Summary
Arbuscular mycorrhizal (AM) fungi gain access to nutrient patches outside the rhizosphere by producing an extensive network of fine hyphae. Here, we focused on establishing the mechanism by ...which AM fungal hyphae reach discrete organic patches with a cohort of functional bacteria transported in a biofilm on their surface.
We investigated the mechanisms and impact of the translocation of phosphate solubilising bacteria (PSB) along AM fungal hyphae in bespoke microcosms. An in vitro culture experiment was also conducted to determine the direct impact of hyphal exudates of AM fungi upon the growth of PSB.
The extraradical hyphae of AM fungi can transport PSB to organic phosphorus (P) patches and enhance organic P mineralisation both under in vitro culture and soil conditions. Bacteria move in a thick water film formed around fungal hyphae. However, the bacteria cannot be transferred to the organic P patch without an energy source in the form of hyphal exudates.
Our results could be harnessed to better manage plant–microbe interactions and improve the ability of biological inocula involving AM fungi and bacteria to enhance the sustainability of agricultural crops in P limited conditions.
See also the Commentary on this article by Jansa & Hodge, 230: 14–16.
More than two-thirds of terrestrial plants acquire nutrients by forming a symbiosis with arbuscular mycorrhizal (AM) fungi. AM fungal hyphae recruit distinct microbes into their hyphosphere, the ...narrow region of soil influenced by hyphal exudates. They thereby shape this so-called second genome of AM fungi, which significantly contributes to nutrient mobilization and turnover. We summarize current insights into characteristics of the hyphosphere microbiome and the role of hyphal exudates on orchestrating its composition. The hyphal exudates not only contain carbon-rich compounds but also promote bacterial growth and activity and influence the microbial community structure. These effects lead to shifts in function and cause changes in organic nutrient cycling, making the hyphosphere a unique and largely overlooked functional zone in ecosystems.
Arbuscular mycorrhizal (AM) fungi release hyphal compounds into the soil to orchestrate the hyphosphere colonized by a diversity of microbes.The composition of the hyphosphere microbiome is different to bulk soil and rhizosphere.Nutrient cycling in the hyphosphere is affected by the change in microbiome.Shifts in microbial function cause changes in organic nutrient cycling, making the hyphosphere a unique and important functional zone in ecosystems.
Summary
The mycorrhizal pathway is an important phosphorus (P) uptake pathway for more than two‐thirds of land plants. The arbuscular mycorrhizal (AM) fungi‐associated hyphosphere microbiome has been ...considered as the second genome of mycorrhizal P uptake pathway and functionality in mobilizing soil organic P (Po). However, whether there is a core microbiome in the hyphosphere and how this is implicated in mining soil Po are less understood.
We established on‐site field trials located in humid, semiarid, and arid zones and a microcosm experiment in a glasshouse with specific AM fungi and varying soil types to answer the above questions.
The hyphosphere microbiome of AM fungi enhanced soil phosphatase activity and promoted Po mineralization in all sites. Although the assemblage of hyphosphere microbiomes identified in three climate zones was mediated by environmental factors, we detected a core set in three sites and the subsequent microcosm experiment. The core members were co‐enriched in the hyphosphere and dominated by Alphaproteobacteria, Actinobacteria, and Gammaproteobacteria. Moreover, these core bacterial members aggregate into stable guilds that contributed to phosphatase activity.
The core hyphosphere microbiome is taxonomically conserved and provides functions, with respect to the mineralization of Po, that AM fungi lack.
See also the Commentary on this article by Johnson & Marín, 238: 461–463.
Background
Most plants have a hyphosphere, the thin zone of soil around extraradical hyphae of arbuscular mycorrhizal (AM) fungi, which extends beyond the rhizosphere. This important interface has ...critical roles in plant mineral nutrition and water acquisition, biotic and abiotic stress resistance, mineral weathering, the formation of soil macroaggregates and aggregate stabilization, carbon (C) allocation to soils and interaction with soil microbes.
Scope
This review focuses on the hyphosphere of AM fungi and critically appraises the important findings related to the hyphosphere processes, including physical, chemical and biological properties and functions. We highlight ecological functions of AM fungal hyphae, which have profound impacts on global sustainability through biological cycling of nutrients, C sequestration in soil, release of greenhouse gas emissions from soil and the diversity and dynamics of the microbial community in the vicinity of the extraradical hyphae.
Conclusions
As a critical interface between AM fungi and soil, hyphosphere processes and their important ecological functions have begun to be understood and appreciated, and are now known to be implicit in important soil processes. Recent studies provide new insights into this crucial zone and highlight how the hyphosphere might be exploited as a nature-based solution, through understanding of interactions with the microbiome and the impacts on key processes governing resource availability, to increase sustainability of agriculture and minimize its environmental impact. Uncovering hyphosphere chemical and biological processes and their subsequent agricultural, ecological and environmental consequences is a critical research activity.
Summary
The extraradical hyphae of arbuscular mycorrhizal fungi (AMF) harbour and interact with a microbial community performing multiple functions. However, how the AMF‐microbiome interaction ...influences the phosphorus (P) acquisition efficiency of the mycorrhizal pathway is unclear. Here we investigated whether AMF and their hyphal microbiome play a role in promoting organic phosphorus (P) mineralizing under field conditions. We developed an AMF hyphae in‐growth core system for the field using PVC tubes sealed with membrane with different size of pores (30 or 0.45 μm) to allow or deny AMF hyphae access to a patch of organic P in root‐free soil. AMF and their hyphae associated microbiome played a role in enhancing soil organic P mineralization in situ in the field, which was shown to be a function of the change in bacteria community on the hyphae surface. The bacterial communities attached to the AMF hyphae surface were significantly different from those in the bulk soil. Importantly, AMF hyphae recruited bacteria that produced alkaline phosphatase and provided a function that was absent from the hyphae. These results demonstrate the importance of understanding trophic interactions to be able to gain insight into the functional controls of nutrient cycles in the rhizosphere.
Summary
The extraradical hyphae of arbuscular mycorrhizal (AM) fungi are colonized by different bacteria in natural and agricultural systems, but the mechanisms by which AM fungi interact with the ...hyphosphere soil microbiome and influence soil organic phosphorus (P) mobilization remain unclear.
We grew Medicago in two‐compartment microcosms, inoculated with Rhizophagus irregularis, or not, in the root compartment and set up P treatments (without P, with P addition as KH2PO4 or nonsoluble phytate) in the hyphal compartment. We studied the processes of soil P turnover and characterized the microbiome functional profiles for P turnover in the hyphosphere soil by metagenomic sequencing.
Compared with the bulk soil, the hyphosphere soil of R. irregularis was inhabited by a specific bacterial community and their functional profiles for P turnover was stimulated. At the species level, the shift in hyphosphere soil microbiome was characterized by the recruitment of the genome bin2.39 harbouring both gcd and phoD genes and genome bin2.97 harbouring the phoD gene, which synergistically drove nonsoluble phytate mobilization in the hyphosphere soil.
Our results suggest that AM fungi recruits a specific hyphosphere soil microbiome and stimulated their functional profiles for P turnover to enhance utilization of phytate.
Background Phosphorus (P) fertilizer is usually applied in excess of plant requirement and accumulates in soils due to its strong adsorption, rapid precipitation and immobilisation into unavailable ...forms including organic moieties. As soils are complex and diverse chemical, biochemical and biological systems, strategies to access recalcitrant soil P are often inefficient, case specific and inconsistently applicable in different soils. Finding a near-universal or at least widely applicable solution to the inefficiency in agricultural P use by plants is an important unsolved problem that has been under investigation for more than half a century. Scope In this paper we critically review the strategies proposed for the remobilization of recalcitrant soil phosphorus for crops and pastures worldwide. We have additionally performed a meta-analysis of available soil 31P–NMR data to establish the potential agronomic value of different stored P forms in agricultural soils. Conclusions Soil inorganic P stocks accounted on average for 1006 ± 115 kg ha−1 (57 ± 7%), while the monoester P pool accounted for 587 ± 32 kg ha−1 (33 ± 2%), indicating the huge potential for the future agronomic use of the soil legacy P. New impact driven research is needed in order to create solutions for the sustainable management of soil P stocks.
Summary
Arbuscular mycorrhizal (AM) fungi‐associated hyphosphere microbiomes can be considered as the second genome of the mycorrhizal phosphorus uptake pathway. Their composition can be thought of ...as a stably recurring component of a holobiont, defined by the hyphosphere core microbiome, which is thought to benefit AM fungal fitness. Here, we review evidence indicating the existence of the hyphosphere core microbiome, highlight its functions linked to those functions lacking in AM fungi, and further explore the mechanisms by which different core members ensure their stable coexistence. We conclude that deciphering and utilizing the hyphosphere core microbiome provides an entry point for understanding the complex interactions among plants, AM fungi, and bacteria.
Intercropping is a farming practice involving two or more crop species, or genotypes, growing together and coexisting for a time. On the fringes of modern intensive agriculture, intercropping is ...important in many subsistence or low‐input/resource‐limited agricultural systems. By allowing genuine yield gains without increased inputs, or greater stability of yield with decreased inputs, intercropping could be one route to delivering ‘sustainable intensification’. We discuss how recent knowledge from agronomy, plant physiology and ecology can be combined with the aim of improving intercropping systems. Recent advances in agronomy and plant physiology include better understanding of the mechanisms of interactions between crop genotypes and species – for example, enhanced resource availability through niche complementarity. Ecological advances include better understanding of the context‐dependency of interactions, the mechanisms behind disease and pest avoidance, the links between above‐ and below‐ground systems, and the role of microtopographic variation in coexistence. This improved understanding can guide approaches for improving intercropping systems, including breeding crops for intercropping. Although such advances can help to improve intercropping systems, we suggest that other topics also need addressing. These include better assessment of the wider benefits of intercropping in terms of multiple ecosystem services, collaboration with agricultural engineering, and more effective interdisciplinary research.
Aims
The rhizosheath is defined as the weight of soil adhering strongly to roots on excavation, and current interest in this trait as a potential tolerance mechanism to abiotic stress has prompted us ...to explore the extent of its occurrence throughout the angiosperm phylogeny.
Methods
Here we describe a robust, novel method which was used to screen species for the presence/absence and strength of a rhizosheath. We correlate the latter with root hair length to provide insight into some of the factors affecting its formation. We go on to compare experimental data with previous observations in the literature.
Results
Results of a glasshouse screen demonstrate that rhizosheaths exist in species from many angiosperm orders, and the frequency of their occurrence and their strength and size are related. No correlation between root hair length and rhizosheath size was found, except when root hairs were extremely short, but the presence of root hairs was required for rhizosheath formation.
Conclusions
The rhizosheath is present in species from many angiosperm orders. Potential to enhance the trait is likely to exist in a range of crop species and could help contribute to future agricultural sustainability.
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