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The revenge of time: Fungal deterioration of

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Environmental Microbiology (2012) 14(3), 559566
Minireview
The revenge of time: fungal deterioration of cultural
heritage with particular reference to books, paper
and parchment emi_2584 559..566
Katja Sterflinger1* and Flavia Pinzari2
1
University of Natural Resouces Life Sciences Vienna,
Department of Biotechnology, Muthgasse 11, 1190
Vienna, Austria.
2
Istituto Centrale per il Restauro e la Conservazione del
Patrimonio Archivistico e Librario. Laboratorio di
Biologia, Via Milano 76, I-00184 Rome, Italy.
Summary
Hyphomycetous fungi so called mould are
the most important agents of biodeterioration in
museums, museums storage rooms, in libraries, col-
lections and restoration studios. Fungi are able to live
at low water activities, they are perfectly adapted to
indoor environments and thrive in microclimatic
niches caused by condensation, lack of ventilation or
water retention by hygroscopic materials. Fungi spoil
valuable pieces of art aesthetically, mechanically,
chemically and by degradation of organic compo-
nents. Historical material made of paper and oil paint-
ings with high amounts of organic binders are
especially susceptible to fungal deterioration. In order
to prevent fungal contamination or to treat already
contaminated objects an integrated approach includ-
ing climate control, material-specific cleaning and
application of carefully selected biocides is necessary.
Introduction
The connection between mould and cultural heritage has
a long history which includes some myths and mysteries:
The so-called curse of the pharaoh the death of several
archaeologists in the team of Howard Carter after discov-
ery and opening of Tutankhamuns tomb was later
explained by the fact that spores of the pathogen fungi
Aspergillus niger and Aspergillus flavus were found on
Received 15 April, 2011; accepted 6 August, 2011. *For correspon-
dence. E-mail katja.sterflinger@boku.ac.at; Tel. (+43) 1 47654 6260;
Fax (+43) 1 47654 6675.
2011 Society for Applied Microbiology and Blackwell Publishing Ltd
doi:10.1111/j.1462-2920.2011.02584.x
and in the sarcophagi and that a lung infection or other
systemic mycosis Aspergillosis was the possible
reason for death. Although there is no statistical evidence
for an accumulation of disease in connection with the
archaeological findings and no real scientific proof for
Aspergillosis as the main cause of discoverers death
there is some truth underlying this story:
(i) Mould always was and still is threatening materials
including historical and contemporary material of
objects of art in libraries and in museums (Nittrus,
2000a; Koestler et al., 2003; Allsopp et al., 2004;
Capitelli et al., 2009; Mesquita et al., 2009; Pangallo
et al., 2009; Sterflinger, 2010). Fungi are also found
on mural paintings in churches, in caves and in cata-
combs and even as biodeteriogens of architectural
surfaces and stone monuments (Sterflinger, 2000;
Saarela et al., 2004; Piar and Sterflinger, 2009;
Ettenauer et al., 2010; Steiger et al., 2011). The oldest
and most precious objects suffering from serious
fungal invasions are rock art caves as for example
Lascaux in France (Bastian and Alabouvette, 2009).
Fungi cause serious esthetical spoiling of paintings,
sculptures, costumes, ceramics, mummies, books
and manuscripts. Due to their ability to form hyphal
networks they penetrate materials deeply, resulting in
material loss due to acid corrosion, enzymatic degra-
dation and mechanical attack. Cleaning and decon-
tamination of infected artefacts, exhibition rooms and
depots account for high expenditures for museums.
The cultural and historical value of many paintings,
books and manuscripts is inestimable and thus cannot
be expressed in terms of money.
(ii) Fungi in libraries, museums and their storage rooms
can seriously threaten the health of the restorers, of
the museum personnel and of the visitors due to their
allergic potential, due to the production of mycotoxins
but also due to their ability to cause systemic infec-
tions in humans (Crook and Burton, 2010). Airborne
fungal spores in storage rooms of museums can well
reach levels of more than 8000 per m3 including fungal
560 K. Sterflinger and F. Pinzari
pathogens such as Aspergillus flavus and Stachybot-
rys chartarum (K. Sterflinger, unpubl. data). The
health risk for restorers and other museum personnel
is evident is such cases.
Both, the deteriorative and pathogenic potential of fungi
have consequences for the handling of objects, their con-
servation, their cleaning and their storage as well as for
the occupational safety and health of museum personnel.
Detection and identification of fungal taxa on paper
and parchment
Currently, and based on phylogenetic studies, the fungal
kingdom is subdivided into five valid divisions (James
et al., 2006): the Chytridiomycota as representatives of
many secondary aquatic fungi. The Glomeromycota live in
symbiosis with plant roots and have little or no importance
in biodeterioration of museum materials. The Zygomycota
comprise many important biodeteriogens of grain, fruit
and vegetables. They sometimes occur on museum mate-
rials as opportunists. The Basidiomycota include most of
the mushrooms and toadstools. The most important wood
decaying indoor fungus Serpula lacrymans belongs to
Basidiomycota and causes damages in churches and his-
torical buildings made of wood (Bech-Andersen and
Elborne, 2004) (Fig. 1). Most of the mould species playing
a role in the deterioration of cultural heritage belong to the
Ascomycetes. Mould is a term applied for the asexually
reproducing forms the Anamorphs in contrast to the
fungi producing spores by sexual reproduction the
Teleomorphs.
The diversity of fungi in the museum environment is
very similar to the diversity of food and indoor fungi in
general (Samson et al., 2010). The most important fungal
Fig. 1. Historical wood working tools in a turnery of a Carthusian
cloister in Austria destroyed by the dry rot fungus Serpula
lacrymans. (Sterflinger).
2011 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 14, 559566
genera found in museums are Alternaria, Aspergillus,
Absidia, Acremonium, Cladosporium, Chaetomium, Chry-
sosporium, Eurotium, Fusarium, Geotrichum, Penicillium,
Paecilomyces, Epicoccum, Phoma, Cunninghamella,
Emericella, Scopulariopsis, Stachybotrys, Trichoderma
and the yeast genus Rhodotorula with a high affinity to
osmotic environments. Some so called black yeasts and
microcolonial fungi, as for example Exophiala, Aureoba-
sidium, Coniosporium and Wallemia are frequently found
in association with materials of high osmolarity (wall paint-
ings) or containing hydrocarbons, tensides, silicone or
paraffin waxes. The fist database for microbes associated
with cultural heritage including bacteria, archaea and
fungi is currently built up at the University of Natural
Resources and Life Sciences Vienna: http://www.
biotec.boku.ac.at/acbr-chm-catalogue.html.
From the biodeterioration point of view the fungi on
cultural heritage items can be divided into two main func-
tional groups: (i) opportunistic fungi that are growing on
practically all types of materials if there is sufficient humid-
ity. These fungi are not able to degrade the material enzy-
matically and to use it as main source of carbon, and (ii)
real material pathogens that are substrate specific and
able to degrade specific materials of works of art such as
cellulolytic fungi on paper and keratinolytic fungi on
leather, hair and feathers (Meier and Petersen, 2006;
Blyskal, 2009). Both groups may cause serious deterio-
ration but only fungi belonging to the second group can
decay the material itself.
In the daily routine of most microbiology groups working
in close collaboration with museums, the identification of
mould isolated from museum material is still based on
morphological studies using appropriate identification
keys for different taxonomic groups (Klich, 2002; Pitt,
2000; Domsch et al., 2007; Samson et al., 2010).
However, reliable identification with resolution of closely
related species is based on multilocus sequence analysis
including 18S rDNA, 26S rDNA and the Internal Tran-
scribes Spacer Regions 1 and 2, the actin-, TEF1-,
tubulin- and calmodulin- genes (Martin and Rygiewicz,
2005; James et al., 2006; Crous et al., 2007; Samson and
Varga, 2007). The ITS region is discussed as the most
suitable candidate for DNA based bar coding despite of
the fact that this region does not resolve all mould species
(Seifert, 2009). A comprehensive list of taxon specific
primers for fungi can be found in the Fungal Tree of Life
Website (http://www.aftol.org).
In order to detect also the non-cultivable fungal portion
of the fungal community or to analyse an extinct fungal
contamination as a retrospective on the objects history,
molecular fingerprints are carried out based on PCR-
amplification of DNA from material samples. The method
most frequently used to analyse paper and parchment is
Denaturing Gradient Gel Electrophoresis (DGGE). The
 Fungi and cultural heritage 561

amplified rRNA genes or ITS sequences (Michaelsen

et al., 2009; 2010) from different fungal species reveal
different electrophoretic patterns of migration. As a con-
sequence, the fungal community of a sample can be
visualized by its electrophoretic profile. This allows the
analysis of the microbial diversity of a specific sample, its
comparison with the fingerprint from other samples, and
the evaluation and/or monitoring of sites and temporal
series. Real-time PCR, in addition, allows quantification of
single species or higher taxa on and in the samples.
Recently, the application of reverse transcriptase PCR is
optimized for its use to measure the activity of the fungi on
paper and parchment as well as to monitor the expression
of single genes that are responsible for the deteriorative
activity (e.g. genes encoding cellulase). This will help to
understand the processes of fungal biodeterioration as a
major basis to elaborate and optimize the prevention and
treatment methods.

Origin of fungi in museums and reasons for growth

Mould distribution in the environment is when mostly

hydrophobic spores and conidia are released and easily
transported by wind and by air flow. Fungal spores are
ubiquitous and materials are constantly exposed to fungal
infection in all indoor and outdoor locations. For this
reason fungal infection of cultural heritage materials is
mostly airborne with significant seasonal variations
and high numbers of spores can accumulate in dust
layers (Kaarakainen et al., 2009). Germination of spores
and development of colonies is determined by the chemi-
cal composition of the material itself and by the environ-
mental factors including temperature, humidity and
airborne nutrients like aromatic substances, dust,
carbon hydrates. Water availability is the most important
factor and the main reason why fungi in museums are
predominant when compared with bacteria or archaea:
Many fungi are able to grow at much lower levels of
humidity with some xerophilic and xerotolerant species
such as Eurotium sp., Aspergillus sp. or Wallemia sp.
growing at water activity > aw 0.6. Water availability of
above aw 0.8 already allows growth of a wide variety of
airborne fungi. In museums the range of 55 % RH is
generally regarded as the border line for fungal growth
and thus climate control is adjusted below this value;
however, with a high complexity regarding micro-niches,
temperature gradients and air flow inside of exhibition and
storage rooms (Camuffo, 1998). Poor ventilation and
surface temperature dishomogeneity can produce water
condensation points and local micro-climates with higher
water availability than in the rest of an indoor environ-
ment. These circumstances are favourable to some fungal
species; as a result these are able to proliferate in places
where the overall environmental conditions would other-
Fig. 2. Volumes stored in compactus-type shelving units and
affected by mould in an Italian public library (Pinzari).
wise appear to be hostile to microbial life. This is the case
of monospecific infections inside compactus shelving
(Fig. 2), which were attributed mainly to fungal species
belonging to the Eurotium genera like Eurotium halophili-
cum (Montanari et al., 2010) or other xerophilic species
(Pinzari and Montanari, 2011). The micro-climate created
inside of such compact shelves or by wrapping of objects
into plastic foils or extremely tight boxes thus not allowing
an exchange of air and vapour are the most important
reasons for heavy mould infections of collections. A fungal
colony can grow up to 4 mm day-1 and an outburst of fungi
can contaminate a whole collection within just a few days.
Historical artefacts are especially susceptible to biode-
terioration because many of them contain a variety of
organic compounds serving as carbon source for fungi:
Paints were made of mineral pigments dispersed in
organic binders such as egg yolk, casein, oil or different
resins (Fig. 3). Linen canvas clamped on wooden frames
served as painting ground and was often primed with
animal glue before painting. Ceramics contain residues of
foodstuff that serves as fungal food thousands of years
later (Fig. 4). Sculptures and other art objects carry
dcors made of textiles, leather, straw, clay, natural hair or
feathers. The most precious documents of humankind are
books, manuscripts and scrolls made of paper, papyrus
and parchment often containing considerable amounts of
starch paste used as adhesive for mounting (Fig. 5).
Fungi due to their remarkable ability to grow at low aw

2011 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 14, 559566
562 K. Sterflinger and F. Pinzari

Fig. 5. Book page in a 15th century bound volume from a historical

Fig. 3. Fungal infection of an oil painting in a museum storage
room. Fungi stared infection on the backside of the painting, and
then penetrated canvas and paint layer (Sterflinger).
values and to excrete a wide variety of exoenzymes
cellulases, glucanases, laccases, phenolases, kerati-
nases, mono-oxygenases and many more are the most
important agents of deterioration in museums., collection
and libraries.
Fungal biodeterioration of books,
paper and parchment
Books and documents are composite objects made
mainly of organic compounds. Paper is based on cellu-
lose which in natural environments represents the major
source of energy for microorganisms (Florian, 2002), and
parchment is made of collagen which is rich of nitrogen
and therefore easily degradable by microorganisms, like
filamentous bacteria and proteolytic fungi. The storage of
books and documents inside structures destined to their
preservation has created new, manmade environments
cloister in Salzburg, Austria. The books were contaminated and
decayed by fungi after water damage (Sterflinger).
for fungal and microbial species to inhabit (Kowalik, 1980;
Zyska, 1997, Nittrus, 2000a). Fungal attack on library
materials inevitably occurs on paper and parchment as
part of that natural process which human eagerness can
only delay. This awareness is as old as the use of sup-
ports for writing. Marco Vitruvio Pollione (25 a.C.) sug-
gested in his De Architectura Liber VI that libraries must
be built facing east, in order to avoid that books rot with
humidity. The systematic study of fungi causing stains and
weakening to paper started in the 19th century. The fungal
names referred to paper (Table 1), for example, are dated
from the first decades of the 1800. The first one who
studied the biodeterioration of paper was Christian Got-
tfried Ehrenberg. In 1818, he completed his doctoral dis-
sertation on fungi, Sylvae mycologicae Berolinenses,
where he described the first species that were named
Table 1. Some of the first fungal species discovered and named in
relation to paper in the 19th century.
Year of
Fungal species description

Chaetomium chartarum Ehrenb. 1818

Stilbospora chartarum Ehrenb. 1818
Myxotrichum chartarum Kunze 1823
Oidium chartarum Link 1824
Ascotricha chartarum Berk. 1838
Torula chartarum (Link) Corda 1840
Alternaria chartarum Preuss 1851
Actinospira chartarum (Nees) Corda; 1854
Myxotrichaceae
Agyrium chartarum Peyl; Agyriaceae 1858
Pleospora chartarum Fuckel, 1870
Macrosporium chartarum Peck; Anamorphic Lewia 1873
Phoma chartarum Berk. & M.A. Curtis; 1873
Anamorphic Didymella
Humaria chartarum Qul.; Pyronemataceae 1879
Pyronema chartarum (Qul.) Sacc.; Pyronemataceae 1889
Fig. 4. Fungal infection on ancient Egyptian pottery (Sterflinger).

2011 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 14, 559566

chartarum. In 1903, Van Iterson published La dcompo-
sition del la cellulose pas les microrganismes, but the first
work entirely dedicated to paper biodeterioration by fungi
was by Pierre Se, Docteur s Sciences who in 1917
published the article Sur les moisissures causant
laltration du papier and in 1919 the volume Les Mala-
dies du Papier Piqu- Les champignons chromognes qui
les provoquent les modes de prservation. A research
line was dedicated in the past also to the risk of books
being a vehicle for infections to people. In 1911, W. R.
Reinick wrote the paper Transmission of Disease by
Books about any human infection cases the source of
which has been traced to books or papers, or in which the
evidence seemed to make books the offender. After Se
(1917), several other authors dedicated their studies to
paper and books microbial deterioration. Worth mention-
ing are the works by Galippe (1919) in which some of the
first studies on treatments for fungal deteriorated paper
were reported. In the first decades of the 20th century, the
Italian school on paper microbiology was particularly out-
standing (Gallo, 1935; Sibilia, 1935; Benveduti, 1939;
Verona, 1939; Bonaventura, 1940; Bonaventura and
Paganini, 1940). In 1938, Alfonso Gallo founded the
Regio Istituto di Patologia del Libro (Gallo, 1940) (now
Istituto Centrale per il Restauro e la Conservazione del
Patrimonio Archivistico e Librario), which represented the
first academic institution in the world entirely dedicated to
the study of the deterioration (and biodeterioration) of
library materials.
Fungal degradation of library materials causes different
kinds of damage depending on the species of organism
responsible for the attack and the characteristics of the
substratum. Damage can occur because of mechanical
stress, production of staining compounds or enzymatic
action (Sterflinger, 2010; Pinzari et al., 2010a). Most of
the filamentous fungi associated with paper damage can
dissolve cellulose fibres with the action of cellulolytic
enzymes, or discolour the support and dissolve glues and
inks. Although there is some evidence about cases of
contamination of paper during the paper or bookmaking
process (Florian, 2002), most of the fungal species
that attack library materials come from dust and dust
inhabitants.
The works based on molecular techniques and focusing
on the investigation of the fungal flora responsible for the
biodeterioration of paper materials (Di Bonaventura et al.,
2003; Michaelsen et al., 2006; Rakotonirainy et al., 2007;
Pangallo et al., 2009; Michaelsen et al., 2009; 2010) show
that results obtained with culturing methods cover only
few viable and culturable organisms (about 5%) of the
total microorganisms actually present in materials. The
complexity of the microbial and fungal community struc-
ture on biodeteriorated paper is always higher than sus-
pected before taking the molecular approach. The
2011 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 14, 559566
Fungi and cultural heritage 563
Fig. 6. Scanning electron microscopical (SEM) image. The surface
of parchment from an Italian archival document (State Archive of
Rome, notary document from the XVth Century) affected by both
fungi (Monascus sp.) and bacteria (Streptomyces sp.). Various
fungal and bacterial structures can be observed coexisting on a
small area of the substrate. (SEM ZEISS EV050, high vacuum,
gold sputtered sample) (Pinzari).
co-occurrence of bacteria and fungi, and the role of these
relationships in substrate exploitation is probably highly
underestimated (Fig. 6).
A very different succession must be expected in librar-
ies and archives when water suddenly becomes avail-
able, such as in floods or when a water pipe bursts. Such
situations are familiar to archivists and librarians who are
well aware of the fact that when papers become saturated
with water, moulds can subsequently develop very rapidly
on them. The moulds associated with water-damage
(water damage moulds, Nielsen, 2002) consist of fungal
species that require high water activity. These species can
produce strong odours (Trichoderma spp.), coloured
stains (Chaetomium spp. and Epicoccum spp.) or toxic
compounds (Stachybotrys spp.).
Some fungal species produce spores which in natural
environments are mainly dispersed by insects and mites
(Deacon, 1997; 2005). Moulds affecting archival and
library materials (Zyska, 1997) can display different types
of interactions with the insects that eat the component
materials of the heritage. Insect-mediated fungal disper-
sion is well documented in natural environments (Ingold,
1965), but it also occurs in indoor environments. Some
heritage eaters, such as Psocoptera and mites are often
directly associated with the presence of moulds (Green,
2008). Conversely, insect infestations in libraries and
archives can frequently be associated with fungally
infected materials. Metabolic water, fragmented debris
and the droppings produced by insects represent a
perfect medium for fungal germination and growth. Some
fungi produce spores that can pass through the intestinal
564 K. Sterflinger and F. Pinzari
Fig. 7. Micrograph obtained by SEM in the backscattered mode.
Paper sample made of softwood and sized with calcium carbonate
(sample infected with Aspergillus terreus Thom, in vitro, at the
Biology Laboratory at ICRCPAL, Rome). Calcium oxalate crystals
were deposited on cellulose fibres as a consequence of A. terreus
metabolic activity (Pinzari).
tracts of insects and mites with no ill effects, and some
insects and mites can feed directly on fungal structures
(Green, 2008).
Fungal activity in library materials can also have visible
effects on mineral materials. Both paper and parchment
contain, in variable percentages, inorganic compounds.
Salts coming from manufacturing processes like sizing
minerals or impurities, or metals from inks made with Cu
and Fe are present in most library materials. Fungal inter-
action with the carbonate substrates, for example,
produce on a micrometric scale a clear replacement of the
original minerals with newly formed crystals that can be
referred to as mycolyths (Fig. 7). These biogenic miner-
als are produced in paper by those fungal strains that are
able to utilize calcium contained in CaCO3 to produce
oxalate crystals that precipitate on fibres and hyphae as
encrustations, and organized clusters (Pinzari et al.,
2010b).
Prevention and treatments
Climate control, frequent cleaning, monitoring of the
objects and of the surrounding premises are the most
important prevention measures. Climate concepts have to
be developed taking into account the individual architec-
ture of the museum. The hygienic status of a museum
especially the amount of fungal spores present on the
objects should be determined and disaster manage-
ment plans have to be developed (Dicus, 2000; Barton
and Wellheiser, 1985). Also the implementation of quar-
antine rooms for contaminated objects is increasing in
museums and restoration studios. New built storage
rooms are now provided with filter systems to prevent the
2011 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 14, 559566
invasion of fungal spores, plant pollen and dirt particles
(filter class F5 to F7). Frequent cleaning using vacuum
cleaners equipped with high efficiency particle absorbers
(HEPA filters) is highly recommended to keep the spore
load at a minimum.
The analysis of the fungal community on and in paper
and parchment as well as the understanding of their func-
tion is a major basis for the development of cleaning and
treatment methods. Although microscopy of fungal con-
tamination does only rarely allow to identify a fungus in
some cases the genus can be addressed because of
specific fruiting structures like perithecia or conidiophores
microscopy is a very important tool to investigate the
status of the fungal infection. Especially sizing the area
and the depth of infection in the material is important.
Dissecting light microscopy is the most important tool to
study the surface growth. Scanning electron microscopy
(SEM) can help to visualize if the fungal infection is more
superficial or if the fungal hyphae are already intermingled
with paper fibres indication attack and penetration of the
material with hyphal extensions (Michaelsen et al., 2010;
Pinzari et al., 2010b; Guiamet et al., 2011). The use of low
vacuum environmental SEM allows an immediate analy-
sis of paper samples without gold sputtering and previous
fixation of samples in glutar-aldehyde. The results from
microscopical analysis are a very important basis to make
decisions about cleaning and treatment methods: super-
ficial colonies for example can be removed from paper
and parchment using swabs and dry sponges; a deep
fungal infection in contrast might necessitate a severe
biocidal treatment.
For disinfection of a recent and progressive fungal
damage a limited range of physical and chemical
methods are available (Allsopp et al., 2004). Chemical
treatments include liquid biocides and fumigation with
gases. The choice of the appropriate biocide is limited
by the European Biocide directive (http://ec.europa.eu/
environment/biocides/index.htm). Topical treatments with
chemicals can be useful but the efficacy depends on the
sensitivity of the single fungal species and the tolerance
of the treated support. Biocides frequently used in res-
toration are: (i) formaldehyde releasers; (ii) quaternary
ammonium compounds with an optimal chain length of
C14-C16; (iii) isothiazolinone, a more recent biocide,
was documented to be not only effective but even pre-
ventive on paper objects; and (iv) the most common dis-
infectant used in microbiology: 70% ethanol. Ethanol can
also have a good fungitoxic effect if the contact time is
at least 23 min (Nittrus, 2000b). A broad spectrum of
chemical and non-chemical mass treatments has been
utilized to kill microfungi attacking paper-made objects in
an attempt to inhibit degradation (Magaudda, 2004). Eth-
ylene oxide (EtO) fumigation is banned in some coun-
tries because it is extremely toxic, but it still represents

the most efficacious system for mass treatment of
mouldy library materials. Gamma-radiation is very effec-
tive against fungi and their spores. Since the dose for
fungi has to exceed 1020 kGy (Nittrus, 2000a) this
method also affects many materials and application is
restricted. The application of gamma rays can result in
cumulative depolymerization of the underlying cellulose
and in severe ageing characteristics (Butterfield, 1987;
Adamo et al., 1998). A public, worldwide archive of infor-
mation on fungi-related damages and successfully
applied treatments would be a fundamental step for a
new shared policy on cultural heritage conservation.
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