Soil Symbionts Research Articles

Selection for agronomic traits in intermediate wheatgrass increases responsiveness to arbuscular mycorrhizal fungi

Societal Impact StatementAgricultural practices have had a negative impact on the physical, chemical, and biological components of soil. Perennial cropping systems that facilitate positive soil microbial interactions could not only rebuild soils but also sustain productivity through expected variations in environmental conditions. Here, we show the presence of arbuscular mycorrhizal (AM) fungi, soil symbionts that can improve host performance and soil health, increased the growth of intermediate wheatgrass, a novel perennial grain crop, in populations that have been increasingly bred for desirable agricultural characteristics. The right pairing of intermediate wheatgrass and a beneficial AM fungal community could lead to more sustainable agroecosystems.Summary Intermediate wheatgrass (IWG) is a novel perennial grain that can provide many soil health benefits in agroecosystems; however, little is known about how selection for agronomic traits has impacted interactions with soil biota. Here, we assess how the selection for agronomic traits in IWG has impacted its relationship with arbuscular mycorrhizal (AM) fungi. First, growth response to AM fungi was compared across five generations of IWG with varying degrees of selection. Second, variation in AM fungal responsiveness was compared among genets of IWG individuals within a more advanced generation. Finally, a meta‐analysis was performed on all published studies exploring AM fungal inocula effects on IWG performance to increase understanding of selection effects. AM fungal responsiveness increased with selection for agronomic traits, responsiveness varied among genets in the advanced generation, and a majority of genets performed better in the presence of AM fungi. The meta‐analysis supported the findings that AM fungal responsiveness has increased with selection in IWG. Further studies are needed to realize the combined potential soil health and sustainability benefits of IWG and AM fungi, including assessment of symbiotic benefits beyond biomass production, identification of IWG traits correlated with responsiveness, and characterization of AM fungal community response to IWG.

Drought reduces productivity and anti-herbivore defences, but not mycorrhizal associations, of perennial prairie forbs.

During drought, plants allocate resources to aboveground biomass production and belowground carbohydrate reserves, often at the expense of production of defence traits. Additionally, drought has been shown to alter floral resources, with potential implications for plant-pollinator interactions. Although soil symbionts, such as arbuscular mycorrhizal (AM) fungi, can alleviate drought stress in plants, certain levels of drought may negatively impact this relationship, with potential cascading effects. Because of their importance to plant and animal community diversity, we examined effects of drought on biomass production, physical defence properties, nectar production, and associated AM fungal abundance of five common prairie forb species in a greenhouse study. Reduced soil moisture decreased vegetative biomass production. Production of trichomes and latex decreased under drought, relative to well-watered conditions. Ruellia humilis flowers produced less nectar under drought, relative to well-watered conditions. Intra-radical AM fungal colonization was not significantly affected by drought, although extra-radical AM fungal biomass associated with S. azurea decreased following drought. Overall, grassland forb productivity, defence, and nectar production were negatively impacted by moderate drought, with possible negative implications for biotic interactions. Reduced flower and nectar production may lead to fewer pollinator visitors, which may contribute to seed limitation in forb species. Reduced physical defences increase the likelihood of herbivory, further decreasing the ability to store energy for essential functions, such as reproduction. Together, these results suggest drought can potentially impact biotic interactions between plants and herbivores, pollinators, and soil symbionts, and highlights the need for direct assessments of these relationships under climate change scenarios.

A way to mechanically activate a suspension of black truffle spores

True truffles, or fungi of the genus Tuber, are among the most valuable, rare, expensive, and mysterious fungi on the planet. The reproduction of truffle fungi in the wild is a complex process that depends on many factors, for example, the presence of suitable host trees, as well as the optimal parameters of temperature, moisture, soil pH, soil symbionts, and other organisms. Successful production and reproduction of truffles require a large number of conditions to be met, primarily the release of their spores from ascii, germination under favorable conditions, and distribution in the environment. The present study aims to develop a method for mechanically breaking ascii in order to release the spores of black truffle. It is shown that homogenization by means of an immersion blender together with a vibrating chopper is a highly effective way to break ascii. The microscopic examination of the specimens at all stages of the experiment revealed that this method leads to the breakdown of at least 85% of ascii and the release of truffle spores. The use of centrifugation approaches enables the separation of black truffle spores from hyphal debris, fungal symbionts, and various associated organisms. Such spores can form mycelium on growth media. The study results can be used to prepare Tuber sp. inoculum and obtain their axenic cultures. Thus, the introduction of methods for releasing spores from ascii improves the efficiency of black truffle cultivation.

Altered plant carbon partitioning enhanced forest ecosystem carbon storage after 25 years of nitrogen additions.

Decades of atmospheric nitrogen (N) deposition in the northeastern USA have enhanced this globally important forest carbon (C) sink by relieving N limitation. While many N fertilization experiments found increased forest C storage, the mechanisms driving this response at the ecosystem scale remain uncertain. Following the optimal allocation theory, augmented N availability may reduce belowground C investment by trees to roots and soil symbionts. To test this prediction and its implications on soil biogeochemistry, we constructed C and N budgets for a long-term, whole-watershed N fertilization study at the Fernow Experimental Forest, WV, USA. Nitrogen fertilization increased C storage by shifting C partitioning away from belowground components and towards aboveground woody biomass production. Fertilization also reduced the C cost of N acquisition, allowing for greater C sequestration in vegetation. Despite equal fine litter inputs, the C and N stocks and C:N ratio of the upper mineral soil were greater in the fertilized watershed, likely due to reduced decomposition of plant litter. By combining aboveground and belowground data at the watershed scale, this study demonstrates how plant C allocation responses to N additions may result in greater C storage in both vegetation and soil.

Fungal community assembly in soils and roots under plant invasion and nitrogen deposition

Abstract Fungal community composition in the Anthropocene is driven by rapid changes in environmental conditions caused by human activities. This study examines the relative importance of two global change drivers – atmospheric nitrogen (N) deposition and annual grass invasion – on structuring fungal communities in a California chaparral ecosystem, with emphasis on arbuscular mycorrhizal fungi. We used molecular markers, functional groupings, generalized linear statistics and joint distribution modeling, to examine how environmental variables structure taxonomic and functional composition of fungal communities. Invasive grasses had a lower richness and relative abundance of symbiotic fungi (both AMF and other fungi) compared to native shrubs. We found a higher richness and abundance of rhizophilic (e.g. Glomeraceae) and edaphophilic (e.g. Gigasporaceae) AMF with increasing soil NO3. Our findings suggest that invasive persistence may decrease the presence of multiple soil symbionts that native species depend on for pathogen protection and increased access to soil resources.

Nitrogen‐fixing bacterial communities in invasive legume nodules and associated soils are similar across introduced and native range populations in Australia

AbstractAimUnderstanding the interactions between invasive legumes and soil biota in both native and introduced ranges could assist in managing biological invasions. We analysed the diversity of putative nitrogen‐fixing bacteria (NFB, i.e. nifH gene present) associated with five invasive legumes, four Acacia spp. and a sister taxon Paraserianthes lophantha in introduced and native range populations in Australia. We predicted that, because these host species are widely distributed, they are likely to encounter different nitrogen‐fixing bacterial communities in soils and nodules across their introduced and native ranges.LocationAustralia.MethodsNifH genes were amplified from rhizosphere soils collected from beneath each species (multiple populations) within their native and introduced range and directly from nodules collected from plants previously grown in the glasshouse using field‐collected soil as inoculum. NifH gene sequences from soils and nodules were 454 pyrosequenced and assigned to taxonomic groups based on nifH consensus taxonomy.ResultsWe found no difference in the NFB community of soils or nodules between native and introduced ranges across the five species, suggesting that these legumes encounter similar NFB communities in soils across Australia. Bradyrhizobium was the most abundant rhizobial genus present in both soils and nodules. Bradyrhizobium species found in nodules were significantly different across the ranges for A. longifolia.Main conclusionsThe results indicate that these invasive legumes have similar nitrogen‐fixing bacterial communities in their rhizosphere and nodules across Australia, with the exception of A. longifolia. This species has diverse Bradyrhizobium genotypes in its nodules suggesting that A. longifolia may be a more generalist host compared to the other four legumes. Thus, it is unlikely that the invasive success of these legumes is constrained by the absence of suitable bacterial symbionts in soil. Better knowledge of legume–soil interactions could facilitate more informed and effective management of invasive legumes in their introduced ranges in Australia and elsewhere.

Reduced plant competition among kin can be explained by Jensen's inequality.

Plants often compete with closely related individuals due to limited dispersal, leading to two commonly invoked predictions on competitive outcomes. Kin selection, from evolutionary theory, predicts that competition between relatives will likely be weaker. The niche partitioning hypothesis, from ecological theory, predicts that competition between close relatives will likely be stronger. We tested for evidence consistent with either of these predictions by growing an annual legume in kin and nonkin groups in the greenhouse. We grew plant groups in treatments of symbiotic nitrogen fixing bacteria differing in strain identity and composition to determine if differences in the microbial environment can facilitate or obscure plant competition patterns consistent with kin selection or niche partitioning. Nonkin groups had lower fitness than expected, based on fitness estimates of the same genotypes grown among kin. Higher fitness among kin groups was observed in mixtures of N-fixing bacteria strains compared to single inoculations of bacteria strains present in the soil, which increased fitness differences between kin and nonkin groups. Lower fitness in nonkin groups was likely caused by increased competitive asymmetry in nonkin groups due to genetic differences in plant size combined with saturating relationships with plant size and fitness- i.e. Jensen's inequality. Our study suggests that microbial soil symbionts alter competitive dynamics among kin and nonkin. Our study also suggests that kin groups can have higher fitness, as predicted by kin selection theory, through a commonly heritable trait (plant size), without requiring kin recognition mechanisms.

The mid-domain effect in ectomycorrhizal fungi: range overlap along an elevation gradient on Mount Fuji, Japan.

Mid-domain effect (MDE) models predict that the random placement of species' ranges within a bounded geographical area leads to increased range overlap and species richness in the center of the bounded area. These models are frequently applied to study species-richness patterns of macroorganisms, but the MDE in relation to microorganisms is poorly understood. In this study, we examined the characteristics of the MDE in richness patterns of ectomycorrhizal (EM) fungi, an ecologically important group of soil symbionts. We conducted intensive soil sampling to investigate overlap among species ranges and the applicability of the MDE to EM fungi in four temperate forest stands along an elevation gradient on Mount Fuji, Japan. Molecular analyses using direct sequencing revealed 302 EM fungal species. Of 73 EM fungal species found in multiple stands, 72 inhabited a continuous range along the elevation gradient. The maximum overlap in species range and the highest species richness occurred at elevations in the middle of the gradient. The observed richness pattern also fit within the 95% confidence interval of the mid-domain null model, supporting the role of the MDE in EM fungal richness. Deviation in observed richness from the mean of the mid-domain null estimation was negatively correlated with some environmental factors, including precipitation and soil C/N, indicating that unexplained richness patterns could be driven by these environmental factors. Our results clearly support the existence of microbial species' ranges along environmental gradients and the potential applicability of the MDE to better understand microbial diversity patterns.

A Lover and a Fighter: The Genome Sequence of an Entomopathogenic Nematode Heterorhabditis bacteriophora

Heterorhabditis bacteriophora are entomopathogenic nematodes that have evolved a mutualism with Photorhabdus luminescens bacteria to function as highly virulent insect pathogens. The nematode provides a safe harbor for intestinal symbionts in soil and delivers the symbiotic bacteria into the insect blood. The symbiont provides virulence and toxins, metabolites essential for nematode reproduction, and antibiotic preservation of the insect cadaver. Approximately half of the 21,250 putative protein coding genes identified in the 77 Mbp high quality draft H. bacteriophora genome sequence were novel proteins of unknown function lacking homologs in Caenorhabditis elegans or any other sequenced organisms. Similarly, 317 of the 603 predicted secreted proteins are novel with unknown function in addition to 19 putative peptidases, 9 peptidase inhibitors and 7 C-type lectins that may function in interactions with insect hosts or bacterial symbionts. The 134 proteins contained mariner transposase domains, of which there are none in C. elegans, suggesting an invasion and expansion of mariner transposons in H. bacteriophora. Fewer Kyoto Encyclopedia of Genes and Genomes Orthologies in almost all metabolic categories were detected in the genome compared with 9 other sequenced nematode genomes, which may reflect dependence on the symbiont or insect host for these functions. The H. bacteriophora genome sequence will greatly facilitate genetics, genomics and evolutionary studies to gain fundamental knowledge of nematode parasitism and mutualism. It also elevates the utility of H. bacteriophora as a bridge species between vertebrate parasitic nematodes and the C. elegans model.

Arbuscular mycorrhizal fungi in national parks, nature reserves and protected areas worldwide: a strategic perspective for their in situ conservation

Soil fungi play a crucial role in producing fundamental ecosystem services such as soil fertility, formation and maintenance, nutrient cycling and plant community dynamics. However, they have received little attention in the field of conservation biology. Arbuscular mycorrhizal fungi (AMF) are beneficial soil symbionts fulfilling a key function in the complex networks of belowground/aboveground biotic interactions as they live in association with the roots of most (80%) land plant families and influence not only soil fertility but also plant nutrition, diversity and productivity. The diversity of AMF communities can decline due to habitat loss and anthropogenic disturbance, especially in agro-ecosystems, and many valuable ecotypes could become extinct before they are even discovered. Consequently, long-term strategies are urgently needed to ensure their conservation in habitats where they naturally occur and have evolved. Protected areas, where living organisms are under the care of national and international authorities, represent an appropriate place for the in situ conservation of AMF, providing them with adapted situations together with established complex networks of interactions with different components within each specific ecosystem. Here, we review data available about the main present-day threats to AMF and the current state of knowledge about their occurrence in protected sites worldwide, providing a checklist of national parks and nature reserves where they have been reported. The aim was to offer a strategic perspective to increase awareness of the importance of conserving these beneficial plant symbionts and of preserving their biodiversity in the years to come.

Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta

Photosynthesis is regulated by environmental factors as well as endogenous sugar signals. Whereas light-driven sugar biosynthesis is essential for terrestrial organisms, as well as belowground microflora, whether and how soil symbionts regulate photosynthesis has yet to be reported. Here, we show that the plant growth-promoting soil bacterium Bacillus subtilis GB03 augments photosynthetic capacity by increasing photosynthetic efficiency and chlorophyll content in Arabidopsis. Mechanistic studies reveal an elevation of sugar accumulation as well as the suppression of classic glucose signaling responses, including hypocotyl elongation and seed germination, with exposure to GB03. Compared with wild-type plants, two Arabidopsis mutants defective in hexokinase-dependent sugar signaling exhibit increased photosynthetic capacity, which is not further enhanced with GB03 exposure. Overlap in sugar/ABA sensing is observed in GB03-exposed plants, with a reduction of ABA-biosynthetic transcripts as well as downstream metabolite levels in leaves. Moreover, exogenous ABA abrogates GB03-triggered increases in photosynthetic efficiency and chlorophyll content. These results demonstrate that certain rhizobacteria elevate photosynthesis through the modulation of endogenous sugar/ABA signaling, and establish a regulatory role for soil symbionts in plant acquisition of energy.