FEMS Microbiology Reviews 29 (2005) 795–811
www.fems-microbiology.org
Living in a fungal world: impact of fungi on soil bacterial
niche development q
Wietse de Boer
a
a,*
, Larissa B. Folman a, Richard C. Summerbell b, Lynne Boddy
c
NIOO-Centre for Terrestrial Ecology, Department of Plant Microorganism Interactions, P.O. Box 40, 6666 ZG Heteren, The Netherlands
b
Centraalbureau voor Schimmelcultures, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands
c
Cardiff School of Biosciences, Cardiff University, Cardiff CF10 3TL, UK
Received 27 May 2004; received in revised form 7 October 2004; accepted 19 November 2004
First published online 16 December 2004
Abstract
The colonization of land by plants appears to have coincided with the appearance of mycorrhiza-like fungi. Over evolutionary
time, fungi have maintained their prominent role in the formation of mycorrhizal associations. In addition, however, they have been
able to occupy other terrestrial niches of which the decomposition of recalcitrant organic matter is perhaps the most remarkable.
This implies that, in contrast to that of aquatic organic matter decomposition, bacteria have not been able to monopolize decomposition processes in terrestrial ecosystems. The emergence of fungi in terrestrial ecosystems must have had a strong impact on the
evolution of terrestrial bacteria. On the one hand, potential decomposition niches, e.g. lignin degradation, have been lost for bacteria, whereas on the other hand the presence of fungi has itself created new bacterial niches. Confrontation between bacteria and
fungi is ongoing, and from studying contemporary interactions, we can learn about the impact that fungi presently have, and have
had in the past, on the ecology and evolution of terrestrial bacteria. In the first part of this review, the focus is on niche differentiation between soil bacteria and fungi involved in the decomposition of plant-derived organic matter. Bacteria and fungi are seen to
compete for simple plant-derived substrates and have developed antagonistic strategies. For more recalcitrant organic substrates,
e.g. cellulose and lignin, both competitive and mutualistic strategies appear to have evolved. In the second part of the review, bacterial niches with respect to the utilization of fungal-derived substrates are considered. Here, several lines of development can be
recognized, ranging from mutualistic exudate-consuming bacteria that are associated with fungal surfaces to endosymbiotic and
mycophagous bacteria. In some cases, there are indications of fungal specific selection in fungus-associated bacteria, and possible
mechanisms for such selection are discussed.
Ó 2004 Federation of European Microbiological Societies. Published by Elsevier B.V. All rights reserved.
Keywords: Fungal–bacterial interactions; Fungus-associated bacteria; Competition; Mutualism; Mycophagy
Contents
1.
2.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Niche differentiation between bacteria and fungi with respect to the decomposition of plant-derived substrates . . . . . .
2.1. Role of fungi and bacteria as decomposers of simple substrates: root exudates . . . . . . . . . . . . . . . . . . . . . . . .
q
This is publication 3466 of NIOO-KNAW Netherlands Institute of Ecology.
Corresponding author. Tel.: +31 26479111; fax: +31 2623227.
E-mail address: [email protected] (W.de Boer).
*
0168-6445/$22.00 Ó 2004 Federation of European Microbiological Societies. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.femsre.2004.11.005
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W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
2.2. Role of fungi and bacteria as decomposers of complex substrates: cellulose . . . . . . . . . . . . . . . . . . . . . . . .
2.3. Role of fungi and bacteria as decomposers of complex substrates: lignin . . . . . . . . . . . . . . . . . . . . . . . . . .
2.4. Possible interactions between bacteria and fungi in relation to breakdown of the lignocellulose complex. . . .
Bacterial niches related to the utilization of fungal-derived substrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1. Fungal-exudate consuming bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2. Selection of fungal-exudate consuming bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3. Effects of fungal-exudate consuming bacteria on fungal performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.4. Endosymbiosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5. Mycophagy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.6. Decomposition of fungal cell walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Perspectives. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
Most of lifeÕs history has been in the aquatic environment. Here, in the past, bacteria have ruled the two most
important processes in organic matter cycling, namely
primary production (autotrophy) and decomposition
(heterotrophy). Nowadays, though eukaryotes, in particular algae, are major contributors to primary production, bacteria are still by far the dominant decomposers
in water and sediments [1].
From the late Ordovician to the early Devonian on,
however, land began to be colonized with plants, being
the majority autotrophs. This was probably also the
time when soil development started [2–4]. Fossils of
the first land plants have revealed that filamentous
fungi, resembling the glomalean mycorrhizal fungi, were
present in their root tissues [4,5]. In fact, it has been
hypothesized that the development of plant-fungal
mutualism preceded the development of roots and,
therefore, has been crucial to the ability of plants to colonize the land [4]. The mycorrhizal association between
fungi and roots of plants has remained very successful
through evolution [6]. Almost all successful extant land
plants (80% angiosperms, 100% gymnosperms and
70% pteridophytes) in nature are associated with one
or several mycorrhizal fungi. Mycorrhizal formation
has not been restricted to the Glomales but is also particular in Basidiomycota. In most cases, the basis of the
mutualism is that the plant provides the major source of
fixed carbon, whereas the fungus provides the host with
mineral nutrients, water and in some cases protection
from root pathogens.
The colonization of land by plants provided a new
habitat for heterotrophs. The soil habitat is essentially
different from that of sediments in that it contains airfilled voids. The inability of the bacterial unicellular
body form to bridge these air-filled voids restricts bacterial motility in soils. This disadvantage is overcome by
the hyphal/mycelial growth form [7]. Furthermore, given
their ability to translocate nutrients [8], fungal hyphae
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are better adapted to cross nutrient-poor spots in soil
than bacteria in searching for the heterogeneously distributed nutrient resources.
In addition to differences in three-dimensional space
between soils and aquatic environments, there are also
strong differences in the composition of the organic matter that they receive [9]. On land, plants had to protect
themselves against desiccation and radiation, and they
developed new structural compounds, e.g. cutin and
suberin that cover leaves, stems and roots [9]. This
development provided the terrestrial decomposer microorganisms with a new challenge, i.e. gaining access to the
well-protected organic matter. Hence, efficient decomposition of bulky plant tissues requires penetration – a
feature of the hyphal growth form.
The clear advantages of the hyphal growth form to
colonize soil and to penetrate vascular plant tissues is
probably the reason that the primitive mycorrhiza-like
fungi could evolve to occupy decomposer niches. Both
fossils and molecular biological data indicate that major
groups of saprotrophic soil fungi, Zygomycota, Ascomycota and Basidiomycota, are descendants of the
glomalean fungi [2,10,11]. Interestingly, an important
terrestrial group of bacterial decomposers, the actinomycetes, have also developed the hyphal growth form
[7], but this has not enabled bacteria to monopolize
terrestrial heterotrophic processes.
The evolution of fungal decomposers not only
included optimization of colonization and penetration
abilities, but also the development of new pathways
to degrade recalcitrant structural compounds that are
unique to vascular plants [12–14]. This is especially
the case for lignin. With cellulose fibrils embedded in
a lignin matrix, plants developed a flexible but very
robust structural framework. This lignocellulose complex is both physically and chemically resistant to degradation even after death of the plants. The evolution
of pathways for lignin degradation has been largely restricted to Basidiomycota and xylariaceous Ascomycota [15,16].
W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
With the monopolisation of two important niches in
terrestrial ecosystems, namely mycorrhiza formation
and decomposition of lignocellulose, fungi have
obtained a pivotal role in the functioning of terrestrial
ecosystems. This must have had a strong impact on
the evolution of terrestrial bacteria. Bacteria and fungi
have undergone niche differentiation in the decomposition of organic material. The evolution of this differentiation is an ongoing process. In this review, we will
consider this aspect with respect to the decomposition
of plant-derived organic matter, including easily assimilable root exudates (Section 2.1), cellulose (2.2) and
recalcitrant lignin (2.3). Some bacteria have evolved
the potential to utilize products released from complex
organic substrates as a result of fungal exoenzyme activity (2.4). The presence of fungi, however, has resulted
not only in the loss of potential niches for bacteria,
but also in the creation of new ones. These are discussed
in the second part of this review, which addresses bacteria growing on fungal exudates (3.1–3.3), living hyphal
compartments (3.4 and 3.5) and the walls of dead
hyphae (3.6).
So far, soil bacteriologists and mycologists have largely neglected each otherÕs research fields [17]. We hope
that this article will inspire them to an intensive
collaboration.
2. Niche differentiation between bacteria and fungi with
respect to the decomposition of plant-derived substrates
During the evolution of terrestrial microbial life,
fungi have become the major decomposers of recalcitrant organic matter. Bacteria on the other hand have
been able to maintain a significant role in the degradation of simple substrates. However, this is only the
general picture and, as it will be shown below, there is
an ongoing confrontation between fungi and bacteria
for both complex and simple substrates.
2.1. Role of fungi and bacteria as decomposers of simple
substrates: root exudates
Plant roots exude substantial amounts of low molecular weight organic compounds such as amino acids,
sugars and organic acids, resulting in increased microbial populations and activity [18–21]. Given the high
numbers of fast-growing bacteria, especially Gramnegative strains, in the zone close to the root (rhizosphere), it has been widely assumed that easily degradable plant exudates are almost exclusively degraded by
bacteria [18,20]. Therefore, most publications on
dynamics of microorganisms in the rhizosphere deal
only with shifts in bacterial communities. However,
saprotrophic and plant pathogenic fungi have been
797
isolated frequently from the rhizosphere and rhizoplane
(root surface) [22–24]. With respect to the saprotrophic
fungi, species with ruderal characteristics, including rapid growth, prolific spore production and ability to
use only relatively simple fixed carbon compounds, appear to be rhizosphere inhabitants [22,23,25]. This is
true, for example, for members of the zygomycetous order Mucorales.
Until recently, it has been difficult to estimate the relative contribution of fungi and bacteria to decomposition in localized environments such as the rhizosphere.
Most studies have relied on selective respiration, i.e.
the respiration that occurs after addition of selective
(fungal or bacterial) antibiotics [26]. Although such
studies have indicated the potential for fungi to compete
for simple substrates, they do not provide a reliable estimate of the competitive strength of fungi versus bacteria, because of artefacts due to mixing, severing of
hyphae, non-target inhibition, incomplete inhibition
and high substrate loading. The advances in analytical
techniques that allow measurement of stable isotopes
(13C) incorporated in biomarkers (e.g., signature fungal
and bacterial phospholipid fatty acids or the characteristic fungal membrane sterol ergosterol) have created
the possibility of a greatly improved evaluation of the
relative importance of fungal and bacterial decomposition [27].
Recent studies using 13C-labelled grasses indicated
that fungi might have a significant contribution to the
decomposition of root exudates [28,29]. Similarly, incorporation of 13C into fungal phospholipid fatty acids was
seen after addition of 13C-labelled model rhizosphere
compounds to soil [30–33]. These studies have revealed
that the fungal contribution to the decomposition of
easily degradable substrates is highest in acid soils and
at high substrate loading rates. This pattern has been
attributed to the ability of fungi in its superior osmotic
stress tolerance capabilities in comparison with those
of the bacteria [31].
At low substrate concentrations, microorganisms
with high-affinity uptake systems are expected to have
the advantage. However, since such high-affinity systems
have been described for both bacteria and fungi, low
substrate concentrations do not necessarily confer an
advantage on either group [7]. Clearly, there is a need
for more studies that address the effects of substrate concentration and composition on the relative competitive
strength of fungi and bacteria. In the near future, more
detailed information on the composition of fungal and
bacterial decomposer active in situ in the rhizosphere,
and in other environments, will become available from
substrate-induced labelling of DNA and RNA (stable
isotope probing) [34].
The presence of filamentous fungi with the ability to
rapidly decompose easily degradable organic compounds must exert a selection pressure on bacteria to
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compete for these nutrients. A multitude of antifungal
strategies has been revealed in bacteria, including production of directly inhibitory factors such as HCN, antibiotics, lytic enzymes and volatiles (interference
competition), as well as nutrient-sequestering factors
such as iron-chelating siderophores (substrate competition) [35–38]. The nature and regulation of production
of such antifungal compounds has been intensively studied with the aim of improving the possibilities for biocontrol of root-infecting and pathogenic fungi [39].
Several of the bacterial competitive strategies, however,
appear to be important not only in the interaction with
fungi but also in the interactions with other bacteria,
e.g., in the rhizopshere. For instance, antibiotics produced by rhizosphere-inhabiting Pseudomonas spp. are
active against a range of fungi and bacteria [40]. Hence,
it is often not clear to what extent an antifungal trait has
actually evolved as a strategy to compete with fungi.
Experimental manipulation of fungal density could be
used as an initial approach to study the impact of fungi
on the selection of bacteria with anti-fungal properties.
The fungi themselves often produce compounds with
antibacterial activity, and have developed several strategies to counteract bacterial antagonism including detoxification, removal of antibiotics by efflux, and
modification of bacterial gene expression [41]. Hence,
it appears that the bacterial and fungal inhabitants of
the rhizosphere are involved in an ongoing evolutionary
arms race.
2.2. Role of fungi and bacteria as decomposers of complex
substrates: cellulose
Cellulose is the most abundant organic compound on
the planet (30–50% of plant dry weight) and, therefore,
represents a huge source of energy for microorganisms.
Microbial decomposition of cellulose can take place under both aerobic and anaerobic conditions. The ability
to degrade cellulose aerobically is widespread among
fungi and is especially well represented among the Ascomycota and Basidiomycota (groups now to considered
to encompass the corresponding asexually reproductive
states formerly grouped separately as Deuteromycota)
[15,42,43]. Aerobic cellulose degradation is also known
for several soil bacterial species in both filamentous
(e.g. Streptomyces, Micromonospora) and non-filamentous (e.g. Bacillus, Cellulomonas, Cytophaga) genera
[43].
Fermentative degradation of cellulose is widely distributed among obligately anaerobic bacteria (e.g. Acetivibrio, Clostridium, Ruminococcus) but is also present
among some fungal species, belonging to the phylum
Chytridiomycota, that inhabit the gastrointestinal tracts
of ruminants [43]. However, in most anoxic environments, bacteria are almost exclusively responsible for
degradation of cellulose [43,44]. The anaerobic bacteria
use complexed cellulase systems, cellulosomes, which allow concerted enzyme activity of different cellulases, and
minimize the distance over which the cellulose hydrolysis products must diffuse to the cells [43,45]. Remarkably, this highly efficient cellulolytic system is not
present in aerobic bacteria. Aerobic cellulolytic fungi
and bacteria produce freely diffusible extracellular cellulase enzyme systems consisting of endoglucanases, exoglucanases and b-glucosidases that act synergistically
in the conversion of cellulose to glucose [43,46]. The cellulases are distributed over different enzyme families
suggesting convergent evolution towards the same substrate specificity [43]. Thus, although components of
the cellulolytic system of soil bacteria and fungi can be
distantly related, their functionality is quite similar.
The presence of functionally equivalent cellulolytic
systems in bacteria and fungi implies that competition
for cellulose may take place in soil. In general, however,
it is assumed that by far the most of cellulose degradation in soils is performed by fungi. This is probably
due to the relative inaccessibility and to the chemical
nature of cellulose. Cellulose fibres are seldom found
in pure form, but embedded in a matrix of other structural polymers, in particular hemicelluloses and lignin.
Furthermore, most cellulose in plant cell walls is resistant to enzymatic hydrolysis because of the crystalline
(fibrillose) structure. Variation in the degree of accessibility and crystallinity of cellulose may lie at the basis
of niche differentiation among different cellulolytic
microorganisms in different substrates, such as wood
or compost.
The hyphal growth of fungi and cellulolytic actinomycetes appears to be an important strategy to access
cellulose fibres, via pores in the cell wall material, and
to bring the cellulases into close contact with the cellulose polymers [43]. In lignified plant material, those
fungi that cause Ôwhite rotÕ are able to gain access to
the cellulose within the lignocellulose complex by
decomposition of the lignin polymers [43,47,48]. However, the ability to decompose lignin is not widespread,
and some fungi, such as those causing brown rot or soft
rot, access cellulose in woody tissues by other means
(Table 1, Section 2.3). The fungi that cause soft rot
(Type 1), produce fine penetration hyphae that give
them access to the S2 woody cell wall layer, in which
they form chains of diamond-shaped cavities in the
immediate vicinity of the hyphae, that follow the orientation of the cellulose microfibrils [15,49]. The fungi that
cause Ôbrown rotÕ are able to modify lignin, but they
decompose it only to a limited extent. They decompose
crystalline cellulose through the concerted action of enzymes (mostly endoacting, e.g. endoglucanases) and
non-enzymatic systems [17,50,51]. The latter may include reduction of pH (e.g., by excretion of oxalate)
and the excretion of iron containing low molecular
weight glycopeptides that generate hydrogen peroxide.
W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
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Table 1
Summary of the characteristics of the major types of wood decay
Decay type
Cell wall constituents used
Anatomical features
Causal agents (major groups)
White rot:
simultaneous
White rot:
sequential/selective
Brown rot
All
Walls attacked progressively from
lumen
Walls attacked progressively from
lumen
Entire wall attacked
Basidiomycota and some
Ascomycota
Basidiomycota and some
Ascomycota
Basidiomycota and
few Ascomycota
Ascomycota, Deuteromycota
and some bacteria
Ascomycota, Deuteromycota
and some bacteria
Soft rot: type 1
Soft rot: type 2
All, though hemicelluloses and
lignin used selectively initially
All except lignin, but the latter is
modified
All except lignin, but the latter is
modified
All except lignin, but the latter is
modified
Free radicals are then produced (by the Fenton reaction:
Fe2+ + H2O2 ! Fe3+ + OH + OH), which presumably diffuse freely into the S2 layer of woody cell walls
and eventually cause the depolymerisation of cellulose.
A range of hypotheses has been put forward concerning
how low molecular weight metabolites, metals and radicals function together in the degradation process, which
has been reviewed elsewhere [51].
Microscopic observations indicate that filamentous
actinomycetes are almost never involved in wood decay
[49]. This is surprising, as these hypha-forming, substrate-penetrating bacteria might at first appear to be
the most likely direct competitors of cellulolytic fungi.
Many cellulolytic actinomycetes, however, are unable
to degrade crystalline cellulose [52,53]. Further, their
cellulases and hemicellulases operate best at neutral to
alkaline pH, in contrast to the fungal enzymes that perform best at low pH [54]. Hence, the often acidic nature
of wood [15], and the increased acidification that generally accompanies fungal growth and activity in wood,
may prevent growth of cellulolytic actinomycetes
[47,51]. Moreover, actinomycete-mediated decomposition of cellulose can be substantial in composts that
remain alkaline due to high ammonification [52]. Thus,
it appears that a high pH and pH-increasing processes,
like ammonification, are important factors mediating
the level of cellulose degradation brought about by actinomycetes. The fact that many streptomycetes are able
to exude antifungal compounds may indicate that they
are competitors of fungi under appropriate environmental conditions [55,56].
Information on the extent of in situ cellulose decomposition by non-filamentous soil bacteria is very limited.
It seems likely that they are confined to easily accessible
cellulose, due to their restricted ability to penetrate solids. Upon addition of cellulose to an agricultural soil, an
initial phase featuring predominantly bacterial cellulose
decomposition was recognized, followed by a stage
dominated by fungal cellulose decomposition [57]. This
could point to an opportunistic strategy of cellulolytic
soil bacteria whereby they respond immediately whenever easily accessible cellulose is present. It is to be
expected that such a strategy would also involve the
Longitudinal cavities develop in S2
wall layer
Walls attacked from lumen (in
conifers mainly the S2 layer)
production of inhibitory compounds, to protect the cellulose resources they colonize from invasion by actinomycetes and fungi. However, although the potential to
produce antifungal metabolites has been shown for
some cellulose-degrading bacteria, e.g. Bacillus pumilis,
this has not been studied in the context of cellulose degradation [58].
Non-filamentous cellulolytic bacteria are also sometimes present in decaying wood, though decay is usually
limited and they are often restricted to parts of the wood
containing easily accessible pectin, cellulose and hemicellulose, e.g. ray cells, and to wood under environmental conditions inimical to fungal growth [15,49,59,60].
Two patterns have been discerned: tunneling (or cavitation) in the S3 layer of the cell wall in the approximately
outer first cm of wood, and erosion, characterised by
depressions, channels and ÔhoneycombÕ patterns [59].
Besides the non-filamentous bacteria that have the
ability to degrade crystalline cellulose, many other soil
bacteria appear to have incomplete cellulolytic systems
[61]. It may be that the cellulases of these bacteria, in
combination with other hydrolytic enzymes, participate
in the penetration of living plants in either pathogenic or
endophytic associations.
2.3. Role of fungi and bacteria as decomposers of complex
substrates: lignin
Lignin was present in the oldest known land plants,
and it appears that the structural rigidity that it imparts
was a prerequisite in the colonization of the terrestrial
environment [12,62]. Despite its widespread distribution
and early appearance in terrestrial life, decomposition of
lignin is largely, but not exclusively, found in certain
genera of Basidiomycota that are collectively named
white-rot fungi (Table 1) [15,16,48,63]. The breakdown
of lignin is mediated by enzymes, such as laccases and
peroxidases, and free radicals, and occurs strictly under
aerobic conditions. Bacterial lignin degradation appears
to be negligible in terrestrial environments compared to
the activity of white-rot fungi [63,64]. However, growth
of both filamentous and non-filamentous bacteria on lignin-like compounds has been observed [65–68]. Several
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actinomycete species have been shown to solubilise lignin, in particular lignin in grasses [63,69]. This may be
a strategy, similar to that of brown-rot fungi (Section
2.2), to gain access to cellulose.
2.4. Possible interactions between bacteria and fungi in
relation to breakdown of the lignocellulose complex
It is clear from the preceding paragraphs that, under
aerobic conditions, lignocellulolytic substrates are
mainly broken down by fungi, despite the ubiquity of
bacteria. However, bacteria present in lignocelluloserich substrates may interact with fungal degraders in
several ways.
The hydrolytic activity of extracellular fungal
enzymes in lignocellulose-rich material results in production of water-soluble sugars and phenolic compounds [65,70,71]. These organic solutes comprise the
actual sources of energy and carbon for the fungus.
They are, however, also good growth substrates for
other microorganisms, and can be competed for by bacteria. Intense bacterial competition could deprive the
fungus of its energy sources and could result in a
decrease in lignocellulose degradation. This bacterially
induced retardation of fungal lignocellulose decomposition has, in fact, been shown to occur in an experiment
on degradation of wheat straw by the white rot fungus
Dichomitus squalens [72]. The same study, though,
showed that the presence of bacteria did not hamper
lignocellulose degradation by a Pleurotus sp. This was
ascribed to the production of bacterial inhibiting compounds by the fungus, which is in agreement with the
results of other studies reporting bactericidal effects of
Pleurotus sp. in soils [73,74]. Indeed, in situ bactericidal
effects are likely to have evolved widely in the fungal
kingdom as discussed earlier (Section 2.1). In addition
to bactericidal effects, fungi have other mechanisms to
prevent bacterial exploitation of released oligomers.
For example, the highly hydrophobic nature of the
mycelium of Pleurotus sp. appeared to prevent bacteria
from penetrating into the straw substrate [72]. Another
strategy may be the extra production of hydroxyl radicals, as has been shown for the brown rot fungus Antrodia vaillantii [75]. Additionally, acidification of the
environment by fungal exudation of strong organic
acids, e.g. oxalic acid, will prevent many bacterial strains
from becoming active [51].
Although the aforementioned studies clearly show
that competitive interactions between fungi and bacteria
can be important during fungal decomposition of recalcitrant organic matter, the interactions are not necessarily always competitive. If fungal growth is constrained
by factors other than the availability of soluble carbohydrates, bacterial consumption of these compounds may
not be negative. For example, in studies on the effect
of bacterial co-inoculation into spruce wood blocks with
white rot fungi (Heterobasidion annosum, Resinicium bicolor, or Hypholoma fasciculare), the degradation of the
wood consistently tended to be higher in co-inoculated
trials than in trials inoculated with the fungus alone,
even though wood decay could not be ascribed to the
bacteria by themselves [76]. This stimulation may simply
have been due to bacterial production of growth factors
needed by the fungi, especially vitamins. It may also
have related, however, to increased fungal enzyme activity stimulated by bacterial utilization of a proportion of
the breakdown products. Relatively high levels of smallmolecule breakdown products would tend to cause
down-regulation of fungal enzymatic activity, but bacterial activity may reduce concentrations sufficiently to
prevent this moderating effect.
Otherwise, bacteria may positively affect fungal activity by producing cellulase and pectinase enzymes that increase accessibility of substrates to the fungus. In
addition, bacteria may also decompose solutes that are
toxic to particular fungi. Finally, the activities of organotrophic, nitrogen-fixing bacteria may increase the
nitrogen levels available for fungal growth [77–79].
3. Bacterial niches related to the utilization of
fungal-derived substrates
The development of fungi in terrestrial ecosystems
has resulted in a loss of some potential niches for bacteria, but it has also created opportunities to establish new
niches. The basis of these niches is bacterial consumption of substrates derived from fungi.
3.1. Fungal-exudate consuming bacteria
Plate counts and in situ microscopic observations
have both revealed the presence of bacteria on the surfaces of fungal hyphae and spores, as well as on mycorrhizal roots and in fruit body insides [80–88]. It is widely
assumed that fungal exudates are a major or exclusive
source of nutrients for these bacteria [84,89–94]. This
assumption underpins the idea that distinct habitats exist, which are characterised by enhanced or altered
microbial activity in the soil around fungal structures.
For example, the soil around mycorrhizas is considered
to be sufficiently under fungal influence that a mycorrhizosphere microhabitat can be distinguished from
the rhizosphere microhabitat found around non-mycorrhizal roots [95,96]. Likewise, soil immediately adjacent
to extraradical mycorrhizal hyphae and non-mycorrhizal hyphae is considered to subtend a mycosphere
habitat distinct from the bulk soil.
Most studies on the composition of bacterial communities on fungal surfaces have been done for agricultural
and economically important fungi, such as mycorrhiza
[116]
[135]
[90]
[87]
[196,197]
[110]
EM on Pinus sylvestris
Fungi grown in cotton compost
Similar results for Hydnum rufescens
EM on Fagus sylvatica
Cellulolytic and chitinolytic bacteria
Fungal strains from culture
collections
Mycorrhizal root
Mycelium
Sporocarps (interior)
Mantle
Sporocarps (interior)
Hyphae
Abbreviations: FISH, fluorescence in situ hybridisation; FAME, fatty acid methyl esters.
Bacillus, Burkholderia and Pseudomonas
Many different genera
Pseudomonas (fluorescent)
a-, b-, c-proteobacteria
Pseudomonas, Bacillus and Paenibacillus
Agrobacterium and Burkholderia
Bacillus, Paenibacillus and Arthrobacter
16S rDNA
Immuno-capture
and plating
Plating
Plating
Plating
Microscopy
Plating
Plating
Hyphae
Unidentified AM-fungi
and Glomus dussii
Suillus luteus (EM)
Pleurotus ostreatus
Cantharellus cibarius (EM)
Lactarius spp.
Tuber borchii
Phanerochaete chrysosporium
Plating
Glomus clarum (AM)
Sporocarps (interior)
Mycorrhizal root
(surface sterilised)
Spores
Suillus grevillei (EM)
Lactarius rufus (EM)
Physiological test, 16S rDNA
16S rDNA
Physiological test
FISH
Physiological test, 16S rDNA
FAME
[99]
[115]
801
Only Bacillus after surface
decontamination
gfp-tagging of Bacillus cereus
Bacillus, Pseudomonas and Burkholderia
EM on Pinus sylvestris
Pseudomonas, Bacillus and Streptomyces
Burkholderia, Pseudomonas and Paenibacillus
Physiological test
Biochemical test, FAME,
16S rDNA
FAME
Identification method
Isolation/counting
method
Surface
Fungal species
Table 2
Examples of bacteria associated with fungal surfaces
An important question to be addressed in the study
of common culturable bacteria is whether there is a specific fungal selection for particular bacterial strains, a
phenomenon that could indicate an established and
ongoing fungal-bacterial association. Exudation of soluble fungal storage sugars (usually trehalose) and polyols
(e.g. mannitol) has been suggested as a possible mechanism for selection of fungus-associated bacterial strains
by ectomycorrhizal (EM) fungi [90,92,101]. Fluorescent
pseudomonads associated with Douglas fir – Laccaria
bicolor mycorrhizas were revealed by genetic fingerprinting to be different from those in the bulk soil [101]. The
EM-associated strains were able to degrade trehalose
(produced by the EM fungus), whereas this ability was
rare among the bulk soil strains. Trehalose-degrading
fluorescent pseudomonads were also dominant among
culturable bacteria in fruit bodies of Cantharellus cibarius [90], but in this case, trehalase activity was also common for Pseudomonas strains in the bulk soil [102].
Organic acids may also be selective for fungus-associated bacterial strains. External hyphae of various EM
fungal species release organic acids, in particular oxalic
acid, which are thought to be involved in nutrient withdrawal from solid mineral substrates [103,104]. Oxalic
acid is also released by white-rot fungi during degradation of lignocellulose [103]. Although the capacity to
degrade the highly oxidized oxalic acid or its salt, oxalate, is not common for soil bacteria, oxalotrophy is
taxonomically widespread [105]. The genus Methylobacterium is frequently found as the dominant oxalotrophic
bacterium on and near oxalate-exuding plants, while the
genera Alcaligenes, Pseudomonas, Ralstonia and Streptomyces have been mentioned as important oxalotrophic
bacteria in soils [105]. Streptomyces has been found in
Dominant bacteria
3.2. Selection of fungal-exudate consuming bacteria
Plating
Plating
Extra information
References
formers, pathogens and saprotrophs that produce edible
fruit bodies. Such studies have been largely restricted to
the culturable fraction of the bacterial community.
Strains closely related to known species of the genera
Pseudomonas, Burkholderia and Bacillus are dominant
among these culturable inhabitants of fungal surfaces
(Table 2); former works in which slightly outdated taxonomies are utilized are also consistent with this picture
[81]. In addition, novel fungus-associated culturable species have also been detected [97,98]. The use of molecular techniques has detected both culturable bacteria, e.g.
bacilli, and non-culturable Archaea [99,100]. Although
culture techniques may have overestimated the importance of pseudomonads and bacilli [87], it is obvious
that these bacteria are frequent inhabitants of fungal
surfaces. Not surprisingly, therefore, to date almost all
studies aiming to elucidate the relationship between
fungi and associated bacteria have been restricted to
these bacterial groups.
[195]
[129]
W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
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W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
association with an oxalate-producing Douglas fir
mycorrhiza [106]. No additional information appears
to be available on associations between oxalotrophic
bacteria and fungi, an area worthy to further examine
in the future.
There is still little information available on the quality and quantity of carbon compounds exuded into the
environment by fungi [92,96,107]. More evidence is
clearly required to support the idea that there is a substrate-mediated increase and selection of bacteria by
fungi, especially in light of a recent study finding that,
when thymidine incorporation was used to quantify in
situ bacterial activity [108], there was no support for
the hypothesis that EM mycelia can stimulate bacterial
growth via carbon exudation. Furthermore, for arbuscular mycorrhizal (AM) fungi, it has been suggested that
the effect of exudates on bacterial populations may be
qualitative (relating to species and strain composition)
rather than quantitative [94].
Exudation of inhibitory chemicals by AM and EM
fungi has been suggested as a mechanism for selection
of fungus-specific, antibiotic-resistant bacteria [89,108].
Some saprotrophic basidiomycetes are also known to
produce antibiotics, i.e., various agaricoid species produced water-extractable antibiotics that inhibited
Gram-positive bacteria but not the Pseudomonas spp.
that had been isolated from the fruit bodies [109]. Since
antibiotic production is likely to be induced in the presence of appropriate bacteria, the range of basidiomycetes found to produce antibiotics is likely to be greater
when screening procedures include bacteria in the fungal
cultures than it would be in a study of pure fungal cultures. Of course, secretion of antibiotics by fungi in pure
culture does not necessarily mean that these antibiotics
are also secreted in natural environments. In various
studies, interesting fungus-associated bacterial strains
have been detected precisely because of their resistance
to broad-spectrum antibacterial antibiotics employed
in isolation media for fungi. This demands that antibiotic-mediated selection of bacteria by fungi deserves
more attention [98,110].
As well as these direct effects of fungi on bacteria,
indirect effects may also be seen. It has been suggested
that mycorrhizal fungi indirectly influence bacterial
communities in the mycorrhizosphere by stimulating
root growth, as well as by altering root exudation patterns and the structure of the surrounding soil
[93,96,111]. Such effects apply not only to free-living
bacteria but also to those involved in root nodule symbioses. AM fungi have been shown to enhance nodulation and nitrogen fixation in legumes. The increased P
uptake that occurs when these fungi are present is beneficial to the functioning of the nitrogenase enzyme of
the bacterial symbiont [96,112].
Although the aforementioned studies certainly do
indicate the potential for specific fungal selection of
bacterial strains, non-specific adherence of bacteria to
fungal hyphae and spores has also been observed
[113–115]. In addition, soil conditions have been shown
to affect the composition of bacterial populations associated with fungi [116]. It would appear that the probability of a particular bacterial species being selected by a
fungus is dependent on its abundance in the bulk soil
bacterial community, with the same fungal species having different bacterial associates in edaphically different
sites. Rhizosphere bacterial community composition
has also been shown to depend on the bacterial community composition of adjacent bulk soil [117].
Besides offering the possibility of growth on fungal
exudates, hyphae may be important for the transport
of bacteria, particularly for those associated with plants.
The nitrogen-fixing, endophytic bacteria of the genus
Azoarcus that occur in grasses have been found in association with rhizosphere-inhabiting fungi [118,119], suggesting that the bacteria colonize new plants via
transport on or in fungal hyphae. Furthermore, the possibility of adherence of Rhizobium leguminosarum to hyphae of the AM-fungus Gigaspora margarita has been
demonstrated [113]. The possible vector function of fungal hyphae does, however, imply active growth or movement of bacteria along the hyphae, as mature parts of
hyphae do not move towards the roots but reach them
via apical growth.
3.3. Effects of fungal-exudate consuming bacteria on
fungal performance
Associated bacteria may have negative, neutral or
positive effects on fungal fitness. There are several indications of mutualistic relationship between fungi and
their associated bacteria, the most obvious being
found in the cyanolichens. The fungi benefit from
the relationship by obtaining a supply of energy from
the cyanobacteria. Unlike the green algal photobionts
in most lichens, some cyanobacterial partners fix nitrogen and supply a portion of the yield to the fungus
[120–123].
Nitrogen transfer may also be important in the
association of organotrophic bacteria with fungi.
Nitrogen-fixing bacilli were associated with Douglas fir
– Rhizopogon vinicolor ‘‘tuberculate’’ EM [124]. Respiration in the tuberculate mycorrhizal complex by the
fungus, roots and associated microorganisms, probably
contributed to maintaining a microaerophilic environment where nitrogen fixation could take place. The
authors of this study hypothesized a mutualistic relationship in which the bacteria supplied the fungus with
nitrogen while growing on fungal exudates. Nitrogenfixing bacteria have also been found on hyphae in
mycorrhizal structures of Arbutus unedo [125]. To date,
however, no data have been reported that would shed
light on the relative importance of nitrogen fixation by
W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
exudate-consuming bacteria for the nitrogen supply of
mycorrhizal fungi.
The most well-known example of beneficial effects
conferred by fungus-associated bacteria is the so-called
EM helper bacteria [126]. The earliest studies concerned
the positive effect on EM establishment by fluorescent
pseudomonads that had been isolated from surface-sterilized EM of the same fungi, e.g. Rhizopogon luteolus
and Laccaria spp. (reviewed by Garbaye [126]). Several
follow-up studies have confirmed the stimulating effect
of these bacteria on mycorrhizal establishment, but the
actual mechanism has not been elucidated yet
[127,128]. Other studies have made it clear that the
ÔhelperÕ phenomenon is not restricted to fluorescent
pseudomonads as EM-associated bacilli and paenibacilli
have also been shown to stimulate mycorrhizal formation [116,129]. In addition, an EM-associated streptomycete was shown to stimulate growth of different EM
fungi [130].
Bacterial stimulation of AM growth and plant infection has also been reported [91,131,132]. However, in
most cases these reports concern so-called plant-growth
promoting rhizosphere bacteria that have no clear association with AM fungi. Nevertheless, such bacteria are
also sometimes referred to as helper bacteria [133].
Fungus-associated bacteria can also have effects on
fruit body formation and spore production. Fruit body
initiation of Agaricus bisporus is dependent on the presence of Pseudomonas putida bacteria. The exact mechanism has yet to be determined but it has been suggested
that the mycelium produces self-inhibiting compounds,
which have to be removed by the bacteria [134]. P. putida strains were also shown to promote mycelial growth
and fruit body formation of Pleurotus ostreatus [135].
However, care should be taken when interpreting the
outcome of these interactions as beneficial to the fungus,
since fruiting and increased hyphal extension rate could
equally well be interpreted as a stress response.
Several cases of stimulation of spore germination by
spore-associated bacteria have been reported [115,136–
138]. The actual mechanism(s) is not known but production of germination-inducing volatiles, degradation of
germination-inhibiting compounds, and enzymatic
weakening of the spore wall have been proposed. The
last-mentioned possibility is supported by electron
micrographs of spore-wall-eroding activities of chitinolytic bacteria [139,140].
In contrast, inhibition of spore germination by
spore-associated bacteria has also been frequently
reported [115,141,142]. In fact, the restriction of germination of most fungal spores in non-amended bulk soil
is a well-known phenomenon, referred to as fungistasis
(or mycostasis), which has been attributed to withdrawal of nutrients from the fungal spores by associated bacteria [141,143] and to the production of
bacterial antibiotics [144,145].
803
3.4. Endosymbiosis
The occurrence of bacteria inside tissues or cells of
eukaryotes has been reported for plants, animals and
protists [146–148]. The status of these bacteria varies
from occasional co-existence to obligate dependency
on the host. Indeed, mitochondria and chloroplasts
may be regarded as the ultimate obligately dependent
bacteria that have lost most of their original bacterial
properties [149,150].
To date, comprehensive studies on the occurrence of
endocellular bacteria in fungi are lacking. A notable
exception is the research of Bonfante and her colleagues
on such bacteria in AM fungi [151,152]. Earlier microscopic studies by different research groups had already
revealed the presence of bacteria-like organisms (BLOs)
inside spores and hyphae of AM fungi (reviewed by
Scannerini and Bonfante-Falso [152]). However, as these
BLOs appeared to be unculturable, it was not until the
advent of PCR analysis that their bacterial status could
be confirmed and their phylogenetic position determined
[153,154]. Most detailed studies have been done on the
endocellular bacteria of Gigaspora margarita. Sequence
analysis of the 16S rDNA revealed that the bacteria
formed a distinct lineage within the b-proteobacteria,
with the genera Burkholderia, Pandoraea and Ralstonia
as closest neighbours [154]. Phylogenetically closely
related bacteria were found in G. margarita isolates from
different geographical regions as well as in two Scutellospora species [155]. In contrast, endocellular bacteria
were not detected in different isolates of Gigaspora rosea.
The nature of the relationship between endocellular
bacteria and AM fungi is not clear. There were no indications that the bacteria had any negative effect on the
symbiotic efficiency of the AM fungus [156]. One study
suggested that the expression of nif (nitrogen fixation)
genes in germinating AM spores could indicate that
the bacteria are supplying the fungus with nitrogen during its pre-infective growth [157]. However, subsequent
studies have shown that this is probably not the case
(Bonfante, personal communication).
The close phylogenetic relationship of the endocellular bacteria in geographically separated AM strains and
in different AM species may indicate that bacterial
acquisition by these fungi was a unique event that
occurred in an ancestral fungus and has since then been
propagated by vertical transmission [155,158]. However,
more data on the identity of BLOs of other AM species
are needed before this idea can be fully evaluated.
Obviously, uptake of bacteria by fungi is a less common event than is uptake by protozoan bacterial predators, which utilize phagocytosis as a mechanism for
incorporating the bacterial cells. The fungal cell wall
as a physical barrier strongly tends to prevent acquisition of bacteria [155]. The wall is not rigid at the hyphal
tip [159], and bacterial acquisition may occasionally
804
W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
occur at this location. Such an event does, in fact, occur
with the fungus Geosiphon pyriforme, which is probably
a representative of a lineage ancestral to AM fungi [160].
This fungus incorporates primordia of free-living cyanobacteria (Nostoc) at the hyphal tips, which thereafter
swell and form bladders in which the Nostoc cells initiate
photosynthetic activity [161].
Another scenario for bacterial acquisition by fungi
could be the lysis of hyphal tips by bacteria, followed
by entry into the fungal mycelium (see Section 3.5). Related to this, a recent work reporting on invasion of AM
fungal spores by Burkholderia sp. is very interesting
[162]. These bacteria appear to invade germinating
spores via germ tubes that were weakened either by
the absence of a host plant or by the action of bacterial
lytic enzymes. In nature, similar events may occur; since
hyphae from germinating AM spores have been shown
to undergo programmed growth arrest and resource
reallocation as a strategy to maintain germination
capacity in the absence of a plant host [163]. The insides
of such retracting hyphae may be readily accessible to
bacteria [162]. It is possible that this type of event has
occasionally been the first step in the evolution of a lineage of endocellular bacteria.
If Ôfungal captureÕ of lytic bacteria, or bacteria that
enter damaged hyphae, is not uncommon, then the
possession of endocellular bacteria by fungi may be
a widespread phenomenon. The increasing number of
reports on the occurrence of endobacteria in fungi,
other than AM, seems to indicate that this may actually be the case [84,164–167]. Interestingly, the only
bacteria that have been indicated as endobacteria of
EM fungi belong to genera with the potential to
hydrolyse fungal cell wall polymers, e.g. Paenibacillus
and Cytophaga [164,166].
3.5. Mycophagy
Besides being competitors or suppliers of exudates,
living fungi may also serve directly as sources of nutrients for other microorganisms. A nutritional strategy
based on targeting fungi as a substrate is well known
for the so-called mycoparasitic fungi. Several studies
have addressed the mechanism and regulation of attack
on fungi by Trichoderma spp. [168–170]. The following
steps can be recognized: (1) chemotropic growth
towards the host fungus, (2) coiling around the host fungus and appressorium formation, (3) secretion of cell
wall degrading enzymes, (4) penetration and (5) degradation of hyphal content [168]. In a previous study, coiling around and penetration of a host fungus by a
Streptomyces strain was also described [171]. However,
with the exception of studies on penetration and killing
of living fungal spores no further attention appears to
have been paid to the occurrence of mycophagy in actinomycetes [172].
Lysis of fungal hyphae by non-filamentous bacteria
has, however, been observed frequently [173–177]. Studies on this topic concern the deformation or destruction
of hyphae of plant pathogenic soil fungi by potential
biocontrol bacteria. However, due to the artificial conditions used in most experiments, e.g. use of liquid nutrient broth and/or the use of damaged mycelium as
inoculum, it is often not clear whether the bacteria are
just feeding on nutrient broth and dead or damaged fungal material or are really able to attack intact fungal hyphae. Even if such an attack is found, it is not evident if
it would also occur in a nutrient-limited soil or soil-like
environment. These studies have revealed how fungal attack by unicellular bacteria might proceed. The fact that
almost all mycolytic bacteria produce polymer hydrolysing enzymes (e.g., chitinases, glucanases or proteases)
as well as antibiotics, indicates that this mixture of compounds may be crucial for degrading living hyphae.
Microscopic observations indicated that the initial bacterial attack proceeded via polar attachment of bacteria
to hyphae, followed by biofilm formation on the hyphal
surface [177,178].
Recently, a new bacterial genus, Collimonas, has
been described to be able to grow at the expense of living hyphae of different fungi in soil microcosms
[179,180]. These bacteria can be dominant among the
culturable, chitinolytic bacteria in fungal-rich, acidic
or sandy soils. The Collimonas strains appear to attack
the hyphal tip using a combination of lytic enzymes
(chitinases) and antibiotics. However, the exact mechanism of this attack, as well as the relative importance
of mycophagous growth, has yet to be elucidated for
these bacteria.
Myxobacteria are also likely to be mycophagous in
soil. These Gram-negative bacteria have been mostly
studied because of their social behavior during collective
food uptake, as well as the cooperative motility involved
in their fruit body formation [181]. They have been
termed micropredators due to their ability to destroy living soil microorganisms, in particular bacteria and
yeasts [182]. They produce various exoenzymes and secondary metabolites that appear to be involved in these
processes. Up till now, their ability to grow on filamentous soil fungi has not been studied intensively. In vitro
studies have revealed hat they can antagonize plant
pathogenic fungi as well as saprotrophic fungi [183].
Myxobacteria were indicated as responsible for perforation of Rhizoctonia sp. hyphae that had been buried in
soil [184]. In this study, myxobacteria isolated from
the buried hyphae were also shown to penetrate and to
empty out Rhizoctonia sp. hyphae in vitro.
Another group of bacteria for which mycophagy may
be important is the paenibacilli. These bacteria are
known for their extracellular lytic enzyme production
and have been shown to attack fungi in vitro
[177,185]. In addition, they are often isolated from the
W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
surfaces or even insides of fungal propagules
[88,116,162,164].
Bacterial pathogens of fungi may be considered as
a special group of mycophagous bacteria. The beststudied case is that of brown blotch disease of the cultivated mushroom (Agaricus bisporus) by Pseudomonas
tolaasii [186]. P. tolaasii grows as an organotrophic
bacterium in soils and composts but under certain
conditions it can attack hyphae in fruit bodies, where
the zones of attack can be recognized as brownish
spots. Several extracellular secondary metabolites, of
which tolaasin appears to be the most important,
are involved in membrane disruption releasing nutrients from within the fungus cells [186]. This attack initiates a cascade of events culminating in the
production of chemical barriers (melanins, quinones)
by means of which the fungus attempts to protect
the cells in the inner parts of the fruit body from
becoming infected.
Not only are there bacteria that feed on fungi, but
also there are fungi that are able to lyse and consume
bacteria [187]. It has been suggested that bacteria may
be an important source of nitrogen during fungal degradation of resources with a high C/N ratio, e.g. wood
[188]. Fungi with the ability to lyse bacteria appear to
be attracted by bacterial colonies. It has been speculated
that density-dependent control of antifungal gene
expression, which is apparent for several soil bacteria,
could be a strategy to defend bacterial colonies against
fungal attack [189]. This idea, however, has not been
experimentally examined yet.
3.6. Decomposition of fungal cell walls
Actinomycetes have long been considered to be the
major degraders of senescent fungal hyphae [190]. This
idea was primarily based on microscopic observations
of the colonization and degradation of fungal hyphae
growing on surfaces. It is known, though, that the use
of surfaces, such as glass slides, may introduce artefacts
that influence these events. On the other hand, it has
been shown frequently that stimulation of fungal growth
by substrate addition is later followed by an increase in
actinomycete densities after the decline of the fungal
activity [191]. In addition, the growth of potworms
(Enchytraeus albidus) feeding on fungi was enhanced
by gut-inhabiting streptomycetes that degraded the fungal cell walls [192]. Hence, it is certainly possible that
actinomycetes play an important role as degraders of
senescent fungal mycelium, but more research on the relative significance of different organisms is needed.
Besides actinomycetes, the soil dwelling myxomycetes
may also be important degraders of senescent fungal
mycelium [182]. Moreover, in wood, when one fungus
replaces another during community development [15],
it is highly likely that both intracellular and wall materi-
805
als are used by the invading organism, which is often
effectively a pure culture, in order to satisfy nitrogen
demands.
4. Perspectives
It will be clear to every soil microbiologist that
interactions between plants and bacteria have had a
strong impact on evolution and niche differentiation
of terrestrial bacteria. It is much less widely appreciated that terrestrial bacterial niche development may
for a large part have been determined by the development of fungi on land. Consideration of this scenario
may give rise to new ideas and concepts in soil microbial ecology.
The increasing availability of both fungal and bacterial genome sequences will undoubtedly provide a better
picture of the impact that fungi have had on bacterial
evolution. Of particular interest in this respect are horizontal gene transfer between fungi and bacteria (and
vice versa), evolution of antifungal compounds, detailed
comparison of fungal and bacterial genes involved in
cellulose degradation, and comparison of genomes of
fungus-associated bacterial strains with those of phylogenetically related free-living strains.
Investigation of fungally engendered bacterial
niches has only recently started, and has already provided exciting findings such as mycorrhiza-helper bacteria, endobacteria and mycophagous bacteria. Other
areas, such as interactions during degradation of recalcitrant organic matter, are almost entirely unexplored. With respect to the last topic, a further
extension of such investigations to aquatic environments is necessary as there is increasing evidence that
interactions between bacteria and fungi occur during
degradation of terrestrially derived organic matter,
e.g. leaves, that are sedimented into lakes and seas
[193,194].
The study of fungal-bacterial interactions in soils is
not only interesting from a basic point of view but
has also yielded findings of societal and economical relevance, such as the application of bacteria for the biocontrol of fungal plant diseases, the improvement of
mushroom cultivation procedures, and the controlled
stimulation of mycorrhizal infection. Better insight into
the co-existence mechanisms of soil bacteria and fungi
may lie at the basis of both new and improved applications. Bacteria that are harmful to fungi may potentially also form a source of new antibiotics with
therapeutic value. A better basic understanding of the
in situ competitive interactions between bacteria and
fungi will probably result in much more straightforward approaches than currently exist to screen for
new antibiotics and other valuable secondary
metabolites.
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W. de Boer et al. / FEMS Microbiology Reviews 29 (2005) 795–811
In summary, there is much to be gained from studying fungal–bacterial interactions and it is encouraging to
see that an increasing number of research groups have
started to explore this fascinating area of microbial
ecology.
[23]
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