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Modes of cell-wall degradation of Sphagnum
fuscum by Acremonium cf. curvulum and
Oidiodendron maius
A. Tsuneda, M.N. Thormann, and R.S. Currah
Abstract: Electron microscopy of cryo-fractured hyaline leaf cells of Sphagnum fuscum Klinggr. revealed that their cell
walls consist of three layers: a thick central layer flanked on either side by a thinner, amorphous layer. Acremonium cf.
curvulum W. Gams and Oidiodendron maius Barron, both isolated from partly decomposed S. fuscum plants, were capable of degrading leaf cell walls of Sphagnum. Where hyphae of A. curvulum accumulated, the amorphous, outer wall
layer of S. fuscum was first fragmented and then removed. The exposed central wall layer consisted of bundles of
microfibrils embedded in an amorphous matrix material. After the matrix material and the inner surface wall layer were
mostly removed, degradation of microfibrils occurred and localized voids were produced. Unlike A. cf. curvulum,
O. maius degraded all wall components more or less simultaneously. In both fungi, active and autolysing hyphae frequently occurred in proximity on the Sphagnum leaves.
Key words: hyphomycetes, peat, phenolics, cellulose, SEM.
Résumé : L’examen en microscopie électronique de cellules foliaires hyalines cryo-fracturées du Sphagnum fuscum
Klinggr. révèle que leurs parois cellulaires comportent trois couches; une couche centrale épaisse enveloppée de chaque
côté par une couche amorphe plus mince. L’Acremonium cf. curvulum W. Gams et l’Oidiodendron maius Barron, tous
deux isolés de plants du S. fuscum partiellement décomposés, sont capables de dégrader les parois cellulaires des sphaignes. Là où les hyphes de l’A. curvulum s’accumulent, la paroi externe amorphe du S. fuscum se fragmente avant
d’être enlevée. La couche centrale exposée de la paroi est constituée de faisceaux de microfibrilles, enrobés dans un
matériel matriciel amorphe. Une fois que le matériel matriciel et la couche superficielle interne ont été a peu près enlevés, il y la dégradation des microfibrilles et on y observe des vides localisés. Contrairement à l’A. curvulum,
l’O. maius dégrade tous les constituants de la paroi plus ou moins simultanément. Chez les deux champignons, on
retrouve fréquemment des hyphes actives ou en autolyse qui se voisinent sur les feuilles des Sphagnum.
Mots clés : hyphomycètes, tourbe, phénols, cellulose, SEM.
[Traduit par la Rédaction]
Tsuneda et al.
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Introduction
Peatlands are defined as ecosystems with at least 30–
40 cm of identifiable peat (Gorham 1991) and have been estimated to cover approximately 4% of the global, 12% of
Canada’s (National Wetlands Working Group 1988), and
16% of Alberta’s land base (Vitt et al. 1996). Peat is a conglomerate of partially decomposed plant material consisting
of approximately 50% carbon (Riley 1994), and its accretion
is the result of a low rate of plant decomposition rather than
a high rate of plant net primary production (Farrish and
Grigal 1988; Vitt 1990). Gorham (1990) estimated that boreal and sub-arctic peatlands store up to 455 Pg (1 Pg = 1 ×
1015 g) of carbon, which represents approximately one third
Received August 24, 2000. Published on the NRC Research
Press website on January 26, 2001.
A. Tsuneda.1 Northern Forestry Centre, Canadian Forest
Service, 5320-122 Street, Edmonton, AB T6H 3S5, Canada.
M.N. Thormann and R.S. Currah. Department of Biological
Sciences, University of Alberta, Edmonton, AB T6G 2E9,
Canada.
1
Corresponding author (e-mail: [email protected]).
Can. J. Bot. 79: 93–100 (2001)
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of the total global terrestrial carbon. Peatlands are considered to be some of the world’s most important ecosystems
(Gorham 1991).
Sphagnum species, dominant in ombrotrophic peatlands
(bogs), are of great importance in northern ecosystems because of their low decomposition rates, abilities to hold large
quantities of water, and abilities to acidify the surrounding
environment (Vitt and Andrus 1977). Fungi may be the
principal microbial decomposers in many acidic ecosystems,
such as bogs, and play a more dominant role than bacteria in
the degradation of plant remains (Latter et al. 1967). This
view is supported by the significantly higher biomass of
fungi compared with bacteria in the oxygenated horizon of
peatlands (acrotelm) (Collins et al. 1978; Wynn-Williams
1982).
A number of reports are available on fungi associated
with bryophytes, including those pathogenic to Sphagnum
(Redhead 1981; Redhead and Spicer 1981; Untiedt and
Müller 1985). Chastukhin (1967) suggested that some
basidiomycetous as well as hyphomycetous fungi, such as
species of Penicillium, Trichoderma, and Torula, are able to
decompose Sphagnum, based on mass losses and the release
of soluble nitrogenous compounds. There have been several
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Figs. 1–5. Branch leaves of Sphagnum fuscum (controls). Fig. 1. Scanning electron micrograph showing typical branch leaves with
abundant pores. Scale bar = 200 µm. Fig. 2. Cryo-fractured leaves attached to a stem (arrow). Scale bar = 100 µm. Fig. 3. Enlarged
view of a part of Fig. 2 showing hyaline cells. Arrows indicate fibrils. Scale bar = 20 µm. Fig. 4. Cryo-fractured cell wall of a hyaline
cell showing the three-layered structure consisting of a central and extremely thin, inner and outer surface layers. The arrow indicates
a sectioned fibril. Scale bar = 1 µm. Fig. 5. Sectioned cell wall of a hyaline cell viewed by TEM. Scale bar = 0.5 µm. Figs. 6–8. Degradation process of S. fuscum leaf cell walls by Acremonium cf. curvulum. Fig. 6. Overall view of an area where hyphae (H) accumulated and caused deformation of the leaf cell wall (arrow). Some hyphae are extremely fine. Scale bar = 10 µm. Fig. 7. Degradation of
the amorphous, outer wall layer (S). Arrows locate microfibrillar elements embedded in a matrix material. Scale bar = 0.5 µm. Fig. 8.
Enlarged view of a portion of Fig. 6. The arrow indicates microfibrillar elements. Note the wavy appearance of the leaf cell wall (arrowhead). H, hyphae. Scale bar = 2 µm.
ultrastructural studies on fungal colonization of bryophytes
(Dickinson and Maggs 1974; Grasso and Scheirer 1981;
Scheirer and Dolan 1983; Untiedt and Müller 1985). However, little is known about the abilities of specific fungi to
degrade bryophyte cell walls, and particularly, the mode of
degradation of cell wall components by fungi remains unknown.
While conducting a survey of the microfungi associated
with Sphagnum fuscum Klinggr., a hummock-forming peat
moss dominant in boreal bogs (Vitt and Andrus 1977), more
than 40 different species of fungi were isolated from living
and decomposing plants. Our preliminary experiments indicated that, of these, two hyphomycetous fungi, Acremonium
cf. curvulum W. Gams and Oidiodendron maius Barron
caused moderate, but significant, mass losses of S. fuscum.
The present ultrastructural study was undertaken to elucidate
the degradation processes of S. fuscum leaf cell walls by
these fungi.
Materials and methods
Acremonium cf. curvulum (CBS 102853) and O. maius (UAMH
9749) were isolated from partly decomposed plants of S. fuscum
from a bog, 5 km east of Perryvale, Alta. Peptone agar (PA) (20 g
agar (Difco, Detroit, Mich.), 1 g bacto-peptone (Difco), 1 L distilled water) was poured into 100 × 80 mm glass Petri dishes,
40 mL per dish, and six of these dishes were inoculated with one
of the fungi. A polyester mesh pouch (2.5 × 3.0 cm, 65 µm pore
size) containing the top 3 cm of four healthy-appearing S. fuscum
plants was placed in each of these dishes. Polyester pouches were
used to prevent the plants from direct contact with agar and from
physical damage during handling. All pouches were weighed and
autoclaved at 121°C (liquid cycle) for 15 min before introducing
them into the dishes. As controls, two of these pouches were
placed on uninoculated PA.
After 4 and 8 weeks, the pouches were removed from six Petri
dishes with the fungi (three dishes per fungus) and from a
nonfungus control dish, and the plants were removed from each
pouch. The top 5–7 mm of these plants were used for electron microscopy. In addition, healthy-appearing, living plants were used as
controls to examine whether the cell wall integrity of S. fuscum
was altered by autoclaving. Methods for fixation, dehydration, and
critical-point drying in specimen preparation for scanning electron
microscopy (SEM) were the same as those described in Tsuneda et
al. (1991), except that materials were immersed in 2% tannic acid
– 2% guanidine hydrochloride solution for 3 h before being postfixed in OsO4. Living and autoclaved control plants were examined
by cryogenic (low-temperature) SEM and transmission electron
microscopy (TEM). Cryo-fracturing was done in an Emitech K
1250 Sputter-Cryo cryogenic preparation system using the method
by Beckett and Read (1986). For TEM, material was fixed with 3%
glutaraldehyde for 2 h under a light vacuum, washed with phos-
phate buffer, and postfixed in 2% OsO4 for 2 h. Following the fixation, specimens were prepared as outlined in Tsuneda and
Murakami (1985). Scanning electron micrographs were taken either with a Hitachi S-510 or a JEOL JSM-6301 FXV fieldemission SEM, and transmission electron micrographs with a
Hitachi H-7000 TEM.
Results
Hyphal behavior and the degradation of leaf cell walls of
S. fuscum by the two test fungi were examined primarily on
the abaxial surface of branch leaves (Figs. 1 and 2). Hyaline
cells, dominant at the abaxial surface, had oval to elliptical
bordered pores and supporting bars, or fibrils (Figs. 3 and 4,
arrows). Cryo-SEM revealed that surfaces of hyaline cells
were smooth (Fig. 3) and the cell wall was three layered,
consisting of a thick central and an outer and an inner surface layer (Fig. 4). Both surface layers were distinguishable
under TEM as highly electron-dense layers. The central
layer, however, was divided further into at least three
sublayers with varying electron density: an electron-lucid
sublayer was flanked on either side by an electron-dense
layer (Fig. 5). Cryogenic SEM and TEM observations of the
specimens prepared from living and autoclaved control
plants revealed that autoclaving caused no visible alterations
in the cell wall structure and integrity.
Degradation of S. fuscum leaf cell walls by A. cf.
curvulum
Degradation of leaf cell walls by A. cf. curvulum was confined to the immediate vicinity of hyphae. The typical degradation process is shown in Figs. 6–10 (4-week incubation)
and in Figs. 11 and 12 (8-week incubation). Where fungal
hyphae accumulated (Fig. 6), swelling and degradation of
the outer surface cell wall layer occurred (Fig. 7), giving the
host cell wall a wavy appearance (Figs. 6–8). The outer surface wall layer first was fragmented (Figs. 9 and 10) and
then removed. The exposed central wall layer consisted of
microfibrillar elements that were embedded in an amorphous
matrix material (Figs. 7–12). Subsequently, the matrix material of the central layer as well as the inner surface wall
layer were largely removed and the microfibrillar elements,
which were more or less flexuous, became clearly visible
(Figs. 11 and 12). Progressive thinning of the central wall
layer resulted in the formation of localized voids (Figs. 8,
10, and 12, arrows).
Hyphal penetration of leaf cell walls was frequent. No visible sign of degradation or indentation was identifiable by
SEM in the leaf cell wall surrounding the penetration hypha
(Fig. 13, arrow). Hyphae occurring on the leaf surface varied
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Figs. 9–14. Degradation process of Sphagnum fuscum leaf cell walls by Acremonium cf. curvulum. Figs. 9 and 10. Enlarged views of
parts of Fig. 6 showing microfibrillar elements (arrows) between fractures of the surface wall layer. Hyphae (H) in Fig. 10 are in early
stages of autolysis. Scale bar = 1 µm. Figs. 11 and 12. Eight-week incubation. Microfibrillar elements exposed as the result of preferential removal of the amorphous surface wall layers. The amorphous matrix material has also been largely removed and the exposed
microfibrillar elements are more or less flexuous (Fig. 12). Note thinned, localized area (white arrow) in the microfibrillar layer and a
localized void (black arrow). H, hyphae. Scale bars = 2 µm (Fig. 11) and 1 µm (Fig. 12). Fig. 13. Penetration hypha (H). No sign of
degradation or indentation is seen in the leaf cell wall (arrow) around the hypha. Scale bar = 1 µm. Fig. 14. Erosion trough (black arrowhead). White arrowheads indicate autolysing hyphae. One of the sound hyphae is degrading the leaf cell wall (arrow). Scale bar =
3 µm.
in size and some of them were extremely fine, measuring
less than 0.5 µm in width (Figs. 6 and 8–14). As hyphae
aged, they often became swollen, lost turgidity, and finally
collapsed (Figs. 6, 8, and 10). Both sound and autolyzing
hyphae commonly occurred in areas where leaf cell wall
degradation was in progress (Fig. 14). An erosion trough
was sometimes found where hyphal autolysis had advanced
to the extent that the leaf cell wall beneath the hypha became visible (Fig. 14, solid arrowhead).
Degradation of S. fuscum leaf cell walls by O. maius
Obvious signs of leaf cell wall degradation by O. maius
were not observed in the specimens incubated for 4 weeks,
except that the wavy deformation of leaf cell walls (Fig. 15)
was frequent and more pronounced than in plants colonized
by A. cf. curvulum. Degradation of leaf cell walls was evident in 8-week specimens, but it was confined to areas
where hyphae accumulated, as in A. cf. curvulum. The affected walls often became distorted (Fig. 16, arrow). Unlike
A. cf. curvulum, which degraded the leaf cell walls in a sequential mode, O. maius degraded all wall components more
or less simultaneously, leaving localized voids (Figs. 17–19,
arrows). Therefore, microfibrillar elements were highly degraded by the time they became visible (Figs. 18 and 19). As
in A. cf. curvulum, both autolysing and sound hyphae often
coexisted, especially in the areas where leaf cell wall degradation was in an advanced stage (Figs. 16 and 19, arrowheads). Penetration of leaf cell walls by O. maius hyphae
was comparable with that observed in plants colonized by
A. cf. curvulum. Oidiodendron maius tended to produce
emergent aerial hyphae from colonized plant leaves that usually developed into conidiophores (Fig. 17, H).
Discussion
The present study revealed the three-dimensional cell wall
architecture of hyaline cells of S. fuscum leaves by examining their degradation processes by two hyphomycetous
fungi. The central layer of Sphagnum hyaline leaf cells consisted of fibrillar elements embedded in an amorphous matrix material and was flanked on either side by an
amorphous layer. The fibrillar elements are most likely bundles of cellulose microfibrils and other component materials
are contained in the amorphous surface and matrix parts of
the Sphagnum cell wall. In fact, the fibrillar elements closely
resemble cellulose microfibrils in delignified wood cell walls
(Tsuneda et al. 1991; Tsuneda and Thorn 1995).
Two types of wood cell wall degradation by white-rot
basidiomycetes have been recognized: (i) preferential type,
in which lignin is selectively removed prior to cellulose
breakdown, and (ii) simultaneous type, in which all wall
components are degraded more or less simultaneously
(Otjen and Blanchette 1986; Eriksson et al. 1990; Tsuneda
and Thorn 1995). Likewise, two types of fungal degradation
of Sphagnum leaf cell walls were recognized in the present
study. The mode of degradation by A. cf. curvulum resembles the preferential type, because it first removes the amorphous cell wall components and then degrades microfibrillar
elements, whereas O. maius causes a simultaneous degradation. The microfibrillar elements were more or less flexuous
when they became visible by the action of A. cf. curvulum.
This indicates that the tensile strength of microfibrillar elements had decreased. The mechanism for the loss of strength
is unknown in Sphagnum, but in wood it is apparently
caused by the degradation of the encompassing
hemicelluloses, especially the xylan constituent (Asunmaa
and Schwab 1965).
Lignin peroxidases of some white-rot basidiomycetes can
diffuse into wood (Blanchette et al. 1989) and cause extensive delignification in wood elements without direct contact
with fungal hyphae (Tsuneda et al. 1991). Unlike white rot
of wood, degradation of the Sphagnum leaf cell walls by either A. cf. curvulum or O. maius was limited to the areas adjacent to, or in direct contact with, hyphae. The highly
confined nature of leaf cell wall degradation by these fungi
is best illustrated by the direct hyphal penetration that
caused no visible sign of indentation or degradation in the
leaf cell wall surrounding the site of penetration. Untiedt and
Müller (1985) observed a similar phenomenon in the colonization of Sphagnum fallax (Klinggr.) Klinggr. cells by the
parasitic fungus Lyophyllum palustre (Peck) Singer: penetration holes were generally smaller than the penetrating
hyphae, because hyphae became constricted at the point of
penetration. Obviously, the direct penetrations in these cases
were accomplished by a process of simultaneous enzymatic
digestion of host cell wall components in advance of the
hyphal tips, where production of extracellular enzymes is
generally most active.
Mechanisms that bring about resistance of the Sphagnum
cell wall to microbial degradation are not well known
(Dickinson and Maggs 1974). Traditionally, it has been attributed, in part, to the chemical characteristics of the Sphagnum cell wall, such as the inhibitory phenolic compound
“sphagnol” (Czapek 1899) and an unusual form of lignin
containing p-hydroxyphenyl units (Lindberg and Theander
1952; Farmer and Morrison 1964). More recently, the presence of lignin in Sphagnum cell walls was debated because
of the absence of typical β-O-4- and phenylcoumaran 13CNMR signals (Nimz and Tutschek 1977) and the lack of
methyl-substituted phenolics in the oxidation products of
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Figs. 15–19. Degradation of S. fuscum leaf cell walls by Oidiodendron maius. Fig. 15. Affected cell wall showing finely wavy deformations (arrows). Scale bar = 3 µm. Fig. 16. Severely distorted leaf cell wall (arrow). Note autolysing hypha (arrowhead) and degraded
leaf cell wall in the immediate vicinity. H, hyphae; C, conidia. Fig. 17. Localized voids (arrows) and hyphae (H) emerged through the
leaf cell wall. Scale bar = 5 µm. Fig. 18. More or less simultaneous degradation of the leaf cell wall by a hypha (H). Arrows indicate
localized voids. Fig. 19. Enlarged view of an area showing the simultaneous type of degradation (arrow). Arrowheads point to
autolysing hyphae. H, sound, turgid hyphae. Scale bar = 2 µm.
Sphagnum mosses with alkaline CuO (Williams et al. 1998).
Instead, two phenolics unique for Sphagnum, sphagnum acid
(p-hydroxy-β-[carboxy-methyl]-cinnamic acid) and hydroxybutenolide, as well as p-hydroxybenzoic acid have been regarded as the principal components that are functionally
similar to lignin, because (i) all of these phenolics are incorporated in the Sphagnum cell walls at later stages in the cell
wall differentiation and (ii) as the incorporation proceeds,
the histochemical detection of cellulose in the cell wall is
masked and resistance of the cell walls to enzymatic degradation is increased (Nimz and Tutschek 1977; Tutschek et
al. 1978; Wilschke et al. 1989; Rasmussen et al. 1995). Our
results agree with the results of the histochemical study by
Tutschek et al. (1978). It is likely that phenolics are contained in the amorphous surface and matrix of the Sphagnum
cell wall and that the amorphous components provide a
physicochemical barrier for microorganisms and their
cellulases to gain access to cellulose. Thus, the ability to degrade the amorphous components, especially phenolics, may
be a prerequisite for microorganisms to utilize Sphagnum
cell walls as their nutrient source.
Peat, like wood, is largely nitrogen deficient, being composed of empty cells whose major cell wall constituents are
cellulosic and phenolic compounds. This feature alone
makes Sphagnum unsuitable for microbial decomposition.
Conversely, fungal cell walls are rich in nitrogen, because
their principal material, chitin, is a homopolymer of Nacetyl-glucosamine (6.9% N). Tsuneda and Thorn (1995)
stated that during wood degradation, fungal cells, including
cell walls, serve as a significant reservoir of nitrogen, which
probably is recycled through parasitic and (or) scavenging
activities among different organisms as well as through the
process of autolysis and reuse (Levy et al. 1968; Lilly et al.
1991) within the same organism. In the present study, we
observed that both active and autolysing hyphae frequently
co-occurred in localized areas on Sphagnum leaves, especially where leaf cell wall degradation was evident (Figs. 8,
14, and 19); this suggests that the “autolysis and reuse”
mechanism is probably operative during the leaf degradation
process by both A. cf. curvulum and O. maius.
Finally, it should be noted that autoclaving may have altered the biochemistry of the Sphagnum cell walls, although
it did not cause discernible changes in their external morphology. A milder means of sterilization, such as gamma irradiation, may provide a more accurate view of the fungal
degradation process in Sphagnum.
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