Mutualistic fungi are reminiscent of parasitic fungi that live on other living organisms. In contrast to parasitism, mutualism benefits all involved organisms. The fungi will get nutrition, mainly carbohydrates, from their partners, but will also give something back to them. Below, different forms of mutualism found in fungi are explained with examples.
The rumen fungi (Neocallimastigomycota) occur in the gastrointestinal tracts of herbivore mammals such as reindeer. Here, they break down indigestible cellulose and hemicellulose found in leaves, twigs and lichens. In this way, the fungi get access to soluble carbohydrates (sugars) while they release the excess sugars together with amino acids and simple proteins. Those are now ready to be taken up in the gastrointestinal tract of the mammal. Without the fungi, these nutrients would have disappeared undigested in the faeces.
Another example of a symbiotic relationship of fungi are lichens. Lichens are composite organisms made up of fungi (usually Ascomycota) living in very close connection with green algae (Chlorophyta) and/or cyanobacteria. The latter two are photoautotrophs, providing the fungi with carbohydrates. The fungi, on the other hand, provide the photoautotrophic partners with protection, mineral nutrition and water. Lichens will not be dealt with in this chapter, but will be given a special treatment by Arve Elvebakk in the following chapter.
Endophytes are fungi growing inside the living tissue of higher plants. They get photosynthates from the plants, and the fungi are thought to protect the hosts from browsing by animals (vertebrates as well as insects and other invertebrates) and even from drought. Studies have shown that fungal endophytes are frequent in arctic environments. There seems to be an increase in colonisation by endophytes compared to arbuscular mycorrhizal fungi (see below) with latitude, indicating that endophytes are well adapted to a short growing season and that they are more successful symbionts than arbuscular mycorrhiza under adverse conditions.
One of the most important mutualistic associations between fungi and other organisms is mycorrhiza (Greek: μυκός = fungus, ριζα = root), where fungal hyphae and plant roots together form a functional unit. The photoautotrophic plants give soluble carbohydrates to the fungus, and the heterotrophic fungi pay back by providing the plant with water, phosphorus, nitrogen and other mineral nutrients. Although the roots are capable of taking up these nutrients themselves, the fungi do the job more effectively. Their thin, branched hyphae have a much larger surface/volume ratio compared to the thicker plant roots. Therefore, they have a much broader contact with soil particles. The fungi’s powerful enzymes and organic acids can break down complicated organic substances that are otherwise unavailable for the roots. Moreover, the fungi often produce hormones that protect against possible pathogenic organisms, which otherwise could attack the root system. About 80 % of all land plant species form associations with mycorrhizal fungi.
Within mycorrhiza we distiguish different types. Three are described here:
Arbuscular mycorrhiza (AM) are the most widespread and common mycorrhiza. The involved fungi belong to the order Glomales in Mucoromycota. It is the oldest type of mycorrhiza, and undoubted fossils are found from the Silurian period, about 430 million years ago. Arbuscular mycorrhizae were probably involved when plants established on land. The mycorrhiza is endotrophic, i.e. the hyphae penetrate the root cell walls without penetrating the cell membrane. Inside the cells, the hyphae develop densely branched arbuscles and, in some species, bladder shaped vesicles. The exchange of nutrients takes place at the arbuscles. The vesicles probably serve as storage organs. Sexual stages are not known, and the fungi spread with large (up to 500 µm in diameter) mitotic chlamydospores produced on hyphae outside the root system. Arbuscular mycorrhizae are efficient in taking up phosphorus from soils and bedrock, and are important for the turnover of this element in the ecosystem. Several different species of plants can establish AM with the same fungus organism, making it possible for them to exchange nutrients via the hyphae. On Svalbard, the AM-fungi hitherto reported are Glomus, Archaeospora and Claroideoglomus spp. Arbuscular mycorrhiza are found in non-ectomycorrhizal plants in the families Asteraceae, Poaceae, and Ranuculaceae. No associations are yet indicated between the abundances of AM structures in roots and the physical or chemical composition of the soil influencing the fungi as abiotic factor.
Ericoid mycorrhiza is the mutualistic association between plants in the heather family (Ericaceae) and fungi in order Helotiales (Ascomycota), especially the Hymenoscyphus ericae species aggregate. Ericoid mycorrhizae establish in very thin roots with swollen bark cells. On the outside of these cells, the hyphae run in a gel-like matrix (mucigel), and some of the hyphae penetrate the bark cells, without penetrating the membrane. Therefore, the mycorrhiza association is considered to be endotrophic. The fungi have the ability to break down complicated organic substances such as amino acids and oligopeptides in humus into mineral nutrients. These are provided to the plant roots. The most important mineral nutrient provided by the ericoid mycorrhiza fungi to the plant is nitrogen, but to a lower degree phosphorus and potassium are provided as well. Without these mutualistic fungi, the plant roots are only able to take up simple nitrogen compounds such as nitrate and ammonium.
Ectomycorrhiza (ECM) is crucial for the survival of ecologically important arctic scrubs such as Betula, Salix and Dryas, and the widespread herbaceous Bistorta vivipara. Ectomycorrhizal roots are characterised by three structural components:
- a sheath or mantle of densely packed hyphae, which encloses the root;
- a labyrinthine inward growth of hyphae, called the Hartig net, between the epidermal and cortical cells; and
- an outwardly growing system of hyphae, the extraradical or external mycelium, which form essential connections both with the soil and the sporocarps.
Mycorrhizal roots are easy to recognise since they are swollen, shortened and more branched than non-mycorrhizal roots. Depending on the higher plant or the fungal species, the mycorrhizal roots have different shapes, sizes, textures or colours. However, for a confident identification of the fungus on an ECM root, molecular methods are essential. The exchange of nutrients takes place between the hyphae of the Hartig net and the neighbouring root cells. Especially in areas with poor soils and/or cold climate, ECM significantly facilitates the uptake of water, nitrogen, phosphorus, calcium, magnesium, potassium and trace elements.
Only 3 % of seed plants, most of them woody, are ECM. However, their global importance is far greater than what one might expect, because of their disproportionate occupancy of large terrestrial land surface habitats such as the boreal taiga and the arctic or alpine tundra.
The fungi forming ECM do not belong to a phylogenetic entity, but are found in many Basidiomycota, some Ascomycota, and even Mucoromycota. This means that the ability to form EMC has developed several times during the evolution of the fungal kingdom. Several ECM fungi produce prominent sporocarps and belong to the conspicuous “mushrooms” found on arctic tundra, where the ECM Basidiomycota comprises genera as Lactarius (Russulales), Leccinum (Boletales), Laccaria, Cortinarius, Inocybe, Hebeloma, Naucoria (Agaricales). Ectomycorrhizal Ascomycota are encountered in the genus Helvella (which also comprises saprotrophic species). Moreover, many fungi with rare and/or inconspicuous sporocarps have recently been detected by molecular analysis of ECM roots from arctic sites. Important are the Basidiomycota Sebacina (Sebacinales), Thelephora and Tomentella (Thelephorales), and the Ascomycota Cenococcum geophilum. They have been vastly underrepresented in sporocarp investigations from the Arctic, but seem to have a high biomass in the soil. On the other hand, some groups with abundant fruiting, e.g. Lactarius and Russula, have been found in low numbers on ECM roots.
Fungi with dark septated hyphae have melanised cell walls and belong to the Ascomycota (e.g. Phialocephala, Cadophora and Leptodontidium). They are found on roots of plants with ectomycorrhizal fungi (see below), such as Dryas or Bistorta vivipara, but also on roots of many non-ectomycorrhizal plants. Ecologically, they constitute a heterogeneous group that functionally overlaps with saprotrophic soil fungi occurring on the root surface (rhizoplane-inhabiting fungi), pathogenic fungi, and mycorrhizal fungi. Melanins may protect the dark septate hyphae from extreme temperatures and drought, and so broaden the ecological niche of these fungi. This may explain why fungi with dark septated hyphae are so frequent in arctic areas.
The diversity of ECM fungi in the Arctic is surprisingly large compared to the low diversity of higher ECM host plants in this environment; Salix, Dryas, Betula and Bistorta vivipara. Nonetheless, these plants are among the more thermophilous species in Arctic climate. For instance, on Svalbard Betula nana is restricted to the climatically most favourable places along the south side of Isfjorden, whereas Salix polaris, Dryas octopetala and Bistorta vivipara are more or less frequent in areas with a summer warmth index above 6 ºC. Molecular data suggest that ECM host plants have re-colonised the Arctic post-glacially. The same is also the case for the ECM fungi. They may have been present during many previous interglacial periods, but were probably wiped out repeatedly by the glaciations and then re-colonised the Arctic areas several times.
The host specificity of ECM fungi is low, shown by molecular investigations of root systems of Salix, Dryas and Bistorta vivipara. No significant relationship was observed between the number of ECM fungi obtained per root system and host plant species. The most abundant order on the roots, irrespective of host species, was Agaricales followed by Thelephorales and Sebacinales.
Studies of ECM fungi on roots of Dryas on Svalbard have demonstrated an average of 7.5 taxa per plant root system in Ny-Ålesund and 6.5 in Longyearbyen. This is rather similar to the average amount of taxa found in mountains in mainland Norway (Tromsø and Finse). The number of root-associated fungal taxa on ECM plants does thus not seem to decline with increasing latitude, at least for Dryas. Moreover, even at a local scale there was little overlap in fungal taxa across root systems, indicating a lack of small-scale spatial structuring. A possible explanation is that plant root systems, together with the fungal mycelia, are three-dimensional, displaying a large fractal-like geometric structure. Both associated biotic factors such as soil microbes, as well as abiotic factors like minerals and water supply vary at micro scales in the soil surrounding the ECM-structure, both spatially and temporally. A high number of micro-niches are thus expected, explaining the high fungal diversity and the high degree of spatial turnover in fungal communities in arctic environments. A corresponding study of ECM on roots of Bistorta vivipara on Svalbard likewise found a lack of small-scale spatial structuring between individual root systems. However, there was a strong spatial component to the fungal community composition, with community similarity being highest within sites and regions, and with a weak structure along the latitudinal gradient. However, there was no spatial autocorrelation between sites, indicating that environmental factors are more important to community composition than spatial location.
The lack of small-scale spatial structuring suggests that ECM fungi in the Arctic do not usually form common mycelial networks across plant roots. Under marginal arctic conditions, the organismal energy budget is under pressure. Resources are primarily allocated to survival and reproduction rather than competition and therefore, host specialisation and the production of common mycelial networks may be too risky.
In this video you can see how the mycorrhizal partners recognise each other, which structures they are forming, and examples of plant-fungi mycorrhiza associations. Video created by the Helmtholtz Centre for Environmental Research.