Ectomycorrhizal extramatrical mycelium

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Ectomycorrhizas and short-distance extramatrical mycelium Myk Erbsenstreuling.jpg
Ectomycorrhizas and short-distance extramatrical mycelium

Ectomycorrhizal extramatrical mycelium (also known as extraradical mycelium) is the collection of filamentous fungal hyphae emanating from ectomycorrhizas. It may be composed of fine, hydrophilic hypha which branches frequently to explore and exploit the soil matrix or may aggregate to form rhizomorphs; highly differentiated, hydrophobic, enduring, transport structures.

Contents

Characteristics

Ectomycorrhizas on Picea glauca roots surrounded by extramatrical mycelium Mycorhizes-01.jpg
Ectomycorrhizas on Picea glauca roots surrounded by extramatrical mycelium

Overview

Apart from mycorrhizas, extramatrical mycelium is the primary vegetative body of ectomycorrhizal fungi. It is the location of mineral acquisition, [1] enzyme production, [2] and a key means of colonizing new root tips. [3] Extramatrical mycelium facilitates the movement of carbon into the rhizosphere, [4] moves carbon and nutrients between hosts [5] and is an important food source for invertebrates. [6]

Exploration type

The mycelial growth pattern, extent of biomass accumulation, and the presence or absence of rhizomorphs are used to classify fungi by exploration type. Agerer first proposed the designation of exploration types in 2001, [7] and the concept has since been widely employed in studies of ectomycorrhizal ecology. Four exploration types are commonly recognized: Contact, Short-distance, Medium-distance and Long-distance.

Contact exploration types possess a predominantly smooth mantle and lack rhizomorphs with ectomycorrhizas in close contact with the surrounding substrate. Short-distance exploration types also lack rhizomorphs but the mantle is surrounded by frequent projections of hyphae, which emanate a short distance into the surrounding substrate. Most ectomycorrhizal ascomycetes are included in this group.

Medium-distance exploration types are further divided into three subtypes defined by the growth range and differentiation of its rhizomorphs. Medium-distance Fringe form interconnected hyphal networks with rhizomorphs that divide and fuse repeatedly. Medium-distance Mat types form dense hyphal mats which aggregate into a homogeneous mass. Finally, the Medium-distance Smooth sub-type has rhizomorphs with smooth mantles and margins.

Fungal Hyphae Cells 1- Hyphal wall 2- Septum 3- Mitochondrion 4- Vacuole 5- Ergosterol crystal 6- Ribosome 7- Nucleus 8- Endoplasmic reticulum 9- Lipid body 10- Plasma membrane 11- Spitzenkorper/growth tip and vesicles 12- Golgi apparatus HYPHAE.png
Fungal Hyphae Cells 1- Hyphal wall 2- Septum 3- Mitochondrion 4- Vacuole 5- Ergosterol crystal 6- Ribosome 7- Nucleus 8- Endoplasmic reticulum 9- Lipid body 10- Plasma membrane 11- Spitzenkörper/growth tip and vesicles 12- Golgi apparatus

Long-distance exploration types are highly differentiated, forming rhizomorphs that contain hollow vessel-like transport tubes. Long distance types are associated with increased levels of organic nitrogen uptake compared to other exploration types and are thought to be less competitive in disturbed systems in contrast to short distance types which are able to regenerate more efficiently after a disturbance event. [8]

Exploration type is primarily consistent within a given lineage. However, some fungal genera which contain a large number of species have a great diversity of extramatrical hyphal morphology and are known to contain more than one exploration type. [9] Because of this, extrapolating exploration type to species known only by lineage is difficult. [10] Often, fungi fail to fit into a defined exploration type, falling instead along a gradient. Exploration type also fails to take into account other aspects of hyphal morphology, such as the extent to which hyphae cross into deeper soil horizons. [11]

Field studies have shown that extramatrical mycelium is more likely to proliferate in mineral soils than in organic material, and may be particularly absent in fresh leaf litter. [12] However, the presence of different ectomycorrhizal groups in different soil horizons suggest that different groups have evolved specialized niche separation, possibly attributable to exploration type. [13]

Ecological implications

Community assembly

Ectomycorrhizal Laccaria fruit bodies in forest community Laccaria, DOE.jpg
Ectomycorrhizal Laccaria fruit bodies in forest community

Because ectomycorrhizas are small and possess a limited contact area with the surrounding soil, the presence of extramatrical hyphae significantly increases the surface area in contact with the surrounding environment. Increased surface area means greater access to necessary nutrient sources. Additionally, the presence of rhizomorphs or mycelial cords, can act comparably to xylem tissue in plants, where hollow tubes of vessel hyphae shuttle water and solubilized nutrients over long distances. [14] The abundance and spatial distribution of host root tips in the rhizosphere is an important factor mediating ectomycorrhizal community assembly. Root density may select for the exploration types best suited for a given root spacing. In Pine systems, Fungi that display short-distance exploration types are less able to colonize new roots spaced far from the mycorrhiza, and long-distance types dominate areas of low root density. Conversely, short-distance exploration types tend to dominate areas of high root density where decreased carbon expenditure makes them more competitive than long-distance species. [15] The growth of extramatrical mycelium has a direct effect on the mutualistic nutrient trading between ectomycorrhizal fungi and their hosts. Increased hyphal occupation of the soil allows the fungus to take greater advantage of water and nutrients otherwise inaccessible to plant roots and to more efficiently transport these resources back to the plant. Conversely, the increased costs in carbon allocation associated with supporting a fungal partner with an extensive mycelial system presents a number of questions related to the costs and benefits of ectomycorrhizal mutualism. [16]

Carbon cycling

Although there is evidence that certain species of mycorrhizal fungi may obtain at least a portion of their carbon via saprotrophic nutrition, [17] the bulk of mycorrhizal carbon acquisition happens by way of trading for host-derived photosynthetic products. Mycorrhizal systems represent a major carbon sink. Laboratory studies predict that around 23% of plant-derived carbon is allocated to extrametrical mycelium, [18] although an estimated 15-30% of this is lost to fungal respiration. [19] [20] Carbon allocation is distributed unequally to extramatrical mycelium depending on fungal taxa, nutrient availability, and the age of the associated mycorrhizas. [21] [22] Much of the carbon allocated to extramatrical mycelium accumulates as fungal biomass, making up an estimated one-third of the total microbial biomass and one-half of the total dissolved organic carbon in some forest soils. [4] Carbon also supports the production of sporocarps and sclerotia, with various taxa investing differentially in these structures rather than in the proliferation of extramatrical mycelium. Carbon acquisition also goes toward the production of fungal exudates. Extramatrical hyphae excrete a range of compounds into the soil matrix, accounting for as much as 40% of total carbon usage. [23] These exudates are released primarily at the growing front, and are used in functions such as mineralization and homeostasis. [24]

Many researchers have attempted projections of the role that extramatrical mycelium may play in carbon sequestration. Although estimates of the life span of individual ectomycorrhizas very considerably, turnover is generally considered on a scale of months.

Cortinarius ectomycorrhizas and extramatrical mycelium on Pseudotsuga menziesii roots Ectomycorrhizae002.jpg
Cortinarius ectomycorrhizas and extramatrical mycelium on Pseudotsuga menziesii roots

After death, the presence ectomycorrhizas on root tips, may increase the rate of root decomposition for some fungal taxa. [25] Besides host plant death and mycorrhizal turnover, rates of carbon sequestration may also be affected by disturbances in the soil, which cause sections of the extramatrical mycelium to become severed from the host plant. Such disturbances, such as those caused by animal disruption, mycophagous invertebrates or habitat destruction, may have a notable impact on turnover rates. These variables make it difficult to estimate the turnover rates of mycorrhizal biomass in forest soils and the relative contribution of extramatrical mycelium to carbon sequestration.

Mycelial networks

The presence of long-distance extramatrical hyphae may affect forest health via the formation of common mycelial networks, in which hyphal connections form between plant hosts, located between the root cells of the host, can facilitate the transfer of carbon and nutrients between hosts. [26] While common mycelial networks (CMNs) allow for interplant carbon exchange primarily between photosynthetic plants, a number of non-photosynthetic plants have also adapted to participate in carbon transfer via CMNs. The extensive reach of the network beyond the roots of a plant enables the fungal hyphae to provide mineral nutrients to its host plant in exchange for carbon. [26]

Beyond facilitating nutrient transfer, CMNs have several other functions including compound signaling and plant-plant communication. [27] CMNs transfer warning signs of pathogen attacks between plants and allow newly developed roots to quickly become colonized by a fully functioning fungal mycelium. [28] CMNs connect many plants and stress-induced signals are transferred from the stress-inflicted plant to others, activating defense-related responses. These warning signals originate from the plant itself and proceed to the roots of the plant. From the roots, the signals enter the mycorrhizal fungi and travel through the network to relay warnings to other plants connected to the network. Mycelial networks may also be responsible for facilitating the transport of allelopathic chemicals from the supplying plant directly to the rhizosphere of other plants. [29] Ectomycorrhizal fungi increase primary production in host plants, with multi trophic effects. In this way, extramatrical mycelium is important to the maintenance of soil food webs, [6] supplying a significant nutritive source to invertebrates and microorganisms as well as overall plant competition and diversity.

While CMNs enable mutually beneficial connections between plants via nutrient transfer and defense warnings, these networks can also lead to unequal relationships between plants in which one benefits at the expense of the other. In a CMN shared between two plants, it is possible that one plant receives more nutrients from the network or supplies an unequal amount of carbon to mutual fungal hyphae, resulting in that plant species exploiting the network and gaining more than the other. Consequently, the other plant will be worse off due to the CMN connecting it to the exploitative plant. [26]

There are two types of mycorrhizal networks. Most plants are associated with arbuscular mycorrhizal fungi (AMF). AMF are able to form symbioses with several plant species and connect to roots of different hosts, allowing CMN. Mycelium networks function through signals that are first produced in plants, then move to the roots and then migrate to AMF. Then, signals go through the plant surface where they can be transported to leaves or other organs. Cells respond to these signals by forming a tube-like structure in preparation for the fungal hyphae. [30] Mycelia of AMF can link many plants across large areas.

The second type is ectomycorrhizal networks (ECMs). ECM fungi are extremely diverse, resulting in varied behaviors towards their plant hosts. Compared to AMFs, ECM are more diverse and form mainly in trees. ECMs mediate plant and tree nutrients by interrupting the sylvigenetic cycle during maturity. Because ECMs vary by tree, tree cutting and logging has shown a reduction in the ECM fungal community. Thus, creating imitations of ECMs in artificial ecosystems could be a solution for designing urban green spaces. [31]

Mineral access

Enzyme production

The enzymatic activities of ectomycorrhizal fungi are highly variable between species. These differences are correlated with exploration type (particularly the presence or absence of rhizomorphs) rather than lineage or host association- suggesting that similar morphologies of extraradical mycelium are an example of convergent evolution. [2] Differences in enzymatic activity, and hence the ability to degrade organic compounds dictate fungal nutrient access, with wide-ranging ecological implications.

Phosphorus

Because diverse ectomycorrhizal fungal taxa differ greatly in their metabolic activity [32] they also often differ in their capacity to trade nutrients with their hosts. [33] Phosphorus acquisition by mycorrhizal fungi, and the subsequent transfer to plant hosts, is thought to be one of the main functions of ectomycorrhizal symbiosis. Extramatrical mycelium is the site of collection for phosphorus within the soil system. This relationship is so strong that starving host plants of phosphorus is known to increase the growth of extramatrical mycelium tenfold. [34]

Nitrogen

Recently, Isotopic studies have been used to investigate relative trading between ectomycorrhizal fungi and plant hosts and to assess the relative importance of exploration type on nutrient trading ability. 15N values are elevated in ectomycorrhizal Fungi and depleted in fungal hosts, as a result of nutrient trading. [35] Fungal species with exploration types producing greater amounts of extraradical mycelium are known to accumulate greater amounts 15N [2] [36] in both root tips and fruit bodies, a phenomenon partially attributed to higher levels of N cycling within these species.

Assessment methods

Amanita phalloides mycelium Amanita phalloides.R.H. 17.jpg
Amanita phalloides mycelium

Determining the longevity of extramatrical mycelium is difficult, and estimates range from just a few months to several years. Turnover rates are assessed in a variety of ways including direct observation and 14 C dating. Such estimates are an important variable in calculating the contribution that ectomycorrhizal fungi have to carbon sequestration. [37] In order to differentiate ectomycorrhizal mycelium from the mycelium of saprotrophic fungi, biomass estimates are often done by ergosterol or phospholipid fatty acid analysis, or by using sand-filled bags, which are likely to be avoided by saprotrophic fungi because they lack organic matter. [37] Detailed morphological characterization of exploration type has been defined for over 550 different ectomycorrhizal species and are compiled in www. deemy. de. Due to the difficulty in classifying exploration types of intermediate forms, other metrics have been proposed to qualify and quantify the growth of extramatrical mycelium, including Specific Actual/Potential Mycelium Space Occupation and Specific Extramatrical Mycelial Length [38] which attempt to account for the contributions of mycelial density, surface area and total biomass.

Related Research Articles

<span class="mw-page-title-main">Mycelium</span> Vegetative part of a fungus

Mycelium is a root-like structure of a fungus consisting of a mass of branching, thread-like hyphae. Its normal form is that of branched, slender, entangled, anastomosing, hyaline threads. Fungal colonies composed of mycelium are found in and on soil and many other substrates. A typical single spore germinates into a monokaryotic mycelium, which cannot reproduce sexually; when two compatible monokaryotic mycelia join and form a dikaryotic mycelium, that mycelium may form fruiting bodies such as mushrooms. A mycelium may be minute, forming a colony that is too small to see, or may grow to span thousands of acres as in Armillaria.

<span class="mw-page-title-main">Hypha</span> Long, filamentous structure in fungi and Actinobacteria

A hypha is a long, branching, filamentous structure of a fungus, oomycete, or actinobacterium. In most fungi, hyphae are the main mode of vegetative growth, and are collectively called a mycelium.

<span class="mw-page-title-main">Mycorrhiza</span> Fungus-plant symbiotic association

A mycorrhiza is a symbiotic association between a fungus and a plant. The term mycorrhiza refers to the role of the fungus in the plant's rhizosphere, its root system. Mycorrhizae play important roles in plant nutrition, soil biology, and soil chemistry.

<span class="mw-page-title-main">Russulaceae</span> Family of fungi in the order Russulales

The Russulaceae are a diverse family of fungi in the order Russulales, with roughly 1,900 known species and a worldwide distribution. They comprise the brittlegills and the milk-caps, well-known mushroom-forming fungi that include some edible species. These gilled mushrooms are characterised by the brittle flesh of their fruitbodies.

<span class="mw-page-title-main">Arbuscular mycorrhiza</span> Symbiotic penetrative association between a fungus and the roots of a vascular plant

An arbuscular mycorrhiza (AM) is a type of mycorrhiza in which the symbiont fungus penetrates the cortical cells of the roots of a vascular plant forming arbuscules. Arbuscular mycorrhiza is a type of endomycorrhiza along with ericoid mycorrhiza and orchid mycorrhiza. They are characterized by the formation of unique tree-like structures, the arbuscules. In addition, globular storage structures called vesicles are often encountered.

<span class="mw-page-title-main">Myco-heterotrophy</span> Symbiotism between certain parasitic plants and fungi

Myco-heterotrophy is a symbiotic relationship between certain kinds of plants and fungi, in which the plant gets all or part of its food from parasitism upon fungi rather than from photosynthesis. A myco-heterotroph is the parasitic plant partner in this relationship. Myco-heterotrophy is considered a kind of cheating relationship and myco-heterotrophs are sometimes informally referred to as "mycorrhizal cheaters". This relationship is sometimes referred to as mycotrophy, though this term is also used for plants that engage in mutualistic mycorrhizal relationships.

<span class="mw-page-title-main">Ericoid mycorrhiza</span> Species of fungus

The ericoid mycorrhiza is a mutualistic relationship formed between members of the plant family Ericaceae and several lineages of mycorrhizal fungi. This symbiosis represents an important adaptation to acidic and nutrient poor soils that species in the Ericaceae typically inhabit, including boreal forests, bogs, and heathlands. Molecular clock estimates suggest that the symbiosis originated approximately 140 million years ago.

<i>Rhizopogon</i> Genus of fungi

Rhizopogon is a genus of ectomycorrhizal basidiomycetes in the family Rhizopogonaceae. Species form hypogeous sporocarps commonly referred to as "false truffles". The general morphological characters of Rhizopogon sporocarps are a simplex or duplex peridium surrounding a loculate gleba that lacks a columnella. Basidiospores are produced upon basidia that are borne within the fungal hymenium that coats the interior surface of gleba locules. The peridium is often adorned with thick mycelial cords, also known as rhizomorphs, that attach the sporocarp to the surrounding substrate. The scientific name Rhizopogon is Greek for 'root' (Rhiz-) 'beard' (-pogon) and this name was given in reference to the rhizomorphs found on sporocarps of many species.

<span class="mw-page-title-main">Mycelial cord</span> Structure produced by fungi

Mycelial cords are linear aggregations of parallel-oriented hyphae. The mature cords are composed of wide, empty vessel hyphae surrounded by narrower sheathing hyphae. Cords may look similar to plant roots, and also frequently have similar functions; hence they are also called rhizomorphs. As well as growing underground or on the surface of trees and other plants, some fungi make mycelial cords which hang in the air from vegetation.

<span class="mw-page-title-main">Hartig net</span> Network of inward-growing hyphae

The Hartig net is the network of inward-growing hyphae, that extends into the plant host root, penetrating between plant cells in the root epidermis and cortex in ectomycorrhizal symbiosis. This network is the internal component of fungal morphology in ectomycorrhizal symbiotic structures formed with host plant roots, in addition to a hyphal mantle or sheath on the root surface, and extramatrical mycelium extending from the mantle into the surrounding soil. The Hartig net is the site of mutualistic resource exchange between the fungus and the host plant. Essential nutrients for plant growth are acquired from the soil by exploration and foraging of the extramatrical mycelium, then transported through the hyphal network across the mantle and into the Hartig net, where they are released by the fungi into the root apoplastic space for uptake by the plant. The hyphae in the Hartig net acquire sugars from the plant root, which are transported to the external mycelium to provide a carbon source to sustain fungal growth.

Nitrogen nutrition in the arbuscular mycorrhizal system refers to...

<i>Tricholoma vaccinum</i> Fungus of the agaric genus Tricholoma

Tricholoma vaccinum, commonly known as the russet scaly tricholoma, the scaly knight, or the fuzztop, is a fungus of the agaric genus Tricholoma. It produces medium-sized fruit bodies (mushrooms) that have a distinctive hairy reddish-brown cap with a shaggy margin when young. The cap, which can reach a diameter of up to 6.5 cm (2.6 in) wide, breaks up into flattened scales in maturity. It has cream-buff to pinkish gills with brown spots. Its fibrous, hollow stipe is white above and reddish brown below, and measures 4 to 7.5 cm long. Although young fruit bodies have a partial veil, it does not leave a ring on the stipe.

The mycorrhizosphere is the region around a mycorrhizal fungus in which nutrients released from the fungus increase the microbial population and its activities. The roots of most terrestrial plants, including most crop plants and almost all woody plants, are colonized by mycorrhiza-forming symbiotic fungi. In this relationship, the plant roots are infected by a fungus, but the rest of the fungal mycelium continues to grow through the soil, digesting and absorbing nutrients and water and sharing these with its plant host. The fungus in turn benefits by receiving photosynthetic sugars from its host. The mycorrhizosphere consists of roots, hyphae of the directly connected mycorrhizal fungi, associated microorganisms, and the soil in their direct influence.

<span class="mw-page-title-main">Mycorrhizal network</span> Underground fungal networks that connect individual plants together

A mycorrhizal network is an underground network found in forests and other plant communities, created by the hyphae of mycorrhizal fungi joining with plant roots. This network connects individual plants together. Mycorrhizal relationships are most commonly mutualistic, with both partners benefiting, but can be commensal or parasitic, and a single partnership may change between any of the three types of symbiosis at different times.

<span class="mw-page-title-main">Mycorrhizal fungi and soil carbon storage</span> Terrestrial ecosystem

Soil carbon storage is an important function of terrestrial ecosystems. Soil contains more carbon than plants and the atmosphere combined. Understanding what maintains the soil carbon pool is important to understand the current distribution of carbon on Earth, and how it will respond to environmental change. While much research has been done on how plants, free-living microbial decomposers, and soil minerals affect this pool of carbon, it is recently coming to light that mycorrhizal fungi—symbiotic fungi that associate with roots of almost all living plants—may play an important role in maintaining this pool as well. Measurements of plant carbon allocation to mycorrhizal fungi have been estimated to be 5 to 20% of total plant carbon uptake, and in some ecosystems the biomass of mycorrhizal fungi can be comparable to the biomass of fine roots. Recent research has shown that mycorrhizal fungi hold 50 to 70 percent of the total carbon stored in leaf litter and soil on forested islands in Sweden. Turnover of mycorrhizal biomass into the soil carbon pool is thought to be rapid and has been shown in some ecosystems to be the dominant pathway by which living carbon enters the soil carbon pool.

<span class="mw-page-title-main">Ectomycorrhiza</span> Non-penetrative symbiotic association between a fungus and the roots of a vascular plant

An ectomycorrhiza is a form of symbiotic relationship that occurs between a fungal symbiont, or mycobiont, and the roots of various plant species. The mycobiont is often from the phyla Basidiomycota and Ascomycota, and more rarely from the Zygomycota. Ectomycorrhizas form on the roots of around 2% of plant species, usually woody plants, including species from the birch, dipterocarp, myrtle, beech, willow, pine and rose families. Research on ectomycorrhizas is increasingly important in areas such as ecosystem management and restoration, forestry and agriculture.

<i>Cenococcum geophilum</i> Species of fungus

Cenococcum geophilum Fr., synonym Cenococcum graniforme (Sow.) Ferd. and Winge, is an Ascomycete fungal species and is the only member in the genus Cenococcum. It is one of the most common ectomycorrhizal fungal species encountered in forest ecosystems. The geographic distribution of the species is notably cosmopolitan; it is found in ecosystems with a wide range of environmental conditions, and in many cases in high relative frequency. Because of its wide distribution and abundance in forest soils, it is one of the most well-studied ectomycorrhizal fungal species. While the species has long been known to be sterile and not produce asexual or sexual spores, cryptic sexual stages may exist. The hyphae produced by C. geophilum are characterized by their thick (1.5-8 um), straight and jet black appearance with little branching. They usually form monopodial (unbranched) ectomycorrhizas. The mantles of C. geophilum ectomycorrhizas are usually thick with few to many emanating hyphae.

Dark septate endophytes (DSE) are a group of endophytic fungi characterized by their morphology of melanized, septate, hyphae. This group is likely paraphyletic, and contain conidial as well as sterile fungi that colonize roots intracellularly or intercellularly. Very little is known about the number of fungal taxa within this group, but all are in the Ascomycota. They are found in over 600 plant species and across 114 families of angiosperms and gymnosperms and co-occur with other types of mycorrhizal fungi. They have a wide global distribution and can be more abundant in stressed environments. Much of their taxonomy, physiology, and ecology are unknown.

Orchid mycorrhizae are endomycorrhizal fungi which develop symbiotic relationships with the roots and seeds of plants of the family Orchidaceae. Nearly all orchids are myco-heterotrophic at some point in their life cycle. Orchid mycorrhizae are critically important during orchid germination, as an orchid seed has virtually no energy reserve and obtains its carbon from the fungal symbiont.

<span class="mw-page-title-main">Mycorrhiza helper bacteria</span> Group of organisms

Mycorrhiza helper bacteria (MHB) are a group of organisms that form symbiotic associations with both ectomycorrhiza and arbuscular mycorrhiza. MHBs are diverse and belong to a wide variety of bacterial phyla including both Gram-negative and Gram-positive bacteria. Some of the most common MHBs observed in studies belong to the phylas Pseudomonas and Streptomyces. MHBs have been seen to have extremely specific interactions with their fungal hosts at times, but this specificity is lost with plants. MHBs enhance mycorrhizal function, growth, nutrient uptake to the fungus and plant, improve soil conductance, aid against certain pathogens, and help promote defense mechanisms. These bacteria are naturally present in the soil, and form these complex interactions with fungi as plant root development starts to take shape. The mechanisms through which these interactions take shape are not well-understood and needs further study.

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