Inhibitory effects of climate change on the growth and extracellular enzyme activities of a widespread Antarctic soil fungus.

Temperatures approaching or exceeding 20°C have been measured during summer in polar regions at the surfaces of barren fellfield soils under cloudless skies around solar noon. However, despite the upper temperature limit for the growth of cold-adapted microbes-which are abundant in polar soils and have pivotal roles in nutrient cycling-typically being close to this temperature, previous studies have not addressed the consequences of climate change for the metabolism of these organisms in the natural environment. Here in a 5-year field experiment on Alexander Island in the southern maritime Antarctic, we show that the abundance of Pseudogymnoascus roseus, the most widespread decomposer fungus in maritime Antarctic fellfield soils, is reduced by 1-2 orders of magnitude when irrigated and nutrient-amended soils are warmed to >20°C during summer. Laboratory experiments under conditions mimicking those during midsummer in the natural environment indicated that the hyphal extension rates of P. roseus isolates and the activities of five extracellular enzymes are reduced by 54%-96% at high water availability after exposure to temperatures cycling daily from 2 to 21°C and 2 to 24°C, relative to temperatures cycling from 2 to 18°C. Given that the temperatures of surface soils at the study site already reach 19°C during midsummer, the observations reported here suggest that, at predicted rates of warming arising from moderate greenhouse gas emissions, inhibitory effects of climate change on the metabolism of P. roseus could manifest themselves within the next few decades. Furthermore, with peak temperatures at the surfaces of fellfield soils at other maritime Antarctic locations and in High Arctic and alpine regions already exceeding 20°C during summer, the observations suggest that climate warming has the potential to inhibit the growth of other cold-adapted microbes, with negative effects on soils as the Earth's climate continues to warm.

Temperature sensitivity of soil respiration rates enhanced by microbial community response.

Soils store about four times as much carbon as plant biomass, and soil microbial respiration releases about 60 petagrams of carbon per year to the atmosphere as carbon dioxide. Short-term experiments have shown that soil microbial respiration increases exponentially with temperature. This information has been incorporated into soil carbon and Earth-system models, which suggest that warming-induced increases in carbon dioxide release from soils represent an important positive feedback loop that could influence twenty-first-century climate change. The magnitude of this feedback remains uncertain, however, not least because the response of soil microbial communities to changing temperatures has the potential to either decrease or increase warming-induced carbon losses substantially. Here we collect soils from different ecosystems along a climate gradient from the Arctic to the Amazon and investigate how microbial community-level responses control the temperature sensitivity of soil respiration. We find that the microbial community-level response more often enhances than reduces the mid- to long-term (90 days) temperature sensitivity of respiration. Furthermore, the strongest enhancing responses were observed in soils with high carbon-to-nitrogen ratios and in soils from cold climatic regions. After 90 days, microbial community responses increased the temperature sensitivity of respiration in high-latitude soils by a factor of 1.4 compared to the instantaneous temperature response. This suggests that the substantial carbon stores in Arctic and boreal soils could be more vulnerable to climate warming than currently predicted.

Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic.

In contrast to the situation in plants inhabiting most of the world's ecosystems, mycorrhizal fungi are usually absent from roots of the only two native vascular plant species of maritime Antarctica, Deschampsia antarctica and Colobanthus quitensis. Instead, a range of ascomycete fungi, termed dark septate endophytes (DSEs), frequently colonise the roots of these plant species. We demonstrate that colonisation of Antarctic vascular plants by DSEs facilitates not only the acquisition of organic nitrogen as early protein breakdown products, but also as non-proteinaceous d-amino acids and their short peptides, accumulated in slowly-decomposing organic matter, such as moss peat. Our findings suggest that, in a warming maritime Antarctic, this symbiosis has a key role in accelerating the replacement of formerly dominant moss communities by vascular plants, and in increasing the rate at which ancient carbon stores laid down as moss peat over centuries or millennia are returned to the atmosphere as CO2 .

Bacterial Community Composition and Diversity Respond to Nutrient Amendment but Not Warming in a Maritime Antarctic Soil.

A resumption of climate warming in maritime Antarctica, arising from continued greenhouse gas emissions to the atmosphere, is predicted to lead to further expansions of plant populations across the region, with consequent increases in nutrient inputs to soils. Here, we test the main and interactive effects of warming, applied with open top chambers (OTCs), and nutrient amendment with tryptic soy broth (TSB), an artificial growth substrate, on bacterial community composition and diversity using Illumina sequencing of 16S rRNA genes in soil from a field experiment in the southern maritime Antarctic. Substantial effects of TSB application on bacterial communities were identified after 49 months, including reduced diversity, altered phylogenetic community assembly processes, increased Proteobacteria-to-Acidobacteria ratios and significant divergence in community composition, notably increases in the relative abundances of the gram-positive genera Arthrobacter, Paeniglutamicibacter and Planococcus. Contrary to previous observations from other maritime Antarctic field warming experiments, we recorded no effects of warming with OTCs, or interactive effects of OTCs and TSB application, on bacterial community composition or diversity. Based on these findings, we conclude that further warming of the maritime Antarctic is unlikely to influence soil bacterial community composition or diversity directly, but that increased nutrient inputs arising from enhanced plant growth across the region may affect the composition of soil bacterial communities, with possible effects on ecosystem productivity.

Biogeographic survey of soil bacterial communities across Antarctica.

BACKGROUND: Antarctica and its unique biodiversity are increasingly at risk from the effects of global climate change and other human influences. A significant recent element underpinning strategies for Antarctic conservation has been the development of a system of Antarctic Conservation Biogeographic Regions (ACBRs). The datasets supporting this classification are, however, dominated by eukaryotic taxa, with contributions from the bacterial domain restricted to Actinomycetota and Cyanobacteriota. Nevertheless, the ice-free areas of the Antarctic continent and the sub-Antarctic islands are dominated in terms of diversity by bacteria. Our study aims to generate a comprehensive phylogenetic dataset of Antarctic bacteria with wide geographical coverage on the continent and sub-Antarctic islands, to investigate whether bacterial diversity and distribution is reflected in the current ACBRs. RESULTS: Soil bacterial diversity and community composition did not fully conform with the ACBR classification. Although 19% of the variability was explained by this classification, the largest differences in bacterial community composition were between the broader continental and maritime Antarctic regions, where a degree of structural overlapping within continental and maritime bacterial communities was apparent, not fully reflecting the division into separate ACBRs. Strong divergence in soil bacterial community composition was also apparent between the Antarctic/sub-Antarctic islands and the Antarctic mainland. Bacterial communities were partially shaped by bioclimatic conditions, with 28% of dominant genera showing habitat preferences connected to at least one of the bioclimatic variables included in our analyses. These genera were also reported as indicator taxa for the ACBRs. CONCLUSIONS: Overall, our data indicate that the current ACBR subdivision of the Antarctic continent does not fully reflect bacterial distribution and diversity in Antarctica. We observed considerable overlap in the structure of soil bacterial communities within the maritime Antarctic region and within the continental Antarctic region. Our results also suggest that bacterial communities might be impacted by regional climatic and other environmental changes. The dataset developed in this study provides a comprehensive baseline that will provide a valuable tool for biodiversity conservation efforts on the continent. Further studies are clearly required, and we emphasize the need for more extensive campaigns to systematically sample and characterize Antarctic and sub-Antarctic soil microbial communities. Video Abstract.

'Follow the Water': Microbial Water Acquisition in Desert Soils.

Water availability is the dominant driver of microbial community structure and function in desert soils. However, these habitats typically only receive very infrequent large-scale water inputs (e.g., from precipitation and/or run-off). In light of recent studies, the paradigm that desert soil microorganisms are largely dormant under xeric conditions is questionable. Gene expression profiling of microbial communities in desert soils suggests that many microbial taxa retain some metabolic functionality, even under severely xeric conditions. It, therefore, follows that other, less obvious sources of water may sustain the microbial cellular and community functionality in desert soil niches. Such sources include a range of precipitation and condensation processes, including rainfall, snow, dew, fog, and nocturnal distillation, all of which may vary quantitatively depending on the location and geomorphological characteristics of the desert ecosystem. Other more obscure sources of bioavailable water may include groundwater-derived water vapour, hydrated minerals, and metabolic hydro-genesis. Here, we explore the possible sources of bioavailable water in the context of microbial survival and function in xeric desert soils. With global climate change projected to have profound effects on both hot and cold deserts, we also explore the potential impacts of climate-induced changes in water availability on soil microbiomes in these extreme environments.

Experimental warming increases fungal alpha diversity in an oligotrophic maritime Antarctic soil.

The climate of maritime Antarctica has altered since the 1950s. However, the effects of increased temperature, precipitation and organic carbon and nitrogen availability on the fungal communities inhabiting the barren and oligotrophic fellfield soils that are widespread across the region are poorly understood. Here, we test how warming with open top chambers (OTCs), irrigation and the organic substrates glucose, glycine and tryptone soy broth (TSB) influence a fungal community inhabiting an oligotrophic maritime Antarctic fellfield soil. In contrast with studies in vegetated soils at lower latitudes, OTCs increased fungal community alpha diversity (Simpson's index and evenness) by 102-142% in unamended soil after 5 years. Conversely, OTCs had few effects on diversity in substrate-amended soils, with their only main effects, in glycine-amended soils, being attributable to an abundance of Pseudogymnoascus. The substrates reduced alpha and beta diversity metrics by 18-63%, altered community composition and elevated soil fungal DNA concentrations by 1-2 orders of magnitude after 5 years. In glycine-amended soil, OTCs decreased DNA concentrations by 57% and increased the relative abundance of the yeast Vishniacozyma by 45-fold. The relative abundance of the yeast Gelidatrema declined by 78% in chambered soil and increased by 1.9-fold in irrigated soil. Fungal DNA concentrations were also halved by irrigation in TSB-amended soils. In support of regional- and continental-scale studies across climatic gradients, the observations indicate that soil fungal alpha diversity in maritime Antarctica will increase as the region warms, but suggest that the accumulation of organic carbon and nitrogen compounds in fellfield soils arising from expanding plant populations are likely, in time, to attenuate the positive effects of warming on diversity.

Regional Diversity of Maritime Antarctic Soil Fungi and Predicted Responses of Guilds and Growth Forms to Climate Change.

We report a metabarcoding study documenting the fungal taxa in 29 barren fellfield soils sampled from along a 1,650 km transect encompassing almost the entire maritime Antarctic (60-72°S) and the environmental factors structuring the richness, relative abundance, and taxonomic composition of three guilds and growth forms. The richness of the lichenised fungal guild, which accounted for 19% of the total fungal community, was positively associated with mean annual surface air temperature (MASAT), with an increase of 1.7 operational taxonomic units (OTUs) of lichenised fungi per degree Celsius rise in air temperature. Soil Mn concentration, MASAT, C:N ratio, and pH value determined the taxonomic composition of the lichenised guild, and the relative abundance of the guild was best predicted by soil Mn concentration. There was a 3% decrease in the relative abundance of the saprotrophic fungal guild in the total community for each degree Celsius rise in air temperature, and the OTU richness of the guild, which accounted for 39% of the community, was negatively associated with Mn concentration. The taxonomic composition of the saprotrophic guild varied with MASAT, pH value, and Mn, NH4 +-N, and SO4 2- concentrations. The richness of the yeast community, which comprised 3% of the total fungal community, was positively associated with soil K concentration, with its composition being determined by C:N ratio. In contrast with a similar study in the Arctic, the relative abundance and richness of lichenised fungi declined between 60°S and 69°S, with those of saprotrophic Agaricales also declining sharply in soils beyond 63°S. Basidiomycota, which accounted for 4% of reads, were much less frequent than in vegetated soils at lower latitudes, with the Ascomycota (70% of reads) being the dominant phylum. We conclude that the richness, relative abundance, and taxonomic composition of guilds and growth forms of maritime Antarctic soil fungi are influenced by air temperature and edaphic factors, with implications for the soils of the region as its climate changes during the 21st century.

No evidence for compensatory thermal adaptation of soil microbial respiration in the study of Bradford et al. (2008).

Bradford et al. (2008) conclude that thermal adaptation will reduce the response of soil microbial respiration to rising global temperatures. However, we question both the methods used to calculate mass-specific respiration rates and the interpretation of the results. No clear evidence of thermal adaptation reducing soil microbial activity was produced.

Strategies for monitoring and managing mass populations of toxic cyanobacteria in recreational waters: a multi-interdisciplinary approach.

Mass populations of toxin-producing cyanobacteria commonly develop in fresh-, brackish- and marine waters and effective strategies for monitoring and managing cyanobacterial health risks are required to safeguard animal and human health. A multi-interdisciplinary study, including two UK freshwaters with a history of toxic cyanobacterial blooms, was undertaken to explore different approaches for the identification, monitoring and management of potentially-toxic cyanobacteria and their associated risks. The results demonstrate that (i) cyanobacterial bloom occurrence can be predicted at a local- and national-scale using process-based and statistical models; (ii) cyanobacterial concentration and distribution in waterbodies can be monitored using remote sensing, but minimum detection limits need to be evaluated; (iii) cyanotoxins may be transferred to spray-irrigated root crops; and (iv) attitudes and perceptions towards risks influence the public's preferences and willingness-to-pay for cyanobacterial health risk reductions in recreational waters.

Soil bacterial diversity is positively associated with air temperature in the maritime Antarctic.

Terrestrial ecosystems in the maritime Antarctic experienced rapid warming during the latter half of the 20th century. While warming ceased at the turn of the millennium, significant increases in air temperature are expected later this century, with predicted positive effects on soil fungal diversity, plant growth and ecosystem productivity. Here, by sequencing 16S ribosomal RNA genes in 40 soils sampled from along a 1,650 km climatic gradient through the maritime Antarctic, we determine whether rising air temperatures might similarly influence the diversity of soil bacteria. Of 22 environmental factors, mean annual surface air temperature was the strongest and most consistent predictor of soil bacterial diversity. Significant, but weaker, associations between bacterial diversity and soil moisture content, C:N ratio, and Ca, Mg, PO43- and dissolved organic C concentrations were also detected. These findings indicate that further rises in air temperature in the maritime Antarctic may enhance terrestrial ecosystem productivity through positive effects on soil bacterial diversity.

Nematodes in a polar desert reveal the relative role of biotic interactions in the coexistence of soil animals.

Abiotic factors are major determinants of soil animal distributions and their dominant role is pronounced in extreme ecosystems, with biotic interactions seemingly playing a minor role. We modelled co-occurrence and distribution of the three nematode species that dominate the soil food web of the McMurdo Dry Valleys (Antarctica). Abiotic factors, other biotic groups, and autocorrelation all contributed to structuring nematode species distributions. However, after removing their effects, we found that the presence of the most abundant nematode species greatly, and negatively, affected the probability of detecting one of the other two species. We observed similar patterns in relative abundances for two out of three pairs of species. Harsh abiotic conditions alone are insufficient to explain contemporary nematode distributions whereas the role of negative biotic interactions has been largely underestimated in soil. The future challenge is to understand how the effects of global change on biotic interactions will alter species coexistence.

Biotic interactions are an unexpected yet critical control on the complexity of an abiotically driven polar ecosystem.

Abiotic and biotic factors control ecosystem biodiversity, but their relative contributions remain unclear. The ultraoligotrophic ecosystem of the Antarctic Dry Valleys, a simple yet highly heterogeneous ecosystem, is a natural laboratory well-suited for resolving the abiotic and biotic controls of community structure. We undertook a multidisciplinary investigation to capture ecologically relevant biotic and abiotic attributes of more than 500 sites in the Dry Valleys, encompassing observed landscape heterogeneities across more than 200 km2. Using richness of autotrophic and heterotrophic taxa as a proxy for functional complexity, we linked measured variables in a parsimonious yet comprehensive structural equation model that explained significant variations in biological complexity and identified landscape-scale and fine-scale abiotic factors as the primary drivers of diversity. However, the inclusion of linkages among functional groups was essential for constructing the best-fitting model. Our findings support the notion that biotic interactions make crucial contributions even in an extremely simple ecosystem.

Soil microbial respiration in arctic soil does not acclimate to temperature.

Warming-induced release of CO2 from the large carbon (C) stores in arctic soils could accelerate climate change. However, declines in the response of soil respiration to warming in long-term experiments suggest that microbial activity acclimates to temperature, greatly reducing the potential for enhanced C losses. As reduced respiration rates with time could be equally caused by substrate depletion, evidence for thermal acclimation remains controversial. To overcome this problem, we carried out a cooling experiment with soils from arctic Sweden. If acclimation causes the reduction in soil respiration observed after experimental warming, then it should subsequently lead to an increase in respiration rates after cooling. We demonstrate that thermal acclimation did not occur following cooling. Rather, during the 90 days after cooling, a further reduction in the soil respiration rate was observed, which was only reversed by extended re-exposure to warmer temperatures. We conclude that over the time scale of a few weeks to months, warming-induced changes in the microbial community in arctic soils will amplify the instantaneous increase in the rates of CO2 production and thus enhance C losses potentially accelerating the rate of 21st century climate change.

Field and pulping performances of transgenic trees with altered lignification.

The agronomic and pulping performance of transgenic trees with altered lignin has been evaluated in duplicated, long-term field trials. Poplars expressing cinnamyl alcohol dehydrogenase (CAD) or caffeate/5-hydroxy-ferulate O-methyltransferase (COMT) antisense transgenes were grown for four years at two sites, in France and England. The trees remained healthy throughout the trial. Growth indicators and interactions with insects were normal. No changes in soil microbial communities were detected beneath the transgenic trees. The expected modifications to lignin were maintained in the transgenics over four years, at both sites. Kraft pulping of tree trunks showed that the reduced-CAD lines had improved characteristics, allowing easier delignification, using smaller amounts of chemicals, while yielding more high-quality pulp. This work highlights the potential of engineering wood quality for more environmentally benign papermaking without interfering with tree growth or fitness.

Global Diversity of Desert Hypolithic Cyanobacteria.

Global patterns in diversity were estimated for cyanobacteria-dominated hypolithic communities that colonize ventral surfaces of quartz stones and are common in desert environments. A total of 64 hypolithic communities were recovered from deserts on every continent plus a tropical moisture sufficient location. Community diversity was estimated using a combined t-RFLP fingerprinting and high throughput sequencing approach. The t-RFLP analysis revealed desert communities were different from the single non-desert location. A striking pattern also emerged where Antarctic desert communities were clearly distinct from all other deserts. Some overlap in community similarity occurred for hot, cold and tundra deserts. A further observation was that the producer-consumer ratio displayed a significant negative correlation with growing season, such that shorter growing seasons supported communities with greater abundance of producers, and this pattern was independent of macroclimate. High-throughput sequencing of 16S rRNA and nifH genes from four representative samples validated the t-RFLP study and revealed patterns of taxonomic and putative diazotrophic diversity for desert communities from the Taklimakan Desert, Tibetan Plateau, Canadian Arctic and Antarctic. All communities were dominated by cyanobacteria and among these 21 taxa were potentially endemic to any given desert location. Some others occurred in all but the most extreme hot and polar deserts suggesting they were relatively less well adapted to environmental stress. The t-RFLP and sequencing data revealed the two most abundant cyanobacterial taxa were Phormidium in Antarctic and Tibetan deserts and Chroococcidiopsis in hot and cold deserts. The Arctic tundra displayed a more heterogenous cyanobacterial assemblage and this was attributed to the maritime-influenced sampling location. The most abundant heterotrophic taxa were ubiquitous among samples and belonged to the Acidobacteria, Actinobacteria, Bacteroidetes, and Proteobacteria. Sequencing using nitrogenase gene-specific primers revealed all putative diazotrophs were Proteobacteria of the orders Burkholderiales, Rhizobiales, and Rhodospirillales. We envisage cyanobacterial carbon input to the system is accompanied by nitrogen fixation largely from non-cyanobacterial taxa. Overall the results indicate desert hypoliths worldwide are dominated by cyanobacteria and that growing season is a useful predictor of their abundance. Differences in cyanobacterial taxa encountered may reflect their adaptation to different moisture availability regimes in polar and non-polar deserts.

Microbial community structure in soils with decomposing residues from plants with genetic modifications to lignin biosynthesis.

Lignin is a major determinant of the decomposition of plant materials in soils. Advances in transgenic technology have led to the possibility of modifying lignin to improve the pulping properties of plant materials for papermaking. Previous studies have shown that lignin modifications also affect the rate of plant material decay in soil. The aim of this work was to investigate short-term changes in soil microbial community structures when tobacco residues with reduced activity of enzymes in the monolignol pathway decompose. The residues from lignin-modified plants all decomposed faster than unmodified plant materials. The relative proportions of some of the structural groups of microbial phospholipid fatty acids were affected by genetic modifications, especially the proportion of double unsaturated chain fatty acids, indicative of fungi.

Temporal dynamics of hot desert microbial communities reveal structural and functional responses to water input.

The temporal dynamics of desert soil microbial communities are poorly understood. Given the implications for ecosystem functioning under a global change scenario, a better understanding of desert microbial community stability is crucial. Here, we sampled soils in the central Namib Desert on sixteen different occasions over a one-year period. Using Illumina-based amplicon sequencing of the 16S rRNA gene, we found that α-diversity (richness) was more variable at a given sampling date (spatial variability) than over the course of one year (temporal variability). Community composition remained essentially unchanged across the first 10 months, indicating that spatial sampling might be more important than temporal sampling when assessing ß-diversity patterns in desert soils. However, a major shift in microbial community composition was found following a single precipitation event. This shift in composition was associated with a rapid increase in CO2 respiration and productivity, supporting the view that desert soil microbial communities respond rapidly to re-wetting and that this response may be the result of both taxon-specific selection and changes in the availability or accessibility of organic substrates. Recovery to quasi pre-disturbance community composition was achieved within one month after rainfall.

The Role of Microbial Community Composition in Controlling Soil Respiration Responses to Temperature.

Rising global temperatures may increase the rates of soil organic matter decomposition by heterotrophic microorganisms, potentially accelerating climate change further by releasing additional carbon dioxide (CO2) to the atmosphere. However, the possibility that microbial community responses to prolonged warming may modify the temperature sensitivity of soil respiration creates large uncertainty in the strength of this positive feedback. Both compensatory responses (decreasing temperature sensitivity of soil respiration in the long-term) and enhancing responses (increasing temperature sensitivity) have been reported, but the mechanisms underlying these responses are poorly understood. In this study, microbial biomass, community structure and the activities of dehydrogenase and ß-glucosidase enzymes were determined for 18 soils that had previously demonstrated either no response or varying magnitude of enhancing or compensatory responses of temperature sensitivity of heterotrophic microbial respiration to prolonged cooling. The soil cooling approach, in contrast to warming experiments, discriminates between microbial community responses and the consequences of substrate depletion, by minimising changes in substrate availability. The initial microbial community composition, determined by molecular analysis of soils showing contrasting respiration responses to cooling, provided evidence that the magnitude of enhancing responses was partly related to microbial community composition. There was also evidence that higher relative abundance of saprophytic Basidiomycota may explain the compensatory response observed in one soil, but neither microbial biomass nor enzymatic capacity were significantly affected by cooling. Our findings emphasise the key importance of soil microbial community responses for feedbacks to global change, but also highlight important areas where our understanding remains limited.

Taxonomic and Functional Diversity of Soil and Hypolithic Microbial Communities in Miers Valley, McMurdo Dry Valleys, Antarctica.

The McMurdo Dry Valleys of Antarctica are an extreme polar desert. Mineral soils support subsurface microbial communities and translucent rocks support development of hypolithic communities on ventral surfaces in soil contact. Despite significant research attention, relatively little is known about taxonomic and functional diversity or their inter-relationships. Here we report a combined diversity and functional interrogation for soil and hypoliths of the Miers Valley in the McMurdo Dry Valleys of Antarctica. The study employed 16S rRNA fingerprinting and high throughput sequencing combined with the GeoChip functional microarray. The soil community was revealed as a highly diverse reservoir of bacterial diversity dominated by actinobacteria. Hypolithic communities were less diverse and dominated by cyanobacteria. Major differences in putative functionality were that soil communities displayed greater diversity in stress tolerance and recalcitrant substrate utilization pathways, whilst hypolithic communities supported greater diversity of nutrient limitation adaptation pathways. A relatively high level of functional redundancy in both soil and hypoliths may indicate adaptation of these communities to fluctuating environmental conditions.