f u n g a l b i o l o g y r e v i e w s 2 4 ( 2 0 1 0 ) 6 8 e7 2
journal homepage: www.elsevier.com/locate/fbr
Review
Fungi and paper manufacture
Russell J. JERUSIK*
Ashland Hercules Water Technology, Research Center, 500 Hercules Road, Wilmington, Delaware 19808-1599, United States
article info
abstract
Article history:
Fungi have a significant impact on the economics of paper making and the end use of paper
Received 14 September 2009
and products employing paper related components. Paper on a practical basis is a deriva-
Received in revised form
tive of wood, and fungi that possess cellulose-degrading enzymes can directly impact the
8 April 2010
value and utility of various types of products. Fungi further have a negative economic
Accepted 10 April 2010
impact on the pulp produced during paper manufacture. Contamination by fungi impacts
on the quality and often the safety of the product to the end user. Packaging materials used
Keywords:
in warm humid climates can be infested with mold which impacts the value and safety of
Cellulase
the packaged product. Building materials whether gypsum wall board, the paper-facing on
Fungicides
insulation materials, or ceiling tiles can sustain fungi and cause numerous problems.
Paper
These fungi create an aesthetic, functional and ultimately, a safety issue to the occupants
Paper degrading fungi
in a mold infested dwelling. Fungal spores are linked to allergy, asthma, and various
Paper manufacture with fungal
pulmonary related disorders. In the U.S., 3e5 million tons of scrap wall board end up in
enzymes
landfills every year which can also create fungal environmental problems. This review
article will describe these problems and strategies to minimize the adverse impact on
paper by fungi. However, fungi are also utilized in a beneficial manner to enhance paper
manufacture by removing detrimental components in paper and can aide in its production.
ª 2010 The British Mycological Society. Published by Elsevier Ltd. All rights reserved.
1.
Introduction
This review considers the role of fungi in paper manufacture.
There is a beneficial role as well as the expected deleterious
impact of fungi on paper. Fungi are utilized to remove free
and esterified steroid ketones that prevents the formation of
detrimental pitch in Eucalyptus wood (Martinez-Inogi et al.,
2001). Pitch is low molecular weight oleophilic material which
deposits during paper manufacture causing holes in the paper.
The various approaches to the usage of fungi to remove undesirable components of wood to make paper will be described.
Enzymes also attack hemicellulose favouring desired depolymerization (Suurnakki et al., 1997). Fungi also play a positive
role in the actual process of making paper. Biobleaching
reduces the usage of conventional bleaching chemicals and
improves pulp and eventual paper quality by improving
brightness, breaking length, burst index, tear index, and
manufacturing yield (Jimenez et al., 1997). This is accomplished with enzymes of fungal origin, such as xylanases
(Sandal et al., 1997). Environmental benefits are derived from
the reduction in chemical usage reducing effluent toxicity
and pollution load. Filamentous fungi can be used as a raw
material to make high gloss paper with acceptable writing
and printing qualities (Yamanak et al., 1992; Van Horn and
Shema, 1957).
Fungi can also cause severe problems for the paper manufacturer and in the end product. Wet pulp is a source or raw
material for the manufacture of paper and in 2007, 40.4 million
* Tel.: þ1 302 995 3177.
E-mail address: rjjerusik@ashland.com
1749-4613/$ e see front matter ª 2010 The British Mycological Society. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.fbr.2010.04.003
Fungi and paper manufacture
69
tons were shipped around the world. Pulp production involves
adding large amounts of water to produce the pulp and significant energy is needed to remove the majority of the water
content to minimize fungal infestation which can dramatically
decrease the economic value of the pulp. Today there is a great
emphasis on the use of re-cycled fibre for environmental
reasons and these fibres are often heavily contaminated with
organic matter increasing the tendency for mold growth.
2.
Fungi as part of the paper making process
While commercial products exist to remove pitch from wood,
Martinez-Inogi et al. (2001) improved on the process by finding
fungi that were able to remove both free and esterified sitosterol. A 1e2 week treatment with either Phlebia radiata or Poria
subvermispora enabled a 70 % removal of sterols with only
a moderate wood loss of 1e4 %. Biobleaching utilizes enzymes
to prepare pulp for paper making. Improvements are documented in brightness, kappa index, yield, breaking length,
burst index, and tear index with xylanases the most
frequently used enzymes (Jimenez et al., 1997). A commercial
recombinant xylanase enhances the brightness of the
bleached pulp reducing the amount of chlorine typically
used in conventional treatments (Sandal et al., 1997) providing
an improved process from an environmental standpoint. The
paper making process often leads to the production of toxic
organochlorine compounds due to the use of chlorine based
oxidizers during paper bleaching. Bajpai and Bajpai (1997)
identified fungal enzymes capable of removing such chemicals from bleach plant effluents.
Research has also shown that fungi can be used to biopulp
wood. Wood is debarked, chipped and steamed, reducing the
natural microbial flora. The material is then inoculated with
the biopulping fungi and the piled chips ventilated with
filtered and humidified air for 1e4 weeks. This process can
provide an energy savings of at least 30 % and also increases
mill output up to 30 % as well as increasing paper strength
of the finished paper (Shukla et al., 2004).
In addition, fungi can be a raw material to make paper.
Fungal mycelium and conventional fibres are combined to
strengthen the paper and this combination is particularly
useful when re-cycled fibres are used. Yamanak et al. (1992)
cultured Fusarium solani with broadleaf tree pulp at 28 C for
2 days after which the culture was filtered and washed to
retain the fibre mycelium complex. A 1954 patent describes
in detail the manufacture of highly flexible, high gloss paper
with acceptable printing and writing qualities with fungal
mycelium making up 10 % of the paper content. In addition,
a transparent paper also possessing acceptable printing and
writing properties contained 90 % fungal mycelia (Van Horn
and Shema, 1957).
3.
Fungal destruction of paper
Fungi perform an important ecological role in the decay of
paper and is historically problematic for the paper industry
(Acree, 1915). A family of enzymes are known to participate
in the breakdown of cellulose into glucose. The mechanism
Fig. 1 e Mechanism of cellulose degradation.
of cellulase activity as portrayed in Fig. 1 was elucidated by
Matthew et al. (2008).
Other researchers have shown variations in the cellulases
produced depending on the fungal species (Bhat and
Maheshwari, 1987) and at least eight different families of
cellulases have been identified (Samejima and Kiyohiko,
2004). The most common fungi associated with paper degradation are shown in Table 1.
This fungal destruction of cellulose can have a serious
impact on the manufacture of paper. Re-cycled pulp is
becoming a more common source for the manufacture of
paper and packaging material for ecological and economic
reasons. Re-cycled pulp is often stored in less than optimal
conditions from the perspective of preventing mold infestation and is often contaminated with food materials. Paper
manufactured with mold adulterated pulp can suffer a 50 %
loss in strength and losses in brightness in the finished
product (Meng, 1998) (see Figs 2 and 3). These data compare
fresh material with pulp stored either covered or uncovered.
The reduction of ring crush/basis weight indicates a lower
strength to the finished packaging material (Fig. 3).
The below photograph provides an example of a Penicillium species growing on pulp (Fig. 4).
Paper/cardboard constructed products, either building
material or packaging materials, can be compromised by
fungal decay. This fungal decay can impact on the value,
utility, and safety of the final product. Gypsum wall board in
the United States is utilized in nearly 90 % of interior finished
surfaces in buildings based on an EPA study. This same study
estimated that 40 % of all homes in North America have fungal
Table 1 e Fungi that degrade papera
Penicillium citrinium
Aspergillus niger
Sporotrichum thermophile
Trichoderma reesei
Penicillium pinophilium
Chaetomium globosum
Aureobasidium pullulans
a Fungi noted in ASTM protocols for testing degradation to paper
products.
70
R. J. Jerusik
Fig. 2 e Strength loss due to bio-deterioration of re-cycle
pulp beverage box containers.
contamination problems (Figs 5 and 6). The rapid growth and
dispersion of mold spores can induce allergy and asthma
episodes for the occupants. These health effects can be even
more serious with immunological, pulmonary and even oncogenic disorders. Manufacturers have responded to this
problem by making mold resistant gypsum wall board. Two
strategies are currently employed to overcome this problem.
The first is the conventional incorporation of fungicides to
the wall board and various commercial fungicides are available and are used commercially (Table 2). These fungicides
are used in packaging materials, the paper-facing of home
insulation, and on the coatings of paper-based ceiling tiles.
The other strategy is to replace cellulose based materials
susceptible to fungal growth with materials that are resistant.
One manufacture of gypsum wall board replaces the paper
with a glass mat resulting in a product with reduced susceptibility to fungal infestation. However, this material performs
differently than conventional gypsum wall board for the end
user, specifically in the effort required for cutting and has to
be handled in a more labour intensive manner compared to
conventional wall board and is a major technical drawback
to this strategy.
A patent from 2007 for manufacturing cellulose fibre with
biocides, such as quaternary ammonium and bromide
providing increased biostability to fungal attack (Jewell and
Reimer, 2007). Murtoniemi et al. (2003) studied the influence
Fig. 4 e Pulp contaminated with mold.
of composition on the growth of Stachybotrys chartarum on
gypsum wall board. Wall board was made without starch in
the core and liner or if the gypsum core was desulfurized
showed inhibited fungal growth. Incorporated biocides while
functional however, led to the production of spores with
even higher cytotoxicity to animal cells. Another study examined the influence of various fillers such as kaolin and titanium dioxide on fungal growth, staining and actual decay of
the paper Nyuksha (1969).
Natural products such as essential oils from clove and
cinnamon and oregano are reported to retard fungal growth
(Rodriguez et al., 2007). Serano et al. (2005) (Fig. 7) fungi can
affect paper in more subtle ways than the overt destruction
of the cellulose content. Art work and historical documents
Summer 2000
Summer 2001
0.350
0.300
Ring
0.250
Crush/
Basis 0.200
Weight 0.150
0.100
0.050
0.000
Fresh
Market
Bales
One Year
Covered
Storage
One Year
on Slab
Fig. 3 e Impact of fungal deterioration on cardboard quality.
Fig. 5 e Wet Lap contaminated with mold.
Fungi and paper manufacture
Fig. 6 e Mold growing on gypsum wall board during an
antifungal evaluation.
can be adversely impacted by fungi due to the production of
coloured pigments that stain and permeate the paper.
Szczepanowska and Lovett (1992) investigated several factors
that influence stain production by several fungi growing on
paper. Temperature, pH, and light were varied with four
fungal strains (Chaetomium globosum, a very active degrader
of paper, Fusarium oxysporum, Alternaria solani, and Penicillium
notatum) and the outcomes were scored based on the degree
of visible staining of the paper. The affect of pH was examined
between 5 and 8 with acidic conditions favouring fungal
growth at pH 5.0 were the stain production was most
pronounced. A notable exception was C. globosum which
produced staining equally at all pH’s tested. Stain production
for the other three test fungi followed a direct correlation with
pH with no stain produced at pH 8.0. Growth did occur to
varying degrees at the elevated pH’s for the three fungi. A. solani did not grow at pH 8.0 while P. notatum and F. oxysporum
grew to equal degrees independent of the pH being acidic or
basic. Temperature and its impact on fungal growth was
studied extensively by Wolf and Wolf (1947). This work
showed that temperatures at 30 and 50 C fungi grew poorly
and also at the elevated temperatures of 30 and 37 C.
Optimal growth was evident between 22 and 29 C. In
comparison, the study by Szczepanowska and Lovett (1992),
none of the four strains grew at 40 C. C. globosum was unique
in growing the best at 37 C. The other 3 test fungi were
Table 2 e Examples of commercially available fungicides
TCMTB
Sulfone
MBTC
TBZ
Zinc or Sodium
Omadine
Quats
Ziram
IPBC
Carbendazim
Iso
2-(Thiocyanomethylthio)benzothiazole
(Diiodo-methyl p tolylsulfone)
(Methylene bisthiocyanate)
(Thiabendazole)
(Pyrithione)
(Quaternary amine surfactants)
(Zinc dimethyldithiocarbamate)
(3-iodo 2 propynyl butylcarbamte)
(Methyl 1H-benzimiazol-2-carbamate)
4,5 dichloro-2-n-octyl-4-isothiazolin-3-one
71
Fig. 7 e Control of mold with eugenol after 16 d of storage
at 2 C.
adversely affected by the elevated temperature, P. notatum
was unable to grow and while growth was inhibited for
F. oxysporum and A. solani. The last physical parameter examined was the influence of light on fungal growth on paper.
Wolf and Wolf (1947) also looked at light and found both stimulatory and inhibitory influences were evident with different
fungi. In the study by Szczepanowska and Lovett (1992), light
was a positive influence on both growth and stain production.
Stain production by F. oxysporum was enhanced with light
exposure compared to growth in the dark. Szczepanowska
and Lovett (1992) also examined the use of solvents to remove
stains on paper as a possible remedial treatment for fungal
stained paper. The principal pigments responsible for the
staining by the four test fungi were characterized. Citronen
and xanthocillin are yellow coloured antibiotics produced by
P. notatum (Rothe, 1950; Wolf and Wolf, 1947). Chaetomidin
is a pigment extracted from Chaetomium species and was
found to be identical to oosprein from Oospora colorans
(Itabashi et al., 1955). Intracellular anthraquinine-like black
pigments from Alternaria have been isolated and identified
as altersolanols (Stoessl, 1969; Zaprometova et al., 1971).
General characterization of fungal stains by Stoessl (1969)
suggest a resemblance to humic acids and melanins. While
numerous solvents were utilized to assess stain removal,
very limited success was observed. The exceptions were 1,4dioxane which was able to completely remove the stains of
F. oxysorum and removed most of the staining caused by C. globosum and P. notatum. N,N dimethylformamide significantly
removed the stains caused by C. globosum and P. notatum.
Papers after drying were tested for any adverse impact on
paper quality and no detectable changes in wet tensile
strength or sizing was measured. These solvents have both
flammability and toxicity issues relevant their usage.
4.
Conclusions
This review highlights the positive and negative impact that
fungi can impose on paper. The destructive aspects of fungi
are daily real consequences that impose severe financial
72
impact to paper manufacturers and subsequently cause
health issues for people when these materials become colonised due to the release of fungal spores into contained indoor
environments. While incorporation of fungicides are aimed at
reducing the negative impacts of fungal growth, continuing
effort will need to continue to elucidate new approaches to
curb the negative impact of fungi on paper both during the
manufacturing process and post production.
Acknowledgements
Thanks Linda Chaney, Christopher Davis, Kurt Bottjer and
other Ashland Hercules Water Technology personnel for their
assistance in providing information for this review.
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