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Keywords:

  • Arbuscular mycorrhiza;
  • Fungal mycelium network;
  • Soil microbial ecology;
  • Interaction;
  • Rhizosphere and mycorrhizosphere

Abstract

  1. Top of page
  2. Abstract
  3. 1Introduction
  4. 2Interactions in the mycorrhizosphere
  5. 3From microcosm to field
  6. Acknowledgements
  7. References

Arbuscular mycorrhizal (AM) fungi interact with a wide variety of organisms during all stages of their life. Some of these interactions such as grazing of the external mycelium are detrimental, while others including interactions with plant growth promoting rhizobacteria (PG PR) promote mycorrhizal functioning. Following mycorrhizal colonisation the functions of the root become modified, with consequences for the rhizosphere community which is extended into the mycorrhizosphere due to the presence of the AM external mycelium. However, we still know relatively little of the ecology of AM fungi and, in particular, the mycelium network under natural conditions. This area merits attention in the future with emphasis on the fungal partner in the association rather than the plant which has been the focus in the past.


1Introduction

  1. Top of page
  2. Abstract
  3. 1Introduction
  4. 2Interactions in the mycorrhizosphere
  5. 3From microcosm to field
  6. Acknowledgements
  7. References

Mycorrhizal associations between a fungus and a plant root are ubiquitous in the natural environment. The associations themselves can be further classified into one of seven different types (i.e. arbuscular, ectomycorrhiza, ectendomycorrhiza, ericoid, arbutoid, orchid and monotropoid) based on the type of fungus involved and the range of resulting structures produced by the root–fungus combination (see [1]). Common to all types of mycorrhizal association, however, is the movement of carbon, generally, but not always, in the direction from plant to fungus. The association may not be obviously mutualistic at all points in time and this together with the range of functions thus far identified for the association (i.e. defence, nutrient uptake, soil aggregation stability, drought resistance) has posed problems in producing a clear definition to best describe the association. Currently, the most useful definition is perhaps that of “a sustainable non-pathogenic biotrophic interaction between a fungus and a root” as proposed by Fitter and Moyersoen [2], although this does not emphasise the importance of the presence of both intra- and extraradical mycelia in the association.

By far the most common type of association is that of the arbuscular mycorrhiza (AM). The AM association is the most ancient and probably aided the first land plants to colonise by scavenging for phosphate [3]. The AM association is so called because of the formation of highly branched intracellular fungal structures or ‘arbuscules’ which are believed to be the site of phosphate exchange between fungus and plant. Vesicles which contain lipids and are thought to be carbon storage structures may also form in some cases, although this will depend on the fungal symbiont as well as environmental conditions [1].

Approximately two-thirds of all land plants form the AM type of association, in sharp contrast with the relatively small numbers of fungi involved, all of which are members of the order Glomales (Zygomycotina) comprising only approximately 150 described taxa [1]. Consequently, the AM association is generally assumed to have no, or at least very low, specificity. More recently however, van der Heijden et al. [4] demonstrated that the biomass of several plant species in microcosms containing four native AM fungal taxa was approximately equal to biomass production in treatments that included the single fungal taxa that induced the largest growth response. This indicated that plants may be able to at least select the AM fungus which may benefit them the most. However, the bulk of knowledge of the AM symbiosis derives from microcosm experiments using a small number of plant and fungal taxa, and with little or no attention paid to the other soil biota with which they must interact. The purpose of this review is to focus on the ecology of the AM association in terms of interactions with other organisms and the implications of these interactions for mycorrhizal development and functioning.

2Interactions in the mycorrhizosphere

  1. Top of page
  2. Abstract
  3. 1Introduction
  4. 2Interactions in the mycorrhizosphere
  5. 3From microcosm to field
  6. Acknowledgements
  7. References

2.1Soil microbial interactions on AM fungi

Soil micro-organisms influence AM fungal development and symbiosis establishment but no clear pattern of response has been found: positive [5–7], negative [8,9] and neutral [10] interactions have all been reported. Negative impacts upon the AM fungi include a reduction in spore germination and hyphal length in the extramatrical stage, decreased root colonisation and a decline in the metabolic activity of the internal mycelium. Which effect is the more predominant has been found to be influenced by the timing of addition of the micro-organisms, the type of AM fungus present and the plant species which the AM fungus has colonised [9,11,12]. These factors together with the complex and dynamic nature of the soil environment mean that it is difficult to draw any useful generalisations. Indeed, even the same genus has been shown to have either a beneficial, negative or neutral effect upon AM fungi, as has been reported for both Trichoderma and Pseudomonas spp. [5,8,10,12–14]. Recent advances in both biochemical and molecular techniques should provide more useful insights into the nature of the interactions between AM fungi and other soil micro-organisms. For example, although the presence of Trichoderma harzianum decreased root colonisation and, when an organic nutrient source was added, external hyphal density of the AM fungus Glomus intraradices, the living AM mycelial biomass (measured as the content of a membrane fatty acid, PFLA16:1ω5) did not decrease nor did AM hyphal transport of 33P [15].

Positive influences on the AM symbiosis after addition of plant growth promoting rhizobacteria (PGPR), which include fluorescent pseudomonads and sporulating bacilli, are frequently reported. For example, dual inoculation of a PGPR (Pseudomonas putida) and an AM fungus induced an additive growth enhancement of subterranean clover when added together rather than singly [5]. Inoculation with the PGPR also increased root colonisation by the AM fungus initially (i.e. measured at 6 weeks) although later (at 12 weeks) colonisation levels were similar regardless of the presence of the PGPR [5]. Enhanced mycelial growth from Glomus mosseae spores by a PGPR has also been reported [16]. Thus, PGPR appear sometimes to promote both mycorrhizal development and functioning. In addition, the mycorrhizal and nodulated (i.e. Frankia, Rhizobium and Bradyrhizobium) symbioses are generally synergistic. It is believed that the AM symbiosis relieves P stress for the plant which in turn has benefits for the N2-fixing nitrogenase system of the other symbiont, resulting in enhanced fixation levels and consequently improved N status of the plant thus promoting plant growth and functioning which in turn also benefits mycorrhizal development (reviewed for legumes by [17]; see [18] for Frankia).

2.2AM influences on soil microbial interactions

Once mycorrhizal colonisation has occurred, subsequent exudation release by the root may be modified both through the mycorrhizal fungus acting as a considerable carbon sink for photoassimilate and through hyphal exudation. This may be expected to lead to changes in both the qualitative and quantitative release of exudates into the mycorrhizosphere. AM colonisation generally decreases root exudation [19] although not always [20] and may be influenced by the species of fungus present [21]. In addition, a reduction in sugar and amino acid release has been reported in some studies [19,22] but there is no clear pattern as to the consistency of this phenomenon. Similarly the reported impact on the mycorrhizosphere community is equally inconsistent with, for example, fluorescent pseudomonads showing a decrease, increase or no effect following AM colonisation [10,21,23,24]. Meyer and Linderman [25] observed no alteration in the total number of bacteria or actinomycetes isolated from the rhizosphere of Zea mays and Trifolium subterranean L. colonised by the AM fungus Glomus fasciculatum. However, there was a change in the functional groups of these organisms including more facultative anaerobic bacteria in the rhizosphere of AM colonised T. subterraneum but fewer fluorescent pseudomonads and chitinase-producing actinomycetes in the rhizosphere of AM-colonised Z. mays. The total number of bacteria isolated from the rhizoplane of both T. subterraneum and Z. mays increased as a result of AM colonisation although total numbers of actinomycetes were unaffected. In addition, leachates from Z. mays rhizosphere soil reduced production of zoospores and sporangia by Phytophthora cinnamomi when colonised by G. fasciculatum than non-mycorrhizal Z. mays rhizosphere leachates indicating a potential mechanism by which AM colonisation may aid pathogen resistance [25]. However, the chitinolytic producing actinomycete population may act as general biocontrol agents, thus, the reduction in this population may mean chitin containing pathogens become more important. Using three different AM fungi (Glomus etunicatum, Glomus mosseae or Gigaspora rosea) Schreiner et al. [26] observed differences in bacterial groups (i.e. Gram-negative or Gram-positive) depending on which fungus had colonised the roots of Glycine max L. (soybean). The AM fungus G. mosseae produced the greatest amount of external hyphae (i.e. 8.1 m g−1 soil). The other two AM fungi did not differ in the amount of external hyphae they produced but soil sampled from pots containing G. etunicatum had higher amounts of Gram-positive bacteria, measured as colony-forming units per g of dry soil, than corresponding samples from G. rosea. Soil from G. etunicatum pots also contained higher counts of Gram-negative bacteria than those counted from G. mosseae. These results would seem to imply that the hyphosphere (the volume of soil influenced by the external mycelium of the AM fungus) of different AM fungi may influence certain bacterial groups however, it should also be noted that where external mycelium production was greatest (i.e. in the case of G. mosseae) the influence on overall counts was less than from G. etunicatum which produced a less extensive mycelium. Indeed, low P status of the soil had a greater effect on total bacterial, and in particular Gram-positive, counts, than did mycorrhizal treatments. Alternatively, the more extensive mycelium could have inhibited bacterial populations as a means of reducing competition for nutrients in the mycorrhizosphere [15,24]. Other studies specifically testing the hyphosphere soil have found no quantitative change in bacterial numbers [27,28]. However, whereas Andrade et al. [27] found variations in bacterial composition which depended on the AM fungus present, Olsson et al. [28] found no such changes in composition or activities of the bacterial community.

Filion et al. [29] examined the release of soluble unidentified substances by the external mycelium of Glomus intraradices on the conidial germination of two fungi and the growth of two bacteria. Conidial germination of Trichoderma harzianum and growth of Pseudomonas chlororaphis were stimulated whereas growth of Clavibacter michiganensis subsp. michiganensis was unaffected and conidial germination of Fusarium oxysporum f.sp. chrysanthemi was reduced. These observed effects were generally correlated with the extract concentration. The authors [29] suggested that this was a possible means by which the AM mycelium may alter the microbial environment so that it was detrimental to pathogens. In contrast, Green et al. [15] also examining the interaction between G. intraradices and T. harzianum, observed no effect of the AM external mycelium on the population density of T. harzianum, except in the presence of an organic substrate when population densities and metabolic activity of T. harzianum were actually reduced. The differing results reported on the influence of AM fungi upon soil micro-organisms therefore are probably not only due to the type of AM fungus present but also the conditions, such as soil nutrient availability, in which the interaction is studied.

2.3Grazing of AM fungi

AM spores and external mycelium are subject to grazing by larger soil organisms such as collembola (or springtails), earthworms and mammals as well as other fungi and actinomycetes (see [30]). For example, although not their preferred food source [31], collembola can graze on the spores and extraradical mycelium of AM hyphae as shown by examination of their gut contents [32,33]. However, the feeding of the collembola Folsomia candida on an exclusive diet of the AM fungi Acaulospora spinosa, Scutellospora calospora and Gigaspora gigantea actually reduced the reproductive capacity of this collembola. In contrast, two other AM fungi (G. intraradices and G. etunicatum) although less palatable than T. harzianum were as profitable in terms of reproductive success [34]. Thus, although active grazing of AM fungal hyphae may not be an important feature under field conditions, collembola may reduce the effectiveness of the mycorrhizal symbiosis in other ways. For example, although the collembola F. candida did not actively graze on hyphae of the AM fungus G. intraradices, they did bite and sever the external AM hyphae from the root before grazing on their preferred food source (conidial fungal hyphae) present at the same time. This severing of AM hyphal networks was as much as 50% at the highest populations of collembola studied [35]. Although under some circumstances grazing by soil organisms such as earthworms, collembola and other organisms will be beneficial (e.g. as spores can survive ingestion thus grazing and deposition elsewhere will aid in dispersal) the grazing or cleavage of external hyphae may have more important consequences on the effectiveness of the mycorrhizal symbiosis [33]. The internal colonisation will remain intact and thus represent a carbon drain on the plant, but with reduced benefits due to a reduction in the external hyphal length. Re-establishment of the external mycelium will again require more plant carbon to be invested.

3From microcosm to field

  1. Top of page
  2. Abstract
  3. 1Introduction
  4. 2Interactions in the mycorrhizosphere
  5. 3From microcosm to field
  6. Acknowledgements
  7. References

The majority of the studies discussed above have involved investigating the interactions between soil micro-organisms and, generally, a single AM fungal inoculum added to microcosm units. Such studies are a first approximation to understanding the complex interactions which can occur using controlled conditions which would be impossible in the field. However, the ecology of AM in the field may be quite different. It certainly is more complex, with diversity of AM fungi in the root systems of plants ranging from two common taxa in an arable ecosystem to ca 11 in a woodland system [36] and ca 23 morphospecies being described from a single farm in Canada [4]. In an arable situation where plants are grown as crops then removed before re-sowing, the AM fungus is continually having to re-establish itself. This is similar to the situation in microcosm units where the fungal inoculum is generally added as colonised root fragments or spores, thus here also the AM fungus has to endure a period of development and establishment. Clearly however, other factors impact on AM formation in arable systems such as pesticide and fertiliser usage. However, in natural undisturbed ecosystems the fungus forms a permanent external mycelium network and plants are linked by a common mycelial network (CMN). This CMN probably becomes the primary source of inoculum by which plants become colonised. However, we know relatively little of the ecology of this network such as the distances to which it can extend, how many plants may be linked, the differing ability of AM fungal taxa to produce such networks and their interaction with each other let alone the interactions with the other soil biota. Some data are available, for example the spread of hyphae of G. fasciculatum through unplanted soil has been estimated to occur at a rate of 1.66 mm day−1[37] but again such estimates generally come from microcosm studies. In a field study, Chiariello et al. [38] applied 32P to the leaves of a donor Plantago erecta plant present in a serpentine annual grassland and detected high levels (i.e. >40% above background counts per min) in the shoots of neighbouring plants at a distance of ca 45 mm after 6–7 days. However, neither the type or size of the neighbouring plants nor the distance between donor and receiver were indicators of the amount of 32P transferred. Thus, there is an urgent need to investigate the ecology of the symbiosis under a range of field conditions in order to more fully understand the context dependence of the data obtained in relation to mycorrhizal functioning and the nature of the interactions with other soil biota.

For the plant, being linked into the CMN may help to reduce the uncertainty of soil heterogeneity with the fungal mycelium being able to locate, access and exploit the nutrient-rich zones or patches which occur naturally in all soils due to organic matter inputs (see [39]) more effectively than plant roots. It is well established that when roots of some plant species encounter such organic patches they proliferate roots within them [39]. This proliferation is believed to be a foraging response to the heterogeneous nature of the environment. AM fungi can also proliferate hyphae within nutrient-rich organic patches [40,41]. Allowing fungal hyphal proliferation instead would be more carbon cost efficient for the plant (see [42]). Furthermore, because of their size, AM fungal hyphae should be better able to compete with the indigenous soil biota for the microbially released nutrients. The AM fungi may also be able to access organic sources directly (i.e. without the prior need for microbial mineralisation) as has been demonstrated for nitrogen under both field [43] and laboratory conditions [44]. The importance and ubiquity of this uptake of intact organic compounds by AM fungi remains controversial (see [1]) and may depend on the competitive ability of AM fungi in comparison with the other soil biota present. However, the distances over which nutrients can effectively be transported among plants via the network may be small (see review by [45]). The reason why we know so little about the CMN is partially the difficulties associated with studying it particularly under field conditions. Furthermore, in the past most emphasis in mycorrhizal research has been placed upon the plant rather than the fungus or indeed the symbiotic state. This is particularly true in the AM association probably due to the essential role the plant plays in ensuring continued growth and functioning of the fungus. However, the fungus should not be out of mind. From the fungal viewpoint, the linking of plants by this CMN makes strategic sense. It allows fungal spread through the soil and maximises carbon capture by active colonisation of roots it encounters ensuring continued growth and activity. Future research emphasis needs to be placed on the fungal symbiont in the association adopting a more mycocentric approach as suggested by Fitter et al. [46].

Recent development of new techniques such as the stable-isotope probing method [47] and fluorescent in situ hybridization combined with microautoradiography [48] and tracking of labelled substrate uptake [49] now make it possible to directly follow the active populations of bacteria (rather than just culturable organisms) in soil. In addition, analysis of appropriately selected phospholipid fatty acid (PLFA) profiles can indicate the amount of fungal and bacterial biomass present and, when coupled with radio- or stable-isotope analysis, can indicate alterations in the activity of this biomass (see [15]). PLFA techniques have recently been used to investigate the interaction between AM fungi and other soil micro-organisms and have shown considerable promise [15,29]. These new methods in soil microbial ecology together with advances in molecular techniques to identify AM fungi both in colonised roots and the external phase mean that following AM fungal ecology and their interaction with the soil biota is now possible. Indeed, molecular methodologies have already shown that spore diversity found in the vicinity of the root is not readily translated into diversity found in the actual colonised root [50]. The combined application of these new techniques in the future should enable valuable insights into the ecological role of interacting groups of soil micro-organisms and AM fungi and their subsequent impact upon carbon dynamics and nutrient translocation under a range of differing soil, and ultimately field, conditions.

Acknowledgements

  1. Top of page
  2. Abstract
  3. 1Introduction
  4. 2Interactions in the mycorrhizosphere
  5. 3From microcosm to field
  6. Acknowledgements
  7. References

I am very grateful to Alastair Fitter for detailed comments and suggestions on earlier drafts. A.H. is funded by a BBSRC David Phillips Fellowship.

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  2. Abstract
  3. 1Introduction
  4. 2Interactions in the mycorrhizosphere
  5. 3From microcosm to field
  6. Acknowledgements
  7. References
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