MiniReview

Microbial ecology of the arbuscular mycorrhiza

Angela Hodge *Department of Biology, The University of York, P.O. Box 373, York YO10 5YW, UK

Received 14 January 2000; received in revised form 13 March 2000; accepted 14 March 2000

Abstract

Arbuscular mycorrhizal (AM) fungi interact with a wide variety of organisms during all stages of their life. Some of these interactionssuch as grazing of the external mycelium are detrimental, while others including interactions with plant growth promoting rhizobacteria (PGPR) promote mycorrhizal functioning. Following mycorrhizal colonisation the functions of the root become modified, with consequencesfor the rhizosphere community which is extended into the mycorrhizosphere due to the presence of the AM external mycelium. However, westill know relatively little of the ecology of AM fungi and, in particular, the mycelium network under natural conditions. This area meritsattention in the future with emphasis on the fungal partner in the association rather than the plant which has been the focus in thepast. ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.

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

1. Introduction

Mycorrhizal associations between a fungus and a plantroot are ubiquitous in the natural environment. The asso-ciations themselves can be further classi¢ed into one ofseven di¡erent types (i.e. arbuscular, ectomycorrhiza, ec-tendomycorrhiza, ericoid, arbutoid, orchid and monotro-poid) based on the type of fungus involved and the rangeof resulting structures produced by the root^fungus com-bination (see [1]). Common to all types of mycorrhizalassociation, however, is the movement of carbon, gener-ally, but not always, in the direction from plant to fungus.The association may not be obviously mutualistic at allpoints in time and this together with the range of func-tions thus far identi¢ed for the association (i.e. defence,nutrient uptake, soil aggregation stability, drought resis-tance) has posed problems in producing a clear de¢nitionto best describe the association. Currently, the most usefulde¢nition is perhaps that of ``a sustainable non-pathogenicbiotrophic interaction between a fungus and a root'' asproposed by Fitter and Moyersoen [2], although thisdoes not emphasise the importance of the presence ofboth intra- and extraradical mycelia in the association.

By far the most common type of association is that ofthe arbuscular mycorrhiza (AM). The AM association is

the most ancient and probably aided the ¢rst land plantsto colonise by scavenging for phosphate [3]. The AM as-sociation is so called because of the formation of highlybranched intracellular fungal structures or `arbuscules'which are believed to be the site of phosphate exchangebetween fungus and plant. Vesicles which contain lipidsand are thought to be carbon storage structures mayalso form in some cases, although this will depend onthe fungal symbiont as well as environmental conditions[1].

Approximately two-thirds of all land plants form theAM type of association, in sharp contrast with the rela-tively small numbers of fungi involved, all of which aremembers of the order Glomales (Zygomycotina) compris-ing only approximately 150 described taxa [1]. Conse-quently, the AM association is generally assumed tohave no, or at least very low, speci¢city. More recentlyhowever, van der Heijden et al. [4] demonstrated thatthe biomass of several plant species in microcosms con-taining four native AM fungal taxa was approximatelyequal to biomass production in treatments that includedthe single fungal taxa that induced the largest growth re-sponse. This indicated that plants may be able to at leastselect the AM fungus which may bene¢t them the most.However, the bulk of knowledge of the AM symbiosisderives from microcosm experiments using a small numberof plant and fungal taxa, and with little or no attentionpaid to the other soil biota with which they must interact.The purpose of this review is to focus on the ecology of

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* Tel. : +44 (1904) 432878; Fax: +44 (1904) 432860;E-mail : ah29@york.ac.uk

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the AM association in terms of interactions with otherorganisms and the implications of these interactions formycorrhizal development and functioning.

2. Interactions in the mycorrhizosphere

2.1. Soil microbial interactions on AM fungi

Soil micro-organisms in£uence AM fungal developmentand symbiosis establishment but no clear pattern of re-sponse has been found: positive [5^7], negative [8,9] andneutral [10] interactions have all been reported. Negativeimpacts upon the AM fungi include a reduction in sporegermination and hyphal length in the extramatrical stage,decreased root colonisation and a decline in the metabolicactivity of the internal mycelium. Which e¡ect is the morepredominant has been found to be in£uenced by the tim-ing of addition of the micro-organisms, the type of AMfungus present and the plant species which the AM fungushas colonised [9,11,12]. These factors together with thecomplex and dynamic nature of the soil environmentmean that it is di¤cult to draw any useful generalisations.Indeed, even the same genus has been shown to have ei-ther a bene¢cial, negative or neutral e¡ect upon AM fungi,as has been reported for both Trichoderma and Pseudomo-nas spp. [5,8,10,12^14]. Recent advances in both biochem-ical and molecular techniques should provide more usefulinsights into the nature of the interactions between AMfungi and other soil micro-organisms. For example,although the presence of Trichoderma harzianum decreasedroot colonisation and, when an organic nutrient sourcewas added, external hyphal density of the AM fungusGlomus intraradices, the living AM mycelial biomass(measured as the content of a membrane fatty acid,PFLA16:1g5) did not decrease nor did AM hyphal trans-port of 33P [15].

Positive in£uences on the AM symbiosis after additionof plant growth promoting rhizobacteria (PGPR), whichinclude £uorescent pseudomonads and sporulating bacilli,are frequently reported. For example, dual inoculation ofa PGPR (Pseudomonas putida) and an AM fungus inducedan additive growth enhancement of subterranean cloverwhen added together rather than singly [5]. Inoculationwith the PGPR also increased root colonisation by theAM fungus initially (i.e. measured at 6 weeks) althoughlater (at 12 weeks) colonisation levels were similar regard-less of the presence of the PGPR [5]. Enhanced mycelialgrowth from Glomus mosseae spores by a PGPR has alsobeen reported [16]. Thus, PGPR appear sometimes to pro-mote both mycorrhizal development and functioning. Inaddition, the mycorrhizal and nodulated (i.e. Frankia, Rhi-zobium and Bradyrhizobium) symbioses are generally syn-ergistic. It is believed that the AM symbiosis relieves Pstress for the plant which in turn has bene¢ts for theN2-¢xing nitrogenase system of the other symbiont, result-

ing in enhanced ¢xation levels and consequently improvedN status of the plant thus promoting plant growth andfunctioning which in turn also bene¢ts mycorrhizal devel-opment (reviewed for legumes by [17]; see [18] for Frank-ia).

2.2. AM in£uences on soil microbial interactions

Once mycorrhizal colonisation has occurred, subsequentexudation release by the root may be modi¢ed boththrough the mycorrhizal fungus acting as a considerablecarbon sink for photoassimilate and through hyphal exu-dation. This may be expected to lead to changes in boththe qualitative and quantitative release of exudates intothe mycorrhizosphere. AM colonisation generally de-creases root exudation [19] although not always [20] andmay be in£uenced by the species of fungus present [21]. Inaddition, a reduction in sugar and amino acid release hasbeen reported in some studies [19,22] but there is no clearpattern as to the consistency of this phenomenon. Simi-larly the reported impact on the mycorrhizosphere com-munity is equally inconsistent with, for example, £uores-cent pseudomonads showing a decrease, increase or noe¡ect following AM colonisation [10,21,23,24]. Meyerand Linderman [25] observed no alteration in the totalnumber of bacteria or actinomycetes isolated from therhizosphere of Zea mays and Trifolium subterranean L.colonised by the AM fungus Glomus fasciculatum. How-ever, there was a change in the functional groups of theseorganisms including more facultative anaerobic bacteria inthe rhizosphere of AM colonised T. subterraneum but few-er £uorescent pseudomonads and chitinase-producing ac-tinomycetes in the rhizosphere of AM-colonised Z. mays.The total number of bacteria isolated from the rhizoplaneof both T. subterraneum and Z. mays increased as a resultof AM colonisation although total numbers of actinomy-cetes were una¡ected. In addition, leachates from Z. maysrhizosphere soil reduced production of zoospores andsporangia by Phytophthora cinnamomi when colonised byG. fasciculatum than non-mycorrhizal Z. mays rhizosphereleachates indicating a potential mechanism by which AMcolonisation may aid pathogen resistance [25]. However,the chitinolytic producing actinomycete population mayact as general biocontrol agents, thus, the reduction inthis population may mean chitin containing pathogens be-come more important. Using three di¡erent AM fungi(Glomus etunicatum, Glomus mosseae or Gigaspora rosea)Schreiner et al. [26] observed di¡erences in bacterialgroups (i.e. Gram-negative or Gram-positive) dependingon which fungus had colonised the roots of Glycine maxL. (soybean). The AM fungus G. mosseae produced thegreatest amount of external hyphae (i.e. 8.1 m g31 soil).The other two AM fungi did not di¡er in the amount ofexternal hyphae they produced but soil sampled from potscontaining G. etunicatum had higher amounts of Gram-positive bacteria, measured as colony-forming units per g

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of dry soil, than corresponding samples from G. rosea. Soilfrom G. etunicatum pots also contained higher counts ofGram-negative bacteria than those counted from G. mos-seae. These results would seem to imply that the hypho-sphere (the volume of soil in£uenced by the external my-celium of the AM fungus) of di¡erent AM fungi mayin£uence certain bacterial groups however, it should alsobe noted that where external mycelium production wasgreatest (i.e. in the case of G. mosseae) the in£uence onoverall counts was less than from G. etunicatum whichproduced a less extensive mycelium. Indeed, low P statusof the soil had a greater e¡ect on total bacterial, and inparticular Gram-positive, counts, than did mycorrhizaltreatments. Alternatively, the more extensive myceliumcould have inhibited bacterial populations as a means ofreducing competition for nutrients in the mycorrhizo-sphere [15,24]. Other studies speci¢cally testing the hypho-sphere soil have found no quantitative change in bacterialnumbers [27,28]. However, whereas Andrade et al. [27]found variations in bacterial composition which dependedon the AM fungus present, Olsson et al. [28] found nosuch changes in composition or activities of the bacterialcommunity.

Filion et al. [29] examined the release of soluble uniden-ti¢ed substances by the external mycelium of Glomus intra-radices on the conidial germination of two fungi and thegrowth of two bacteria. Conidial germination of Tricho-derma harzianum and growth of Pseudomonas chlororaphiswere stimulated whereas growth of Clavibacter michiga-nensis subsp. michiganensis was una¡ected and conidialgermination of Fusarium oxysporum f.sp. chrysanthemiwas reduced. These observed e¡ects were generally corre-lated with the extract concentration. The authors [29] sug-gested that this was a possible means by which the AMmycelium may alter the microbial environment so that itwas detrimental to pathogens. In contrast, Green et al. [15]also examining the interaction between G. intraradices andT. harzianum, observed no e¡ect of the AM external my-celium on the population density of T. harzianum, exceptin the presence of an organic substrate when populationdensities and metabolic activity of T. harzianum were ac-tually reduced. The di¡ering results reported on the in£u-ence of AM fungi upon soil micro-organisms therefore areprobably not only due to the type of AM fungus presentbut also the conditions, such as soil nutrient availability,in which the interaction is studied.

2.3. Grazing of AM fungi

AM spores and external mycelium are subject to grazingby larger soil organisms such as collembola (or spring-tails), earthworms and mammals as well as other fungiand actinomycetes (see [30]). For example, although nottheir preferred food source [31], collembola can graze onthe spores and extraradical mycelium of AM hyphae asshown by examination of their gut contents [32,33]. How-

ever, the feeding of the collembola Folsomia candida on anexclusive diet of the AM fungi Acaulospora spinosa, Scu-tellospora calospora and Gigaspora gigantea actually re-duced the reproductive capacity of this collembola. Incontrast, two other AM fungi (G. intraradices and G. etu-nicatum) although less palatable than T. harzianum were aspro¢table in terms of reproductive success [34]. Thus,although active grazing of AM fungal hyphae may notbe an important feature under ¢eld conditions, collembolamay reduce the e¡ectiveness of the mycorrhizal symbiosisin other ways. For example, although the collembolaF. candida did not actively graze on hyphae of the AMfungus G. intraradices, they did bite and sever the externalAM hyphae from the root before grazing on their pre-ferred food source (conidial fungal hyphae) present atthe same time. This severing of AM hyphal networkswas as much as 50% at the highest populations of collem-bola studied [35]. Although under some circumstancesgrazing by soil organisms such as earthworms, collembolaand other organisms will be bene¢cial (e.g. as spores cansurvive ingestion thus grazing and deposition elsewherewill aid in dispersal) the grazing or cleavage of externalhyphae may have more important consequences on thee¡ectiveness of the mycorrhizal symbiosis [33]. The inter-nal colonisation will remain intact and thus represent acarbon drain on the plant, but with reduced bene¢ts dueto a reduction in the external hyphal length. Re-establish-ment of the external mycelium will again require moreplant carbon to be invested.

3. From microcosm to ¢eld

The majority of the studies discussed above have in-volved investigating the interactions between soil micro-organisms and, generally, a single AM fungal inoculumadded to microcosm units. Such studies are a ¢rst approx-imation to understanding the complex interactions whichcan occur using controlled conditions which would be im-possible in the ¢eld. However, the ecology of AM in the¢eld may be quite di¡erent. It certainly is more complex,with diversity of AM fungi in the root systems of plantsranging from two common taxa in an arable ecosystem toca 11 in a woodland system [36] and ca 23 morphospeciesbeing described from a single farm in Canada [4]. In anarable situation where plants are grown as crops thenremoved before re-sowing, the AM fungus is continuallyhaving to re-establish itself. This is similar to the situationin microcosm units where the fungal inoculum is generallyadded as colonised root fragments or spores, thus herealso the AM fungus has to endure a period of develop-ment and establishment. Clearly however, other factorsimpact on AM formation in arable systems such as pesti-cide and fertiliser usage. However, in natural undisturbedecosystems the fungus forms a permanent external myce-lium network and plants are linked by a common mycelial

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network (CMN). This CMN probably becomes the pri-mary source of inoculum by which plants become colon-ised. However, we know relatively little of the ecology ofthis network such as the distances to which it can extend,how many plants may be linked, the di¡ering ability ofAM fungal taxa to produce such networks and their in-teraction with each other let alone the interactions withthe other soil biota. Some data are available, for examplethe spread of hyphae of G. fasciculatum through unplantedsoil has been estimated to occur at a rate of 1.66 mmday31 [37] but again such estimates generally come frommicrocosm studies. In a ¢eld study, Chiariello et al. [38]applied 32P to the leaves of a donor Plantago erecta plantpresent in a serpentine annual grassland and detected highlevels (i.e. s 40% above background counts per min) inthe shoots of neighbouring plants at a distance of ca 45mm after 6^7 days. However, neither the type or size ofthe neighbouring plants nor the distance between donorand receiver were indicators of the amount of 32P trans-ferred. Thus, there is an urgent need to investigate theecology of the symbiosis under a range of ¢eld conditionsin order to more fully understand the context dependenceof the data obtained in relation to mycorrhizal functioningand the nature of the interactions with other soil biota.

For the plant, being linked into the CMN may help toreduce the uncertainty of soil heterogeneity with the fungalmycelium being able to locate, access and exploit the nu-trient-rich zones or patches which occur naturally in allsoils due to organic matter inputs (see [39]) more e¡ec-tively than plant roots. It is well established that whenroots of some plant species encounter such organic patchesthey proliferate roots within them [39]. This proliferationis believed to be a foraging response to the heterogeneousnature of the environment. AM fungi can also proliferatehyphae within nutrient-rich organic patches [40,41]. Al-lowing fungal hyphal proliferation instead would bemore carbon cost e¤cient for the plant (see [42]). Further-more, because of their size, AM fungal hyphae should bebetter able to compete with the indigenous soil biota forthe microbially released nutrients. The AM fungi may alsobe able to access organic sources directly (i.e. without theprior need for microbial mineralisation) as has been dem-onstrated for nitrogen under both ¢eld [43] and laboratoryconditions [44]. The importance and ubiquity of this up-take of intact organic compounds by AM fungi remainscontroversial (see [1]) and may depend on the competitiveability of AM fungi in comparison with the other soilbiota present. However, the distances over which nutrientscan e¡ectively be transported among plants via the net-work may be small (see review by [45]). The reason whywe know so little about the CMN is partially the di¤cul-ties associated with studying it particularly under ¢eldconditions. Furthermore, in the past most emphasis inmycorrhizal research has been placed upon the plantrather 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 con-tinued growth and functioning of the fungus. However,the fungus should not be out of mind. From the fungalviewpoint, the linking of plants by this CMN makes stra-tegic sense. It allows fungal spread through the soil andmaximises carbon capture by active colonisation of rootsit encounters ensuring continued growth and activity. Fu-ture research emphasis needs to be placed on the fungalsymbiont in the association adopting a more mycocentricapproach as suggested by Fitter et al. [46].

Recent development of new techniques such as the sta-ble-isotope probing method [47] and £uorescent in situhybridization combined with microautoradiography [48]and tracking of labelled substrate uptake [49] now makeit possible to directly follow the active populations of bac-teria (rather than just culturable organisms) in soil. Inaddition, analysis of appropriately selected phospholipidfatty acid (PLFA) pro¢les can indicate the amount offungal and bacterial biomass present and, when coupledwith radio- or stable-isotope analysis, can indicate alter-ations in the activity of this biomass (see [15]). PLFAtechniques have recently been used to investigate the in-teraction between AM fungi and other soil micro-organ-isms and have shown considerable promise [15,29]. Thesenew methods in soil microbial ecology together with ad-vances in molecular techniques to identify AM fungi bothin colonised roots and the external phase mean that fol-lowing AM fungal ecology and their interaction with thesoil biota is now possible. Indeed, molecular methodolo-gies have already shown that spore diversity found in thevicinity of the root is not readily translated into diversityfound in the actual colonised root [50]. The combinedapplication of these new techniques in the future shouldenable valuable insights into the ecological role of inter-acting groups of soil micro-organisms and AM fungi andtheir subsequent impact upon carbon dynamics and nu-trient translocation under a range of di¡ering soil, andultimately ¢eld, conditions.

Acknowledgements

I am very grateful to Alastair Fitter for detailed com-ments and suggestions on earlier drafts. A.H. is funded bya BBSRC David Phillips Fellowship.

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