mycorrhizal (AM) fungi association may help understand the complexities of radionuclide bioaccumulation within the rhizosphere. Plant bioaccumulation of uranium, thorium and radium was demonstrated at two field sites, where plant tissue concentrations reached up to 46.93 µg g-1 238U, 0.67 µg g-1 232Th and 18.27 kBq kg-1 226Ra. High root retention of uranium was consistent in all plant species studied. In contrast, most plants showed greater bioaccumulation of thorium and radium into above-ground tissues. The influence of specific soil parameters on root radionuclide bioaccumulation was examined. Total organic carbon significantly explained the variation in root uranium concentration, while other soil factors including copper concentration, magnesium concentration and pH significantly correlated with root concentrations of uranium, radium and thorium, respectively. All four orders of Glomeromycota were associated with root samples from both sites and all plant species studied showed varying association with AM fungi, ranging from zero to >60% root colonisation by fungal arbuscules. Previous laboratory studies using single plant-fungal species association had found a positive role of AM fungi in root uranium transfer, but no significant correlation between the amount of fungal infection and root uranium content in the field samples was found here. However, there was a significant negative correlation between AM fungal infection and radium accumulation. This study is the first to examine the role of AM fungi in radionuclide soil-plant transfer at a community level within the natural environment. We conclude that biotic factors alongside various abiotic factors influence the soil-plant transfer of radionuclides and future mechanistic studies are needed to explain these interactions in more detail.

Discrete taxa of saprotrophic fungi respire different ages of carbon from Antarctic soils.

Different organic compounds have distinct residence times in soil and are degraded by specific taxa of saprotrophic fungi. It hence follows that specific fungal taxa should respire carbon of different ages from these compounds to the atmosphere. Here, we test whether this is the case by radiocarbon (14C) dating CO2 evolved from two gamma radiation-sterilised maritime Antarctic soils inoculated with pure single cultures of four fungi. We show that a member of the Helotiales, which accounted for 41-56% of all fungal sequences in the two soils, respired soil carbon that was aged up to 1,200 years BP and which was 350-400 years older than that respired by the other three taxa. Analyses of the enzyme profile of the Helotialean fungus and the fluxes and δ13C values of CO2 that it evolved suggested that its release of old carbon from soil was associated with efficient cellulose decomposition. Our findings support suggestions that increases in the ages of carbon respired from warmed soils may be caused by changes to the abundances or activities of discrete taxa of microbes, and indicate that the loss of old carbon from soils is driven by specific fungal taxa.

Asynchrony among local communities stabilises ecosystem function of metacommunities.

Temporal stability of ecosystem functioning increases the predictability and reliability of ecosystem services, and understanding the drivers of stability across spatial scales is important for land management and policy decisions. We used species-level abundance data from 62 plant communities across five continents to assess mechanisms of temporal stability across spatial scales. We assessed how asynchrony (i.e. different units responding dissimilarly through time) of species and local communities stabilised metacommunity ecosystem function. Asynchrony of species increased stability of local communities, and asynchrony among local communities enhanced metacommunity stability by a wide range of magnitudes (1-315%); this range was positively correlated with the size of the metacommunity. Additionally, asynchronous responses among local communities were linked with species' populations fluctuating asynchronously across space, perhaps stemming from physical and/or competitive differences among local communities. Accordingly, we suggest spatial heterogeneity should be a major focus for maintaining the stability of ecosystem services at larger spatial scales.

Not poles apart: Antarctic soil fungal communities show similarities to those of the distant Arctic.

Antarctica's extreme environment and geographical isolation offers a useful platform for testing the relative roles of environmental selection and dispersal barriers influencing fungal communities. The former process should lead to convergence in community composition with other cold environments, such as those in the Arctic. Alternatively, dispersal limitations should minimise similarity between Antarctica and distant northern landmasses. Using high-throughput sequencing, we show that Antarctica shares significantly more fungi with the Arctic, and more fungi display a bipolar distribution, than would be expected in the absence of environmental filtering. In contrast to temperate and tropical regions, there is relatively little endemism, and a strongly bimodal distribution of range sizes. Increasing southerly latitude is associated with lower endemism and communities increasingly dominated by fungi with widespread ranges. These results suggest that micro-organisms with well-developed dispersal capabilities can inhabit opposite poles of the Earth, and dominate extreme environments over specialised local species.

Radioactivity and the environment: technical approaches to understand the role of arbuscular mycorrhizal plants in radionuclide bioaccumulation.

Phytoaccumulation of radionuclides is of significant interest with regards to monitoring radionuclide build-up in food chains, developing methods for environmental bioremediation and for ecological management. There are many gaps in our understanding of the characteristics and mechanisms of plant radionuclide accumulation, including the importance of symbiotically-associated arbuscular mycorrhizal (AM) fungi. We first briefly review the evidence that demonstrates the ability of AM fungi to enhance the translocation of (238)U into plant root tissues, and how fungal association may prevent further mobilization into shoot tissues. We then focus on approaches that should further advance our knowledge of AM fungi-plant radionuclide accumulation. Current research has mostly used artificial cultivation methods and we consider how more ecologically-relevant analysis might be performed. The use of synchrotron-based X-ray fluorescence imaging and absorption spectroscopy techniques to understand the mechanisms of radionuclide transfer from soil to plant via AM fungi is evaluated. Without such further knowledge, the behavior and mobilization of radionuclides cannot be accurately modeled and the potential risks cannot be accurately predicted.

Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time.

Understanding the sensitivity of tundra vegetation to climate warming is critical to forecasting future biodiversity and vegetation feedbacks to climate. In situ warming experiments accelerate climate change on a small scale to forecast responses of local plant communities. Limitations of this approach include the apparent site-specificity of results and uncertainty about the power of short-term studies to anticipate longer term change. We address these issues with a synthesis of 61 experimental warming studies, of up to 20 years duration, in tundra sites worldwide. The response of plant groups to warming often differed with ambient summer temperature, soil moisture and experimental duration. Shrubs increased with warming only where ambient temperature was high, whereas graminoids increased primarily in the coldest study sites. Linear increases in effect size over time were frequently observed. There was little indication of saturating or accelerating effects, as would be predicted if negative or positive vegetation feedbacks were common. These results indicate that tundra vegetation exhibits strong regional variation in response to warming, and that in vulnerable regions, cumulative effects of long-term warming on tundra vegetation - and associated ecosystem consequences - have the potential to be much greater than we have observed to date.

Plant community responses to experimental warming across the tundra biome.

Recent observations of changes in some tundra ecosystems appear to be responses to a warming climate. Several experimental studies have shown that tundra plants and ecosystems can respond strongly to environmental change, including warming; however, most studies were limited to a single location and were of short duration and based on a variety of experimental designs. In addition, comparisons among studies are difficult because a variety of techniques have been used to achieve experimental warming and different measurements have been used to assess responses. We used metaanalysis on plant community measurements from standardized warming experiments at 11 locations across the tundra biome involved in the International Tundra Experiment. The passive warming treatment increased plant-level air temperature by 1-3 degrees C, which is in the range of predicted and observed warming for tundra regions. Responses were rapid and detected in whole plant communities after only two growing seasons. Overall, warming increased height and cover of deciduous shrubs and graminoids, decreased cover of mosses and lichens, and decreased species diversity and evenness. These results predict that warming will cause a decline in biodiversity across a wide variety of tundra, at least in the short term. They also provide rigorous experimental evidence that recently observed increases in shrub cover in many tundra regions are in response to climate warming. These changes have important implications for processes and interactions within tundra ecosystems and between tundra and the atmosphere.

Enzyme production by Mycena galopus mycelium in artificial media and in Picea sitchensis F1 horizon needle litter.

Mycena galopus is among the most important leaf litter decomposers in UK coniferous and angiosperm woodlands, having the potential to utilise all the major constituents of plant litter. Even so, the enzyme or combination of enzymes produced by M. galopus responsible for lignin depolymerisation was previously unknown. A range of media from liquid and semi-solid cultures to more natural substrata was tested to determine whether laccase was produced by an isolate of M. galopus, M9053. Malt extract liquid medium (MEL) with 2,5-xylidine favoured laccase production as compared with the same medium containing the inducers veratryl alcohol, veratryl aldehyde, veratric acid, homoveratric acid, vanillic acid or p-anisic acid. A semi-solid medium of cereal bran in phosphate buffer and a solid medium of Picea sitchensis F1 horizon needle litter were also not as effective as MEL with 2,5-xylidine as an inducer. Compared with six other isolates of the same species grown in MEL without inducers, M9053 exhibited rates of laccase activity fairly typical for M. galopus. An isolate from a dark coloured basidiome of M. galopus, but not var. nigra, exhibited the greatest activity while var. candida showed relatively low laccase activity. Marasmius androsaceus exhibited peak laccase production several days later than M. galopus. In addition, a manganese-dependent peroxidase that was responsible for 15% (in MEL culture fluid) and 39% (in needle litter extract III) of ligninolytic activity was produced by M9053. A further peroxidase was found to be the major ligninolytic constituent in MEL extracts (53%), and had a similar contribution to total activity (29%) as laccase (32%) in needle litter fraction III. Mycena galopus produced water- and buffer-extractable mannases and xylanases when grown on needle litter.