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FEMS Microbiology Ecology 32 (2000) 91^96
www.fems-microbiology.org
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 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. 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 plant
root are ubiquitous in the natural environment. The associations themselves can be further classi¢ed into one of
seven di¡erent 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 identi¢ed for the association (i.e. defence,
nutrient uptake, soil aggregation stability, drought resistance) has posed problems in producing a clear de¢nition
to best describe the association. Currently, the most useful
de¢nition 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
* Tel. : +44 (1904) 432878; Fax: +44 (1904) 432860;
E-mail : [email protected]
the most ancient and probably aided the ¢rst 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, speci¢city. 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 bene¢t 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
0168-6496 / 00 / $20.00 ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 6 4 9 6 ( 0 0 ) 0 0 0 2 3 - 4
92
A. Hodge / FEMS Microbiology Ecology 32 (2000) 91^96
the AM association in terms of interactions with other
organisms and the implications of these interactions for
mycorrhizal development and functioning.
ing in enhanced ¢xation levels and consequently improved
N status of the plant thus promoting plant growth and
functioning which in turn also bene¢ts mycorrhizal development (reviewed for legumes by [17]; see [18] for Frankia).
2. Interactions in the mycorrhizosphere
2.2. AM in£uences on soil microbial interactions
2.1. Soil microbial interactions on AM fungi
Soil micro-organisms in£uence 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 e¡ect is the more
predominant has been found to be in£uenced 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 di¤cult to draw any useful generalisations.
Indeed, even the same genus has been shown to have either a bene¢cial, negative or neutral e¡ect 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,
PFLA16:1g5) did not decrease nor did AM hyphal transport of 33 P [15].
Positive in£uences on the AM symbiosis after addition
of plant growth promoting rhizobacteria (PGPR), which
include £uorescent 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 bene¢ts for the
N2 -¢xing nitrogenase system of the other symbiont, result-
Once mycorrhizal colonisation has occurred, subsequent
exudation release by the root may be modi¢ed 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 in£uenced 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, £uorescent pseudomonads showing a decrease, increase or no
e¡ect 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 £uorescent 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 una¡ected. 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 di¡erent AM fungi
(Glomus etunicatum, Glomus mosseae or Gigaspora rosea)
Schreiner et al. [26] observed di¡erences 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 g31 soil).
The other two AM fungi did not di¡er in the amount of
external hyphae they produced but soil sampled from pots
containing G. etunicatum had higher amounts of Grampositive bacteria, measured as colony-forming units per g
A. Hodge / FEMS Microbiology Ecology 32 (2000) 91^96
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 in£uenced by the external mycelium of the AM fungus) of di¡erent AM fungi may
in£uence 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 in£uence 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 e¡ect 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 speci¢cally 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 unidenti¢ed 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 una¡ected and conidial
germination of Fusarium oxysporum f.sp. chrysanthemi
was reduced. These observed e¡ects 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 e¡ect 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 di¡ering results reported on the in£uence 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.
2.3. Grazing 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]. How-
93
ever, 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
pro¢table in terms of reproductive success [34]. Thus,
although active grazing of AM fungal hyphae may not
be an important feature under ¢eld conditions, collembola
may reduce the e¡ectiveness 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 bene¢cial (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
e¡ectiveness of the mycorrhizal symbiosis [33]. The internal colonisation will remain intact and thus represent a
carbon drain on the plant, but with reduced bene¢ts due
to a reduction in the external hyphal length. Re-establishment of the external mycelium will again require more
plant carbon to be invested.
3. From microcosm to ¢eld
The majority of the studies discussed above have involved investigating the interactions between soil microorganisms and, generally, a single AM fungal inoculum
added to microcosm units. Such studies are a ¢rst approximation to understanding the complex interactions which
can occur using controlled conditions which would be impossible 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 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
94
A. Hodge / FEMS Microbiology Ecology 32 (2000) 91^96
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 di¡ering 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
day31 [37] but again such estimates generally come from
microcosm studies. In a ¢eld study, Chiariello et al. [38]
applied 32 P to the leaves of a donor Plantago erecta plant
present in a serpentine annual grassland and detected high
levels (i.e. s 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 32 P transferred. Thus, there is an urgent need to investigate the
ecology of the symbiosis under a range of ¢eld 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 e¡ectively 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 e¤cient 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 ¢eld [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 e¡ectively 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 di¤culties associated with studying it particularly under ¢eld
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 £uorescent 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) pro¢les 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 di¡ering soil, and
ultimately ¢eld, conditions.
Acknowledgements
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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www.fems-microbiology.org
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 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. 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 plant
root are ubiquitous in the natural environment. The associations themselves can be further classi¢ed into one of
seven di¡erent 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 identi¢ed for the association (i.e. defence,
nutrient uptake, soil aggregation stability, drought resistance) has posed problems in producing a clear de¢nition
to best describe the association. Currently, the most useful
de¢nition 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
* Tel. : +44 (1904) 432878; Fax: +44 (1904) 432860;
E-mail : [email protected]
the most ancient and probably aided the ¢rst 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, speci¢city. 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 bene¢t 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
0168-6496 / 00 / $20.00 ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 6 4 9 6 ( 0 0 ) 0 0 0 2 3 - 4
92
A. Hodge / FEMS Microbiology Ecology 32 (2000) 91^96
the AM association in terms of interactions with other
organisms and the implications of these interactions for
mycorrhizal development and functioning.
ing in enhanced ¢xation levels and consequently improved
N status of the plant thus promoting plant growth and
functioning which in turn also bene¢ts mycorrhizal development (reviewed for legumes by [17]; see [18] for Frankia).
2. Interactions in the mycorrhizosphere
2.2. AM in£uences on soil microbial interactions
2.1. Soil microbial interactions on AM fungi
Soil micro-organisms in£uence 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 e¡ect is the more
predominant has been found to be in£uenced 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 di¤cult to draw any useful generalisations.
Indeed, even the same genus has been shown to have either a bene¢cial, negative or neutral e¡ect 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,
PFLA16:1g5) did not decrease nor did AM hyphal transport of 33 P [15].
Positive in£uences on the AM symbiosis after addition
of plant growth promoting rhizobacteria (PGPR), which
include £uorescent 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 bene¢ts for the
N2 -¢xing nitrogenase system of the other symbiont, result-
Once mycorrhizal colonisation has occurred, subsequent
exudation release by the root may be modi¢ed 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 in£uenced 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, £uorescent pseudomonads showing a decrease, increase or no
e¡ect 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 £uorescent 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 una¡ected. 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 di¡erent AM fungi
(Glomus etunicatum, Glomus mosseae or Gigaspora rosea)
Schreiner et al. [26] observed di¡erences 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 g31 soil).
The other two AM fungi did not di¡er in the amount of
external hyphae they produced but soil sampled from pots
containing G. etunicatum had higher amounts of Grampositive bacteria, measured as colony-forming units per g
A. Hodge / FEMS Microbiology Ecology 32 (2000) 91^96
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 in£uenced by the external mycelium of the AM fungus) of di¡erent AM fungi may
in£uence 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 in£uence 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 e¡ect 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 speci¢cally 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 unidenti¢ed 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 una¡ected and conidial
germination of Fusarium oxysporum f.sp. chrysanthemi
was reduced. These observed e¡ects 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 e¡ect 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 di¡ering results reported on the in£uence 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.
2.3. Grazing 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]. How-
93
ever, 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
pro¢table in terms of reproductive success [34]. Thus,
although active grazing of AM fungal hyphae may not
be an important feature under ¢eld conditions, collembola
may reduce the e¡ectiveness 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 bene¢cial (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
e¡ectiveness of the mycorrhizal symbiosis [33]. The internal colonisation will remain intact and thus represent a
carbon drain on the plant, but with reduced bene¢ts due
to a reduction in the external hyphal length. Re-establishment of the external mycelium will again require more
plant carbon to be invested.
3. From microcosm to ¢eld
The majority of the studies discussed above have involved investigating the interactions between soil microorganisms and, generally, a single AM fungal inoculum
added to microcosm units. Such studies are a ¢rst approximation to understanding the complex interactions which
can occur using controlled conditions which would be impossible 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 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
94
A. Hodge / FEMS Microbiology Ecology 32 (2000) 91^96
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 di¡ering 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
day31 [37] but again such estimates generally come from
microcosm studies. In a ¢eld study, Chiariello et al. [38]
applied 32 P to the leaves of a donor Plantago erecta plant
present in a serpentine annual grassland and detected high
levels (i.e. s 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 32 P transferred. Thus, there is an urgent need to investigate the
ecology of the symbiosis under a range of ¢eld 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 e¡ectively 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 e¤cient 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 ¢eld [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 e¡ectively 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 di¤culties associated with studying it particularly under ¢eld
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 £uorescent 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) pro¢les 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 di¡ering soil, and
ultimately ¢eld, conditions.
Acknowledgements
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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