The poly-extreme tolerant black yeasts are prevalent under high ultraviolet light and climatic seasonality across soils of global biomes

Black yeasts are among the most stress-tolerant organisms of the planet, thriving under all types of terrestrial habitats and extreme environments. Yet, their global patterns and ecology remain far less studied, limiting our capacity to identify the main environmental drivers of these important organisms across biomes. To fill this knowledge gap, we analysed topsoils from 235 terrestrial ecosystems across and within globally distributed climate groups (i.e. dry, temperate and continental). We found that soils are important repositories of black yeasts, and that ultraviolet light, fine soil texture, and precipitation seasonality are the most consistent environmental factors associated with their diversity across biomes. Finally, we identified Exophiala and Cladophialophora as the most dominant black yeasts genera in soils across the globe. These findings provide novel evidence of global distribution of black yeasts and their key environmental predictors, giving new insights for speculating the evolution and spreading of these extreme-tolerant organisms throughout both natural and human associated extreme environments.     

Elevated native terrestrial snail abundance and diversity in association with an invasive understory shrub,Berberis thunbergii,in a North American deciduous forest

Invasive terrestrial plants often substantially reshape environments, yet how such invasions affect terrestrial snail assemblages remains understudied. We investigated how snail assemblages in deciduous forest soils with dense Berberis thunbergii (Japanese barberry), an invasive shrub in eastern North America, differ from forest areas lacking the shrub. Leaf litter and soil samples were collected from forest patches with dense B. thunbergii understories and adjacent control areas within two exurban forest tracts in western Pennsylvania, U.S.A. Snails were identified to species and quantified by standard diversity metrics. Contrary to our expectations, snails were significantly more abundant and diverse in B. thunbergii-invaded areas. Despite differences in abundance, the snail community composition did not differ between invaded and control habitats. The terrestrial snail assemblage we observed, which was composed entirely of native species, appears to respond favorably to B. thunbergii invasion and therefore may not be negatively impacted by physicochemical changes to soils typically observed in association with the plant. Such findings could reflect the fact that B. thunbergii likely creates more favorable habitat for snails by creating cooler, more humid, and more alkaline soil environments. However, the snail assemblages we retrieved may consist mostly of species with high tolerance to environmental degradation due to a legacy of land use change and acid deposition in the region.     

Microplastics as an emerging threat to terrestrial ecosystems

Microplastics (plastics <5 mm, including nanoplastics which are <0.1 μm) originate from the fragmentation of large plastic litter or from direct environmental emission. Their potential impacts in terrestrial ecosystems remain largely unexplored despite numerous reported effects on marine organisms. Most plastics arriving in the oceans were produced, used, and often disposed on land. Hence, it is within terrestrial systems that microplastics might first interact with biota eliciting ecologically relevant impacts. This article introduces the pervasive microplastic contamination as a potential agent of global change in terrestrial systems, highlights the physical and chemical nature of the respective observed effects, and discusses the broad toxicity of nanoplastics derived from plastic breakdown. Making relevant links to the fate of microplastics in aquatic continental systems, we here present new insights into the mechanisms of impacts on terrestrial geochemistry, the biophysical environment, and ecotoxicology. Broad changes in continental environments are possible even in particle‐rich habitats such as soils. Furthermore, there is a growing body of evidence indicating that microplastics interact with terrestrial organisms that mediate essential ecosystem services and functions, such as soil dwelling invertebrates, terrestrial fungi, and plant‐pollinators. Therefore, research is needed to clarify the terrestrial fate and effects of microplastics. We suggest that due to the widespread presence, environmental persistence, and various interactions with continental biota, microplastic pollution might represent an emerging global change threat to terrestrial ecosystems.     

The Development of Fungal Networks in Complex Environments

Fungi are of fundamental importance in terrestrial ecosystems playing important roles in decomposition, nutrient cycling, plant symbiosis and pathogenesis, and have significant potential in several areas of environmental biotechnology such as biocontrol and bioremediation. In all of these contexts, the fungi are growing in environments exhibiting spatio-temporal nutritional and structural heterogeneities. In this work, a discrete mathematical model is derived that allows detailed understanding of how events at the hyphal level are influenced by the nature of various environmental heterogeneities. Mycelial growth and function is simulated in a range of environments including homogeneous conditions, nutritionally-heterogeneous conditions and structurally-heterogeneous environments, the latter emulating porous media such as soils. Our results provide further understanding of the crucial processes involved in fungal growth, nutrient translocation and concomitant functional consequences, e.g. acidification, and have implications for the biotechnological application of fungi.     

Paradigm shifts in soil organic matter research affect interpretations of aquatic carbon cycling: transcending disciplinary and ecosystem boundaries

New conceptual models that highlight the importance of environmental, rather than molecular, controls on soil organic matter affect interpretations of organic matter (OM) persistence across terrestrial and aquatic boundaries. We propose that changing paradigms in our thinking about OM decomposition explain some of the uncertainties surrounding the fate of land-derived carbon (C) in marine environments. Terrestrial OM, which historically has been thought to be chemically recalcitrant to decay in soil and aquatic environments, dominates inputs to rivers yet is found in trace amounts in the ocean. We discuss three major transformations in our understanding of OM persistence that influence interpretations of the fate of aquatic OM: (1) a shift away from an emphasis on chemical recalcitrance as a primary predictor of turnover; (2) new interpretations of radiocarbon ages, which affect predictions of reactivity; and (3) the recognition that most OM leaving soils in dissolved form has been microbially processed. The first two explain rapid turnover for terrigenous OM in aquatic ecosystems once it leaves the soil matrix. The third suggests that the presence of terrestrial OM in aquatic ecosystems may be underestimated by the use of plant biomarkers. Whether these mechanisms occur in isolation of each other or in combination, they provide insight into the missing terrestrial C signature in the ocean. Spatially and temporally varying transformations of OM along land–water networks require that common terrestrial source indicators be interpreted within specific environmental contexts. We identify areas of research where collaborations between aquatic and terrestrial scientists will enhance quantification of C transfer from soils to inland water bodies, the ocean, and the atmosphere. Accurate estimates of OM processing are essential for improving predictions of the response of vulnerable C pools at the interface of soil and water to changes in climate and land use.     

A critical review of soil algae as a crucial soil biological component of high ecological and economic significance

Aero-terrestrial algae are ecologically and economically valuable bioresources contributing to carbon sequestration, sustenance of soil health, and fertility. Compared to aquatic algae, the literature on subaerial algae is minimal, including studies of distinctive habitats such as forest soils, agricultural fields, deserts, polar regions, specific subaerial zones, artificial structures, and tropical soils. The primary goal here was to identify the gaps and scope of research on such algae. Accordingly, the literature was analyzed per sub-themes, such as the “nature of current research data on terrestrial algae,” “methodological approaches,” “diversity,” “environmental relationships,” “ecological roles,” and “economic significance.” The review showed there is a high diversity of algae in soils, especially members belonging to the Cyanophyta (Cyanobacteria) and Chlorophyta. Algal distributions in terrestrial environments depend on the microhabitat conditions, and many species of soil algae are sensitive to specific soil conditions. The ecological significance of soil algae includes primary production, the release of biochemical stimulants and plant growth promoters into soils, nitrogen fixation, solubilization of minerals, and the enhancement and maintenance of soil fertility. Since aero-terrestrial habitats are generally stressed environments, algae of such environments can be rich in rare metabolites and natural products. For example, epilithic soil algae use wet adhesive molecules to fix them firmly on the substratum. Exploring the ecological roles and economic utility of soil and other subaerial algae could be helpful for the development of algae-based industries and for achieving sustainable soil management.     

Toxicological Considerations of Contaminants in the Terrestrial Environment for Ecological Risk Assessment

The terrestrial environment acts as a “sink” for contaminants that have been purposely or accidentally released into the environment. Science and policy that support protective measures for terrestrial ecosystems have run behind those of aquatic toxicology and water quality concerns. As a result ecological risk assessment (ERA) involving terrestrial environments tends to be conducted at a simplistic level, relying on numeric targets (soil quality criteria) as a basis for decision-making. However, soil criteria for ecological receptors are somewhat deficient in terms of the numbers available and the data that supports these numbers. Direct toxicity assessments (DTA) for terrestrial environments, such as those used for water quality evaluations, can provide additional useful information about the toxicity and bioavailability of mixtures of contaminants present in soils. This article outlines the approaches used for assessing the toxicity of soil contaminants in terrestrial environments and critiques their advantages and pitfalls.     

Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs

Extracellular enzymes produced by heterotrophic microbial communities are major drivers of carbon and nutrient cycling in terrestrial, freshwater, and marine environments. Although carbon and nutrient cycles are coupled on global scales, studies of extracellular enzymes associated with terrestrial, freshwater, and marine microbial communities are not often compared across ecosystems. In part, this disconnect arises because the environmental parameters that control enzyme activities in terrestrial and freshwater systems, such as temperature, pH, and moisture content, have little explanatory power for patterns of enzyme activities in marine systems. Instead, factors such as the functional diversity of microbial communities may explain varying patterns of enzyme activities observed in the ocean to date. In any case, many studies across systems focus on similar issues that highlight the commonalities of microbial community organization. Examples include the effective lifetime of enzymes released into the environment; the extent to which microbial communities coordinate enzyme expression to decompose complex organic substrates; and the influence of microbial community composition on enzyme activities and kinetics. Here we review the often-disparate research foci in terrestrial, freshwater, and marine environments. We consider the extent to which environmental factors may regulate extracellular enzyme activities within each ecosystem, and highlight commonalities and current methodological challenges to identify research questions that may aid in integrating cross-system perspectives in the future.     

Ecophysiology of psychrophilic and psychrotolerant microorganisms.

This review describes psychrophilic and psychrotolerant microorganisms, which are abundant in different kinds of environments. Their ecophysiological properties and strategies for survival are reviewed in relation to their occurrences in marine and terrestrial environments, with special reference to the deep-sea, the sea ice and the permafrost soils.     

Predator–prey interactions and changing environments: who benefits?

While aquatic environments have long been thought to be more moderate environments than their terrestrial cousins, environmental data demonstrate that for some systems this is not so. Numerous important environmental parameters can fluctuate dramatically, notably dissolved oxygen, turbidity and temperature. The roles of dissolved oxygen and turbidity on predator-prey interactions have been discussed in detail elsewhere within this issue and will be considered only briefly here. Here, we will focus primarily on the role of temperature and its potential impact upon predator-prey interactions. Two key properties are of particular note. For temperate aquatic ecosystems, all piscine and invertebrate piscivores and their prey are ectothermic. They will therefore be subject to energetic demands that are significantly affected by environmental temperature. Furthermore, the physical properties of water, particularly its high thermal conductivity, mean that thermal microenvironments will not exist so that fine-scale habitat movements will not be an option for dealing with changing water temperature in lentic environments. Unfortunately, there has been little experimental analysis of the role of temperature on such predator-prey interactions, so we will instead focus on theoretical work, indicating that potential implications associated with thermal change are unlikely to be straightforward and may present a greater threat to predators than to their prey. Specifically, we demonstrate that changes in the thermal environment can result in a net benefit to cold-adapted species through the mechanism of predator-prey interactions.     

Ecoenzymatic stoichiometry of stream sediments with comparison to terrestrial soils

The kinetics and elemental composition of cellular units that mediate production and respiration are the basis for the metabolic and stoichiometric theories of ecological organization. This theoretical framework extends to the activities of microbial enzymes released into the environment (ecoenzymes) that mediate the release of assimilable substrate from detrital organic matter. In this paper, we analyze the stoichiometry of ecoenzymatic activities in the surface sediments of lotic ecosystems and compare those results to the stoichiometry observed in terrestrial soils. We relate these ecoenzymatic ratios to energy and nutrient availability in the environment as well as microbial elemental content and growth efficiency. The data, collected by US Environmental Protection Agency, include the potential activities of 11 enzymes for 2,200 samples collected across the US, along with analyses of sediment C, N and P content. On average, ecoenzymatic activities in stream sediments are 2–5 times greater per gC than those of terrestrial soils. Ecoenzymatic ratios of C, N and P acquisition activities support elemental analyses showing that microbial metabolism is more likely to be C-limited than N or P-limited compared to terrestrial soils. Ratios of hydrolytic to oxidative activities indicate that sediment organic matter is more labile than soil organic matter and N acquisition is less dependent on humic oxidation. The mean activity ratios of glycosidases and aminopeptidases reflect the environmental abundance of their respective substrates. For both freshwater sediments and terrestrial soils, the mean C:nutrient ratio of microbial biomass normalized to growth efficiency approximates the mean ecoenzymatic C:nutrient activity ratios normalized to environmental C:nutrient abundance. This relationship defines a condition for biogeochemical equilibrium consistent with stoichiometric and metabolic theory.     

High beta diversity of bacteria in the shallow terrestrial subsurface

While there have been a vast number of studies on bacterial alpha diversity in the shallow terrestrial subsurface, beta diversity - how the bacterial community composition changes with spatial distance - has received surprisingly limited attention. Here, bacterial beta diversity and its controlling factors are investigated by denaturing gradient gel electrophoresis and cloning of samples from a 700-cm-long sediment core, the lower half of which consisted of marine-originated sediments. According to canonical correspondence analysis with variation partitioning, contemporary environmental variables explain beta diversity in a greater proportion than depth. However, we also found that community similarity decayed significantly with spatial distance and the slopes of the distance-decay relationships are relatively high. The high beta diversity indicates that the bacterial distribution patterns are not only controlled by contemporary environments, but also related to historical events, that is, dispersal or depositional history. This is highlighted by the different beta diversity patterns among studied sediment layers. We thus conclude that the high beta diversity in the shallow terrestrial subsurface is a trade-off between historical events and environmental heterogeneity. Furthermore, we suggest that the high beta diversity of bacteria is likely to be recapitulated in other terrestrial sites because of the great frequency of high geochemical and/or historical variations along depth.     

A consensus protocol for the recovery of mercury methylation genes from metagenomes

Mercury (Hg) methylation genes (hgcAB) mediate the formation of the toxic methylmercury and have been identified from diverse environments, including freshwater and marine ecosystems, Arctic permafrost, forest and paddy soils, coal-ash amended sediments, chlor-alkali plants discharges and geothermal springs. Here we present the first attempt at a standardized protocol for the detection, identification and quantification of hgc genes from metagenomes. Our Hg-cycling microorganisms in aquatic and terrestrial ecosystems (Hg-MATE) database, a catalogue of hgc genes, provides the most accurate information to date on the taxonomic identity and functional/metabolic attributes of microorganisms responsible for Hg methylation in the environment. Furthermore, we introduce “marky-coco”, a ready-to-use bioinformatic pipeline based on de novo single-metagenome assembly, for easy and accurate characterization of hgc genes from environmental samples. We compared the recovery of hgc genes from environmental metagenomes using the marky-coco pipeline with an approach based on coassembly of multiple metagenomes. Our data show similar efficiency in both approaches for most environments except those with high diversity (i.e., paddy soils) for which a coassembly approach was preferred. Finally, we discuss the definition of true hgc genes and methods to normalize hgc gene counts from metagenomes.     

Hydrocarbon degradation in soils and methods for soil biotreatment

The cleanup of soils and groundwater contaminated with hydrocarbons is of particular importance in minimizing the environmental impact of petroleum and petroleum products and in preventing contamination of potable water supplies. Consequently, there is a growing industry involved in the treatment of contaminated topsoils, subsoils, and groundwater. The biotreatment methodologies employed for decontamination are designed to enhance in situ degradation by the supply of oxygen, inorganic nutrients, and/or microbial inocula to the contaminated zone. This review considers the fate and effects of hydrocarbon contaminants in terrestrial environments, with particular reference to the factors that limit biodegradation rates. The potential efficiencies, advantages, and disadvantages of biotreatment techniques are discussed and the future research directions necessary for process development are considered.     

Peeking through a frosty window: molecular insights into the ecology of Arctic soil fungi

Fungi are ubiquitous in Arctic soils, where they function as symbionts and decomposers and may affect the carbon balance of terrestrial ecosystems subjected to climate change, and yet little is known about soil fungi at high latitudes. Here we review data from recent molecular studies to determine broad patterns in Arctic soil fungal ecology. The data indicate comparatively high fungal diversity in Arctic soils, with currently no evidence for lower species richness at higher latitudes. The dominant fungi, and particularly ectomycorrhizal-forming fungi, appear to be cosmopolitan species. Arctic soil fungi are capable of growth at sub-zero temperatures, melanized forms are frequent, host specificity is low and there is evidence that community composition alters under experimental warming. Future challenges are to determine the drivers of fungal diversity, whether or not diversity alters at higher latitudes and how apparently cosmopolitan fungi are able to survive the extreme environments encountered in Arctic habitats.     

Drivers of epsilonproteobacterial community composition in sulfidic caves and springs

Epsilonproteobacteria are widely distributed in marine, freshwater, and terrestrial environments, although most well-studied groups are from hydrothermal vents and the human intestinal tract. The environmental variables that control epsilonproteobacterial communities in sulfidic terrestrial environments, however, are poorly understood. Here, the environmental variables that influence epsilonproteobacterial community composition in geographically separated sulfidic caves and springs were determined by coarse and fine-scale approaches: denaturing gradient gel electrophoresis profiling of 23S rRNA PCR amplicons and clone library sequencing of the 16S-ITS-23S rRNA operon. Sequences retrieved from this study were not closely related to cultured representatives, indicating that existing culture collections do not adequately capture the diversity of terrestrial Epsilonproteobacteria. Comparisons of 16S-ITS-23S rRNA operon sequences from four sites revealed that some distant communities (> 8000 km) share closely related populations of Epsilonproteobacteria, while other sites have nearly clonal and phylogenetically distinct populations. Statistical evaluations of sequence data reveal that multiple environmental variables (e.g. temperature, pH, salinity, dissolved oxygen, and bicarbonate concentrations) influence Epsilonproteobacteria community composition. Locations with clonal populations tended to be from higher temperatures and intermediate dissolved oxygen concentrations. rRNA operon sequences outside of the 16S rRNA gene may be critical to recognizing environmental drivers of epsilonproteobacterial community composition.     

Frankia and Alnus rubra Canopy Roots: An Assessment of Genetic Diversity, Propagule Availability, and Effects on Soil Nitrogen

The ecological importance of microbial symbioses in terrestrial soils is widely recognized, but their role in soils that accumulate in forest canopies is almost entirely unknown. To address this gap, this study investigated the Frankia–Alnus rubra symbiosis in canopy and forest floor roots at Olympic National Park, WA, USA. Sixteen mature A. rubra trees were surveyed and Frankia genetic diversity in canopy and forest floor nodules was assessed with sequence-based nifH analyses. A seedling bioassay experiment was conducted to determine Frankia propagule availability in canopy and forest floor soils. Total soil nitrogen from both environments was also quantified. Nodules were present in the canopies of nine of the 16 trees sampled. Across the study area, Frankia canopy and forest floor assemblages were similar, with both habitats containing the same two genotypes. The composition of forest floor and canopy genotypes on the same tree was not always identical, however, suggesting that dispersal was not a strictly local phenomenon. Frankia seedling colonization was similar in canopy soils regardless of the presence of nodules as well as in forest floor soils, indicating that dispersal was not likely to be a major limiting factor. The total soil nitrogen of canopy soils was higher than that of forest floor soils, but the presence of Frankia nodules in canopy soils did not significantly alter soil nitrogen levels. Overall, this study indicates that the Frankia–A. rubra symbiosis is similar in canopy and forest floor environments. Because canopy roots are exposed to different environmental conditions within very small spatial areas and because those areas can be easily manipulated (e.g., fertilizer or watering treatments), they present microbial ecologists with a unique arena to examine root–microbe interactions.     

Ecological partitioning among parapatric cryptic species

Geographic range differences among species may result from differences in their physiological tolerances. In the intertidal zone, marine and terrestrial environments intersect to create a unique habitat, across which physiological tolerance strongly influences range. Traits to cope with environmental extremes are particularly important here because many species live near their physiological limits and environmental gradients can be steep. The snail Melampus bidentatus occurs in coastal salt marshes in the western Atlantic and the Gulf of Mexico. We used sequence data from one mitochondrial (COI) and two nuclear markers (histone H3 and a mitochondrial carrier protein, MCP) to identify three cryptic species within this broad‐ranging nominal species, two of which have partially overlapping geographic ranges. High genetic diversity, low population structure, and high levels of migration within these two overlapping species suggest that historical range limitations do not entirely explain their different ranges. To identify microhabitat differences between these two species, we modelled their distributions using data from both marine and terrestrial environments. Although temperature was the largest factor setting range limits, other environmental components explained features of the ranges that temperature alone could not. In particular, the interaction of precipitation and salinity likely sets physiological limits that lead to range differences between these two cryptic species. This suggests that the response to climatic change in these snails will be mediated by changes to multiple environmental factors, and not just to temperature alone.     

Conditions in Home and Transplant Soils Have Differential Effects on the Performance of Diploid and Allotetraploid Anthericum Species

Due to increased levels of heterozygosity, polyploids are expected to have a greater ability to adapt to different environments than their diploid ancestors. While this theoretical pattern has been suggested repeatedly, studies comparing adaptability to changing conditions in diploids and polyploids are rare. The aim of the study was to determine the importance of environmental conditions of origin as well as target conditions on performance of two Anthericum species, allotetraploid A. liliago and diploid A. ramosum and to explore whether the two species differ in the ability to adapt to these environmental conditions. Specifically, we performed a common garden experiment using soil from 6 localities within the species’ natural range, and we simulated the forest and open environments in which they might occur. We compared the performance of diploid A. ramosum and allotetraploid A. liliago originating from different locations in the different soils. The performance of the two species was not affected by simulated shading but differed strongly between the different target soils. Growth of the tetraploids was not affected by the origin of the plants. In contrast, diploids from the most nutrient poor soil performed best in the richest soil, indicating that diploids from deprived environments have an increased ability to acquire nutrients when available. They are thus able to profit from transfer to novel nutrient rich environments. Therefore, the results of the study did not support the general expectation that the polyploids should have a greater ability than the diploids to adapt to a wide range of conditions. In contrast, the results are in line with the observation that diploids occupy a wider range of environments than the allotetraploids in our system.     

Yeast forms dominate fungal diversity in the deep oceans

Fungi are the principal degraders of biomass in most terrestrial ecosystems. In contrast to surface environments, deep-sea environmental gene libraries have suggested that fungi are rare and non-diverse in high-pressure marine environments. Here, we report the diversity of fungi from 11 deep-sea samples from around the world representing depths from 1,500 to 4,000 m (146-388 atm) and two shallower water column samples (250 and 500m). We sequenced 239 clones from 10 fungal-specific 18S rRNA gene libraries constructed from these samples, from which we detected only 18 fungal 18S-types in deep-sea samples. Our phylogenetic analyses show that a total of only 32 fungal 18S-types have so far been recovered from deep-sea habitats, and our results suggest that fungi, in general, are relatively rare in the deep-sea habitats we sampled. The fungal diversity detected suggests that deep-sea environments host an evolutionarily diverse array of fungi dominated by groups of distantly related yeasts, although four putative filamentous fungal 18S-types were detected. The majority of our new sequences branch close to known fungi found in surface environments. This pattern contradicts the proposal that deep-sea and hydrothermal vent habitats represent ancient ecosystems, and demonstrates a history of frequent dispersal between terrestrial and deep-sea habitats.