Unearthing the soil-borne microbiome of land plants.

Plant-soil biodiversity interactions are fundamental for the functioning of terrestrial ecosystems. Yet, the existence of a set of globally distributed topsoil microbial and small invertebrate organisms consistently associated with land plants (i.e., their consistent soil-borne microbiome), together with the environmental preferences and functional capabilities of these organisms, remains unknown. We conducted a standardized field survey under 150 species of land plants, including 58 species of bryophytes and 92 of vascular plants, across 124 locations from all continents. We found that, despite the immense biodiversity of soil organisms, the land plants evaluated only shared a small fraction (less than 1%) of all microbial and invertebrate taxa that were present across contrasting climatic and soil conditions and vegetation types. These consistent taxa were dominated by generalist decomposers and phagotrophs and their presence was positively correlated with the abundance of functional genes linked to mineralization. Finally, we showed that crossing environmental thresholds in aridity (aridity index of 0.65, i.e., the transition from mesic to dry ecosystems), soil pH (5.5; i.e., the transition from acidic to strongly acidic soils), and carbon (less than 2%, the lower limit of fertile soils) can result in drastic disruptions in the associations between land plants and soil organisms, with potential implications for the delivery of soil ecosystem processes under ongoing global environmental change.

Inoculation with extreme endophytes improves performance and nutritional quality in crop species grown under exoplanetary conditions.

Introduction: Technological advances have made possible long space travels and even exoplanetary colonies in the future. Nevertheless, the success of these activities depends on our ability to produce edible plants in stressful conditions such as high radiation, extreme temperatures and low oxygen levels. Since beneficial microorganisms, such as fungal endophytes from extreme environments, have helped agriculture cope with those difficulties, endophytic fungi may be a putative tool to ensure plant growth under exoplanetary conditions. Additionally, growing crops in polyculture has been shown to increase productivity and spatial efficiency, which is essential given the likely space restrictions in such conditions. Methods: We evaluated the effect of the inoculation with a mix of two fungal endophytes from the Atacama Desert on performance (survival and biomass) and nutritional quality of three crop species (lettuce, chard and spinach) grown under exoplanetary conditions. In addition, we measured the amount of antioxidants (flavonoids and phenolics) as possible mechanisms to cope with such abiotic conditions. The exoplanetary conditions were; high UV radiation, low temperature, low water availability, and low oxygen levels. These crops were put in growing chambers in monoculture, dual culture and polyculture (the three species in the same pot) for 30 days. Results and Discussion: Our results show that inoculation with extreme endophytes improved survival by ca. 15 - 35% and biomass by ca. 30 - 35% in all crop species. The most evident increase was when grown in polyculture, except for survival in spinach, where inoculated plants had higher survival only in dual culture. Nutritional quality and the amount of the antioxidant compounds antioxidants increased in all crop species when inoculated with the endophytes. Overall, fungal endophytes isolated from extreme environments such as the Atacama Desert, the driest desert in the world, could be a key biotechnological tool for future space agriculture, helping plants cope with environmental stress. Additionally, inoculated plants should be grown in polyculture to increase crop turnover and space-use efficiency. Lastly, these results provide useful insights to face the future challenges of space-farming.

Genetic control underlying the flowering-drought tolerance trade-off in the Antarctic plant Colobanthus quitensis.

Plants inhabiting environments with stressful conditions often exhibit a low number of flowers, which can be attributed to the energetic cost associated with reproduction. One of the most stressful environments for plants is the Antarctic continent, characterized by limited soil water availability and low temperatures. Induction of dehydrins like those from the COR gene family and auxin transcriptional response repressor genes (IAAs), which are involved in floral repression, has been described in response to water stress. Here, we investigated the relationship between the water deficit-induced stress response and the number of flowers in Colobanthus quitensis plants collected from populations along a latitudinal gradient. The expression levels of COR47 and IAA12 genes in response to water deficit were found to be associated with the number of flowers. The relationship was observed both in the field and growth chambers. Watering the plants in the growth chambers alleviated the stress and stimualted flowering, thereby eliminating the trade-off observed in the field. Our study provides a mechanistic understanding of the ecological constraints on plant reproduction along a water availability gradient. However, further experiments are needed to elucidate the primary role of water availability in regulating resource allocation to reproduction in plants inhibiting extreme environments.

Electromagnetic fields disrupt the pollination service by honeybees.

We assessed the effect that electromagnetic field (EMF) exerts on honeybees' pollination efficiency using field and laboratory experiments. First, we measured levels of gene and protein expression in metabolic pathways involved in stress and behavioral responses elicited by EMF. Second, we assessed the effect of EMF on honeybee behavior and seed production by the honeybee-pollinated California poppy and, lastly, by measuring the consequences of pollination failure on plants' community richness and abundance. EMF exposure exerted strong physiological stress on honeybees as shown by the enhanced expression of heat-shock proteins and genes involved in antioxidant activity and affected the expression levels of behavior-related genes. Moreover, California poppy individuals growing near EMF received fewer honeybee visits and produced fewer seeds than plants growing far from EMF. Last, we found a hump-shaped relationship between EMF and plant species richness and plant abundance. Our study provides conclusive evidence of detrimental impacts of EMF on honeybee's pollination behavior, leading to negative effects on plant community.

Assessing the Importance of Native Mycorrhizal Fungi to Improve Tree Establishment after Wildfires.

The Chilean matorral is a heavily threatened Mediterranean-type ecosystem due to human-related activities such as anthropogenic fires. Mycorrhizal fungi may be the key microorganisms to help plants cope with environmental stress and improve the restoration of degraded ecosystems. However, the application of mycorrhizal fungi in the restoration of the Chilean matorral is limited because of insufficient local information. Consequently, we assessed the effect of mycorrhizal inoculation on the survival and photosynthesis at set intervals for two years after a fire event in four native woody plant species, namely: Peumus boldus, Quillaja saponaria, Cryptocarya alba, and Kageneckia oblonga, all dominant species of the matorral. Additionally, we assessed the enzymatic activity of three enzymes and macronutrient in the soil in mycorrhizal and non-mycorrhizal plants. The results showed that mycorrhizal inoculation increased survival in all studied species after a fire and increased photosynthesis in all, but not in P. boldus. Additionally, the soil associated with mycorrhizal plants had higher enzymatic activity and macronutrient levels in all species except in Q. saponaria, in which there was no significant mycorrhization effect. The results suggest that mycorrhizal fungi could increase the fitness of plants used in restoration initiatives after severe disturbances such as fires and, consequently, should be considered for restoration programs of native species in threatened Mediterranean ecosystems.

Soil contamination in nearby natural areas mirrors that in urban greenspaces worldwide.

Soil contamination is one of the main threats to ecosystem health and sustainability. Yet little is known about the extent to which soil contaminants differ between urban greenspaces and natural ecosystems. Here we show that urban greenspaces and adjacent natural areas (i.e., natural/semi-natural ecosystems) shared similar levels of multiple soil contaminants (metal(loid)s, pesticides, microplastics, and antibiotic resistance genes) across the globe. We reveal that human influence explained many forms of soil contamination worldwide. Socio-economic factors were integral to explaining the occurrence of soil contaminants worldwide. We further show that increased levels of multiple soil contaminants were linked with changes in microbial traits including genes associated with environmental stress resistance, nutrient cycling, and pathogenesis. Taken together, our work demonstrates that human-driven soil contamination in nearby natural areas mirrors that in urban greenspaces globally, and highlights that soil contaminants have the potential to cause dire consequences for ecosystem sustainability and human wellbeing.

Role of Microbes in the degradation of organic semivolatile compounds in polar ecosystems: A review.

The Arctic and the Antarctic Continent correspond to two eco-regions with extreme climatic conditions. These regions are exposed to the presence of contaminants resulting from human activity (local and global), which, in turn, represent a challenge for life forms in these environments. Anthropogenic pollution by semi-volatile organic compounds (SVOCs) in polar ecosystems has been documented since the 1960s. Currently, various studies have shown the presence of SVOCs and their bioaccumulation and biomagnification in the polar regions with negative effects on biodiversity and the ecosystem. Although the production and use of these compounds has been regulated, their persistence continues to threaten biodiversity and the ecosystem. Here, we summarize the current literature regarding microbes and SVOCs in polar regions and pose that bioremediation by native microorganisms is a feasible strategy to mitigate the presence of SVOCs. Our systematic review revealed that microbial communities in polar environments represent a wide reservoir of biodiversity adapted to extreme conditions, found both in terrestrial and aquatic environments, freely or in association with vegetation. Microorganisms adapted to these environments have the potential for biodegradation of SVOCs through a variety of genes encoding enzymes with the capacity to metabolize SVOCs. We suggest that a comprehensive approach at the molecular and ecological level is required to mitigate SVOCs presence in these regions. This is especially patent when considering that SVOCs degrade at slow rates and possess the ability to accumulate in polar ecosystems. The implications of SVOC degradation are relevant for the preservation of polar ecosystems with consequences at a global level.

Sunspot activity influences tree growth: Molecular evidence and ecological implications.

Solar activity has a significant influence on Earth's climate and may drive many biological processes. Here, we measured growth in 11 tree species distributed along an ≈600-km latitudinal gradient in South-Central Chile, recording the width of their growth-rings among periods of maximum (highest number of sunspots) and minimum (lowest number of sunspots) solar activity. In one of these species, Quillaja saponaria, we experimentally assessed three ecophysiological traits (CO2 fixation through photosynthesis [Amax ], growth and leaf production) as well as the expression of five genes related to cell wall elongation and expansion following exposure to high and low levels of UV-B radiation, simulating scenarios of maximum and minimum solar activity, respectively. We found lower tree growth during the periods of maximum solar activity, with this trend being more evident at lower latitudes, where UV-B radiation is higher. Exposure of Q. saponaria to higher levels of UV-B affected the ecophysiological parameters, revealing a decrease in Amax , growth and leaf production. In addition, higher levels of UV-B led to repression in four of the five genes studied. Our results may help foresee environmental scenarios for different plant species associated with solar activity.

The global distribution and environmental drivers of the soil antibiotic resistome.

BACKGROUND: Little is known about the global distribution and environmental drivers of key microbial functional traits such as antibiotic resistance genes (ARGs). Soils are one of Earth's largest reservoirs of ARGs, which are integral for soil microbial competition, and have potential implications for plant and human health. Yet, their diversity and global patterns remain poorly described. Here, we analyzed 285 ARGs in soils from 1012 sites across all continents and created the first global atlas with the distributions of topsoil ARGs. RESULTS: We show that ARGs peaked in high latitude cold and boreal forests. Climatic seasonality and mobile genetic elements, associated with the transmission of antibiotic resistance, were also key drivers of their global distribution. Dominant ARGs were mainly related to multidrug resistance genes and efflux pump machineries. We further pinpointed the global hotspots of the diversity and proportions of soil ARGs. CONCLUSIONS: Together, our work provides the foundation for a better understanding of the ecology and global distribution of the environmental soil antibiotic resistome. Video Abstract.

Global hotspots for soil nature conservation.

Soils are the foundation of all terrestrial ecosystems1. However, unlike for plants and animals, a global assessment of hotspots for soil nature conservation is still lacking2. This hampers our ability to establish nature conservation priorities for the multiple dimensions that support the soil system: from soil biodiversity to ecosystem services. Here, to identify global hotspots for soil nature conservation, we performed a global field survey that includes observations of biodiversity (archaea, bacteria, fungi, protists and invertebrates) and functions (critical for six ecosystem services) in 615 composite samples of topsoil from a standardized survey in all continents. We found that each of the different ecological dimensions of soils-that is, species richness (alpha diversity, measured as amplicon sequence variants), community dissimilarity and ecosystem services-peaked in contrasting regions of the planet, and were associated with different environmental factors. Temperate ecosystems showed the highest species richness, whereas community dissimilarity peaked in the tropics, and colder high-latitudinal ecosystems were identified as hotspots of ecosystem services. These findings highlight the complexities that are involved in simultaneously protecting multiple ecological dimensions of soil. We further show that most of these hotspots are not adequately covered by protected areas (more than 70%), and are vulnerable in the context of several scenarios of global change. Our global estimation of priorities for soil nature conservation highlights the importance of accounting for the multidimensionality of soil biodiversity and ecosystem services to conserve soils for future generations.

Biological Soil Crusts as Ecosystem Engineers in Antarctic Ecosystem.

Biological soil crusts (BSC) are considered as pivotal ecological elements among different ecosystems of the world. The effects of these BSC at the micro-site scale have been related to the development of diverse plant species that, otherwise, might be strongly limited by the harsh abiotic conditions found in environments with low water availability. Here, we describe for the first time the bacterial composition of BSCs found in the proximities of Admiralty Bay (Maritime Antarctica) through 16S metabarcoding. In addition, we evaluated their effect on soils (nutrient levels, enzymatic activity, and water retention), and on the fitness and performance of Colobanthus quitensis, one of the two native Antarctic vascular plants. This was achieved by comparing the photochemical performance, foliar nutrient, biomass, and reproductive investment between C. quitensis plants growing with or without the influence of BSC. Our results revealed a high diversity of prokaryotes present in these soil communities, although we found differences in terms of their abundances. We also found that the presence of BSCs is linked to a significant increase in soils' water retention, nutrient levels, and enzymatic activity when comparing with control soils (without BSCs). In the case of C. quitensis, we found that measured ecophysiological performance parameters were significantly higher on plants growing in association with BSCs. Taken together, our results suggest that BSCs in Antarctic soils are playing a key role in various biochemical processes involved in soil development, while also having a positive effect on the accompanying vascular flora. Therefore, BSCs would be effectively acting as ecosystem engineers for the terrestrial Antarctic ecosystem.

What if the cold days return? Epigenetic mechanisms in plants to cold tolerance.

MAIN CONCLUSION: The epigenetic could be an important, but seldom assessed, mechanisms in plants inhabiting cold ecosystems. Thus, this review could help to fill a gap in the current literature. Low temperatures are one of the most critical environmental conditions that negatively affect the growth, development, and geographic distribution of plants. Exposure to low temperatures results in a suit of physiological, biochemical and molecular modifications through the reprogramming of the expression of genes and transcription factors. Scientific evidence shows that the average annual temperature has increased in recent years worldwide, with cold ecosystems (polar and high mountain) being among the most sensitive to these changes. However, scientific evidence also indicates that there would be specific events of low temperatures, due it is highly relevant to know the capacity for adaptation, regulation and epigenetic memory in the face of these events, by plants. Epigenetic regulation has been described to play an important role in the face of environmental stimuli, especially in response to abiotic stress. Several studies on epigenetic mechanisms have focused on responses to stress as drought and/or salinity; however, there is a gap in the current literature considering those related to low temperatures. In this review, we focus on systematizing the information published to date, related to the regulation of epigenetic mechanisms such as DNA methylation, histone modification, and non-coding RNA-dependent silencing mechanisms, in the face of plant´s stress due to low temperatures. Finally, we present a schematic model about the potential responses by plants taking in count their epigenetic memory; considering a global warming scenario and with the presence or absence of extreme specific events of low temperatures.

Evolution of physiological performance in invasive plants under climate change.

Climate change is expected to promote biological invasions. Invasive species often undergo adaptive evolution, but whether invasive species show greater evolutionary potential than their native counterparts under climate change has rarely been evaluated. We conducted experimental evolution trials comparing the evolution of physiological performance (light-saturated photosynthetic rate, Amax ) of coexisting and closely related (1) invasive-native species pairs from Arid, Alpine, and Antarctic ecosystems, and (2) an invasive-naturalized species pair from a Mediterranean ecosystem differing in invasiveness. Experiments were conducted over three generations and under four environments of temperature and water availability resembling typical and climate change conditions in each ecosystem. Amax increased across generations for most species. Invasive species from Arid, Alpine, and Antarctic ecosystems showed similar, greater, and lesser evolution of Amax than their native counterparts, respectively. The Mediterranean invasive species showed greater evolution of Amax than its naturalized congener. Similar patterns were observed in all four experimental environments for each ecosystem, suggesting that comparable responses may be expected under climate change scenarios. All study species showed a positive association between Amax and reproductive output. Results suggest that invasive plants and their native (or naturalized) counterparts would show similar evolutionary responses of physiological performance to global warming and drought.

Symbiotic Interaction Enhances the Recovery of Endangered Tree Species in the Fragmented Maulino Forest.

Beneficial plant-associated microorganisms, such as fungal endophytes, are key partners that normally improve plant survival under different environmental stresses. It has been shown that microorganisms from extreme environments, like those associated with the roots of Antarctica plants, can be good partners to increase the performance of crop plants and to restore endangered native plants. Nothofagus alessandrii and N. glauca, are among the most endangered species of Chile, restricted to a narrow and/or limited distributional range associated mainly to the Maulino forest in Chile. Here we evaluated the effect of the inoculation with a fungal consortium of root endophytes isolated from the Antarctic host plant Colobanthus quitensis on the ecophysiological performance [photosynthesis, water use efficiency (WUE), and growth] of both endangered tree species. We also, tested how Antarctic root-fungal endophytes could affect the potential distribution of N. alessandrii through niche modeling. Additionally, we conducted a transplant experiment recording plant survival on 2 years in order to validate the model. Lastly, to evaluate if inoculation with Antarctic endophytes has negative impacts on native soil microorganisms, we compared the biodiversity of fungi and bacterial in the rhizospheric soil of transplanted individuals of N. alessandrii inoculated and non-inoculated with fungal endophytes. We found that inoculation with root-endophytes produced significant increases in N. alessandrii and N. glauca photosynthetic rates, water use efficiencies and cumulative growth. In N. alessandrii, seedling survival was significantly greater on inoculated plants compared with non-inoculated individuals. For this species, a spatial distribution modeling revealed that, inoculation with root-fungal endophytes could potentially increase the current distributional range by almost threefold. Inoculation with root-fungal endophytes, did not reduce native rhizospheric microbiome diversity. Our results suggest that the studied consortium of Antarctic root-fungal endophytes improve the ecophysiological performance as well as the survival of inoculated trees and can be used as a biotechnological tool for the restoration of endangered tree species.

A Systematic Review on the Effects of Epichloë Fungal Endophytes on Drought Tolerance in Cool-Season Grasses.

Symptomless fungal endophytes in the genus Epichloë are repeatedly mentioned to increase tolerance of cool-season grasses to a wide range of environmental stress factors, mainly drought. However, the generality of this idea is challenged because (i) most studies have been conducted on two economically important forage grasses {tall fescue [Festuca arundinacea (Schreb.) Dumort] and perennial ryegrass (Lolium perenne L.)}, (ii) endophyte-mediated mechanisms and effects on plant responses to drought have shown to be highly variable across species, and that (iii) symbiosis incidence in plant populations occurring in extremely arid environments is usually low. We question this idea by reviewing the existing information about Epichloë fungal endophyte effects on drought tolerance in cool-season grasses. We combined standard review, vote counting, and calculation of effect sizes to synthesize the literature, identify information gaps, and guide future research. The total number of studies was higher for domesticated than for wild species, a ratio that was balanced when papers with data quality for effect size calculus were considered. After the drought, endophyte-infected plants accumulated more aboveground and belowground biomass than non-infected counterparts, while no effect on tillering was observed. However, these effects remained significant for wild (even on tillering) but not for domesticated species. Interestingly, despite the continuous effort in determining physiological mechanisms behind the endophyte effects, no studies evaluated plant fecundity as a measure of ecological fitness nor vital rates (such as survival) as to escalate individual-level variables to population. Together with the high variability in results, our work shows that generalizing a positive effect of fungal endophytes in plant tolerance to drought may be misleading. Future studies combining field surveys with manipulative experiments would allow us to unravel the role of fungal endophytes in plant adaptation by considering the evolutionary history of species and populations to the different ecological contexts.

Isolation and characterization of microsatellites for the endangered endemic tree Nothofagus alessandrii (Nothofagaceae).

Nothofagus alessandrii (Nothofagaceae) is one of the most endangered trees from Chile due to high rates of habitat disturbance caused by human activities. Despite its conservation status, few molecular markers are available to study its population genetic, connectivity and to assist reproduction programs. Thus, the species needs urgent actions to restore its original distribution. Novel polymorphic microsatellites from the genome of N. alessandrii were isolated and characterized using high-through sequencing. A total of 30 primer pairs were synthesized and 18 microsatellites were amplified correctly. Polymorphism and genetic diversity was evaluated in 58 individuals from three populations of N. alessandrii. Sixteen of them were polymorphic and the number of alleles in the pooled sample ranged from 2 to 14, the mean number of alleles was 4.81. The mean values of observed heterozigosity (HO) and excepted heterozygosity (HE) are similar in all studied populations. Linkage disequilibrium was found between a few pairs of loci (five out of 263 tests) suggesting that most of the markers can be considered as independent. Significant deviations from Hardy-Weinberg equilibrium (P < 0.05) were found in four loci probably due to low sampling size. Transferability to the congeneric N. pumilio was successful in only four out of the sixteen polymorphic markers. The microsatellite markers developed in this study will be useful to study the genetic diversity and structure and to develop integrated management plans for the conservation of this endangered species.

Getting ready for the ozone battle: Vertically transmitted fungal endophytes have transgenerational positive effects in plants.

Ground-level ozone is a global air pollutant with high toxicity and represents a threat to plants and microorganisms. Although beneficial microorganisms can improve host performance, their role in connecting environmentally induced maternal plant phenotypes to progeny (transgenerational effects [TGE]) is unknown. We evaluated fungal endophyte-mediated consequences of maternal plant exposure to ozone on performance of the progeny under contrasting scenarios of the same factor (high and low) at two stages: seedling and young plant. With no variation in biomass, maternal ozone-induced oxidative damage in the progeny that was lower in endophyte-symbiotic plants. This correlated with an endophyte-mediated higher concentration of proline, a defence compound associated with stress control. Interestingly, ozone-induced TGE was not associated with reductions in plant survival. On the contrary, there was an overall positive effect on seedling survival in the presence of endophytes. The positive effect of maternal ozone increasing young plant survival was irrespective of symbiosis and only expressed under high ozone condition. Our study shows that hereditary microorganisms can modulate the capacity of plants to transgenerationally adjust progeny phenotype to atmospheric change.

Epichloë Fungal Endophytes Influence Seed-Associated Bacterial Communities.

Seeds commonly harbour diverse bacterial communities that can enhance the fitness of future plants. The bacterial microbiota associated with mother plant's foliar tissues is one of the main sources of bacteria for seeds. Therefore, any ecological factor influencing the mother plant's microbiota may also affect the diversity of the seed's bacterial community. Grasses form associations with beneficial vertically transmitted fungal endophytes of genus Epichloë. The interaction of plants with Epichloë endophytes and insect herbivores can influence the plant foliar microbiota. However, it is unknown whether these interactions (alone or in concert) can affect the assembly of bacterial communities in the produced seed. We subjected Lolium multiflorum plants with and without its common endophyte Epichloë occultans (E+, E-, respectively) to an herbivory treatment with Rhopalosiphum padi aphids and assessed the diversity and composition of the bacterial communities in the produced seed. The presence of Epichloë endophytes influenced the seed bacterial microbiota by increasing the diversity and affecting the composition of the communities. The relative abundances of the bacterial taxa were more similarly distributed in communities associated with E+ than E- seeds with the latter being dominated by just a few bacterial groups. Contrary to our expectations, seed bacterial communities were not affected by the aphid herbivory experienced by mother plants. We speculate that the enhanced seed/seedling performance documented for Epichloë-host associations may be explained, at least in part, by the Epichloë-mediated increment in the seed-bacterial diversity, and that this phenomenon may be applicable to other plant-endophyte associations.