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Review

Fungi Affecting Wall Paintings of Historical Value: A Worldwide Meta-Analysis of Their Detected Diversity

by
Laura Zucconi
1,†,
Fabiana Canini
1,†,
Daniela Isola
1,2,* and
Giulia Caneva
2
1
Department of Ecological and Biological Sciences (DEB), University of Tuscia, 01100 Viterbo, Italy
2
Department of Sciences, Roma Tre University, 00146 Rome, Italy
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Appl. Sci. 2022, 12(6), 2988; https://doi.org/10.3390/app12062988
Submission received: 4 February 2022 / Revised: 9 March 2022 / Accepted: 10 March 2022 / Published: 15 March 2022
(This article belongs to the Special Issue The Role of Fungi in Biodeterioration of Cultural Heritage: New Insights for Their Control)
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Abstract

:
Wall paintings have been a cultural expression of human creativity throughout history. Their degradation or destruction represents a loss to the world’s cultural heritage, and fungi have been identified as a major contributor to their decay. We provide a critical review of fungi isolated from worldwide wall paintings between 1961–2021. One-hundred three scientific papers were reviewed focusing on fungal diversity, isolation protocols, and spatial distribution of data. The study sites were grouped into five environmental categories on the basis of the expected major microclimatic conditions (temperature, relative humidity, ventilation), and the possible relationship with the species found was investigated. The highest number of records were localized in Europe, with 38 sites on a total of 74, 20 of which were from Italy. A total of 378 fungal entries were obtained, consisting of 1209 records, belonging to 260 different species and 173 genera. The accuracy level in taxa determination was highly variable among different papers analyzed. Data showed a dominance of Ascomycota, mainly of orders Eurotiales and Hypocreales probably due to their wide distribution and easily air dispersed spores and due to the possible pitfalls linked to the isolation methods, favoring rapidly growing taxa. Statistical analyses revealed that fungal communities were not strictly linked to environmental categories with different ventilation, temperature, and humidity. Such findings may be due to the wide geographical area, the wide heterogeneity of the data, and/or the absence of standardized sampling and analyses protocols. They could also be the result of the dominance of some prevailing factors in the various sites that mask the influence one of each other.

1. Introduction

Wall paintings are among the most representative elements of figurative artworks and have been developed by human creativity since prehistoric times [1]. Their technique of execution requires a layered structure consisting of a support, a ground, and a paint layer, which changed over time across different cultures (secco, such as tempera, or frescoes) [2]. In secco technique, which is the earliest, the preparation layers are applied, but the colors remain on the surface, whereas in the frescoes the colors are applied before the mortar dries, allowing their in-depth penetration [2]. The employed colors usually have a mineral origin, but some pigments can also be derived from plants. Organic compounds can later be added during restoration or because of other human activities (e.g., firing candles in the churches) [3].
The observed deterioration phenomena of mural paintings depend largely on the materials used and the environmental conditions [4]. Indeed, mural paintings are subject to a variety of biodeterioration phenomena, which varies depending on the humidity, lighting, temperature, ventilation, and nutrients, which also select the occurring biological agents [1,5]. Furthermore, many environmental factors may synergistically or antagonistically contribute to the deteriorating actions of microorganisms [6]. Organisms belonging to all domains (bacteria, algae, fungi, animals and sometimes also lichens, mosses, ferns, and higher plants) have been isolated from the surfaces of mural paintings [4,7]. Indeed, given the indoor conditions of most mural paintings, photoautotrophs are highly limited, while fungi and bacteria are more frequent [8]. Bacteria with reduced nutritional needs have been often suggested to be the first colonizers. With their death and lyses, they release organic matter that promotes the growth of secondary colonizers, such as fungi [9,10,11]. Fungi, instead, can produce a large assortment of enzymes and have the remarkable ability to grow and thrive in a wide variety of environmental conditions, including low water activity [12]. Fungi have been rightly recognized as the most common cause of biodeterioration of painted surfaces and other artworks, causing both physical and chemical deterioration phenomena, with aesthetic and structural consequences [1,13,14].
Generally, damage is due to the mycelial growth on the substrate, hyphal penetration, and fruiting bodies production onto and into the substrate, all of which increases the volume and number of cracks, causing the rupture of the pigment layer and leading to surface fragments detachments [1,15]. Fungal colonization generally starts on the surface and then moves in-depth, up to decreasing painted layer cohesion and cause exfoliations and loss of the paint [9,16]. A study carried out by Dornieden and colleagues demonstrated that some fungi, as the so called microcolonial black fungi, are among the most dangerous for cultural heritages and can influence the resistance to shear and torsion stress of mortar and marble, contributing to the separation of different layers of material in mural paintings [17]. Aesthetic damages are also frequent, due to pigment discolorations, mycelial pigmentation, and/or the release of organic pigments of different colors, depending on the species involved. Moreover, secondary compounds such as extracellular enzymes and/or organic acids are generally released in the substrate from fungal hyphae, and this may cause chemical alterations of the mineral constituents of the surfaces as well as the original pigments [9,16]. The secretion of organic acids (e.g., oxalic, citric, succinic, formic, malic, acetic, fumaric, glyoxylic, gluconic, and tartaric acids) also plays a significant role in chemical attack, causing acidification of the substrate [18,19]. They can cause dissolution of cations and chelation of metal ions from mortar and mineral pigments, leading to the formation of stable metal complexes whose crystallization causes an increase of internal pressure resulting in cracking, peeling, and the eventual loss of mural fragments [20].
Awareness of the considerable role played by microorganisms in the preservation of art objects and historical buildings dates back to the 1950s [21]. Ionita and colleagues provided one of the first detailed descriptions of the mycoflora involved in the deterioration of mural paintings of monasteries in Moldavia, noting that it was favored by the various nutritional sources present in the materials used for the realization of the frescoes and by local environmental parameters [21]. This was perhaps one of the first statements of the importance of interdisciplinary studies to prevent and control deterioration processes and define restoration and preservation strategies. Two interesting mini-reviews were later published by Garg and Ciferri teams [1,16]. Many papers have been published after that, showing a growing awareness of the degradative role of fungi as well as the importance of mycological analyses as an integral part of the state-of-the-art system of wall painting safeguards [22].
Despite the fact that the fungal role in the deterioration of frescoes has been documented by a huge number of papers, a global inventory of fungal diversity and their optimal settlement conditions is not yet available. These paintings are mainly present in confined and semi-confined environments, both hypogean and non-hypogean. A fungal alteration pattern dependent on the environmental conditions of these different sites was expected. Those present in hypogean environments are often subjected to a constant extreme humidity, promoting fungal spores germination and mycelial growth. The amount and type of available nutrients also affects the fungal growth rate and the type of fungal taxa. Nutrients may arrive from the external environment as airborne particles, and the more confined are the environments, the lower are the air spores dispersion phenomena. With this contribution, we aimed to describe the diversity of fungal colonizers involved in the deterioration of wall paintings, as well as their distribution under different environmental conditions. Additionally, we aimed to determine if a correlation among the different species recorded and the different types of environments-hypogean, non-hypogean, confined, non-confined, and open-exists and to speculate on their preferential habitat and their possible origin. A dataset of all the fungal taxa occurring on wall paintings based on bibliographic references was created for these purposes.

2. Materials and Methods

2.1. The Bibliographic Search

An extensive search was made among peer reviewed literature, proceedings to conferences, and books. The literature was identified using international databases, such as Scopus (https://www.scopus.com, 29 December 2021), Science Direct (https://www.sciencedirect.com, 29 December 2021), Web of Science (http://www.webofknowledge.com, 29 December 2021) and Google Scholar (https://scholar.google.com, 29 December 2021), that were consulted by using keywords such as ‘wall paintings’, ‘mural paintings’, ‘frescoes’, ‘fungi’, ‘biodeterioration’, ‘microbial deterioration’, and ‘biodeteriogenic agents’. The thematic databases of ICCROM (International Centre for the Study of the Preservation and Restoration of Cultural Property) and the Italian ISCR (Istituto Superiore per la Conservazione e il Restauro) were also consulted, being important reference institutions in the field. Such sources were fundamental in the search of literature related to congresses and reports, that are not found by the most common scientific reference tools. The search covered more than 50 years, dating back to the first papers published in the 1960s (Figure 1), even if mostly of the papers containing useful taxonomic information were published after the 1980s.

2.2. The Database

A list of all the entries retrieved, corresponding to taxa identified at both species and genus level, was compiled. Few were the entries referring to taxa above the rank of genus and they are listed at the end of the database. Current names of the taxa were reported according to the Index Fungorum (www.indexfungorum.org, 20 January 2022). The synonyms under which the different species were eventually reported in the analyzed papers were also indicated. Those entries recorded on paintings that have been the subject of multiple studies over the years, such as Takamatsuzuka and Kitora tumuli in Japan [23,24,25], were reported once accompanied by all bibliographic references.

2.2.1. The Geographic Localization of the Study Sites

The geographical locations and coordinates of the studied monuments were retrieved using Google Maps. The graphical representation on a map of sites distribution was performed using the 3D Map function of the Excel package. Some papers dealt with an unidentified number of monuments, as in the case of ‘Monasteries in Romania’ [21], ‘several churches’ in Northern Portugal [26], or ‘Ajanta caves’ in India [27,28,29,30,31,32]. In these cases, one or more sites were counted, depending on the details provided by the authors within the studied area and on their geographical distribution. Instead, some papers dealt with different monuments from the same area (e.g., different buildings in the historical site of Herculanum, Italy), that have been considered as a single site for the purpose of this study. This is why the total number of monuments is higher than the total number of geographical sites assessed in the statistical analyses.

2.2.2. Isolation and Identification Methods Used

The following information has been recorded: the type of culture media used, the growth temperature and incubation time, and the methods used for isolates identification.

2.2.3. The Types of Environments

The environments that housed the wall paintings object of the studies considered were grouped into five categories, based on whether they were hypogean or not, as well as the expected ventilation, confinement, and moisture conditions. The following are the definitions of the categories:
  • C-HE: Confined Hypogean Environment (isolated, without air circulation, with generally high humidity levels and relatively stable and low temperatures) as tumuli, close tombs, or prehistoric caves. They are often characterized by not negligible organic matter inputs from dripping waters, animals, and their fecal pellets and may be influenced by the presence of visitors, promoting the introduction and movement of airborne particulate.
  • NC-HE: Non-Confined Hypogean Environment (hypogean environments with reduced air circulation), such as underground crypts, catacombs, rupestrian churches, or Roman houses. These sub-aerial environments offer semi- or non-confined situations that are partially isolated from the external environment, with humidity and temperature comparatively more stable than the outdoor conditions but influenced by external day-night cycles and seasonal fluctuations.
  • C-NHE: Confined Non-Hypogean Environment: the sub-aerial environment of churches, monasteries, temples, refectories, and castle chapels represents a confined condition in which the microbial community is enclosed in a mesocosm. They are partially isolated from the external environment and have relatively more stable humidity and temperature than outdoor conditions, but they are influenced by external day-night cycles, seasonal variations in temperature, and relative humidity values. They are more prone to microbial attacks since they include more visited sites.
  • SC-NHE: Semi Confined Non-Hypogean Environment (open towards the outdoor environment but protected by wide changes in environmental parameters), such as ancient archaeological buildings and private homes. They are open to the outdoors but sheltered from rain and ventilation; they all experience seasonal and daily relative humidity and temperature fluctuations.
  • O-SPE: Open and Semi-Protected or Protected Environment; they include buildings’ walls or collapsed caves, which are among the most exposed sites to biodeterioration risks.

2.3. Statistical Analyses

A data dissimilarity matrix was inferred using the Jaccard’s dissimilarity index [33], and a hierarchical cluster analysis was performed on this matrix using the UPGMA method. Two dendrograms relating dissimilarities between sites and entries were plotted. Entries identified at the genus level were considered as diverse elements. The Silhouette index was used to resolve the optimal number of clusters [34]. A contingency table between the obtained clusters and the environmental categories to which they belonged was also constructed to assess the relationship between their data. An indicator species analysis of the individual clusters was performed, which identifies associations between entries or combinations of entries and clusters, using the Indval index [35,36].
All analyses were performed with the R Software with the packages ade4, vegan, gclus, cluster, vegclust, and indicspecies.

3. Results

3.1. The Fungal Data Set

A total of 103 papers dealing with the fungal deterioration of wall paintings were collected, regarding 107 different monuments grouped in 74 sites. A total of 378 fungal entries were obtained, consisting of 1209 records belonging to 173 genera and 260 species (Table 1).
The taxonomic distribution of the total fungal diversity and within different types of environments, at phylum and order level, is reported in Figure 2. Ascomycota was the dominant phylum, ranging from 89 to 97% (except for the environment O-SPE where a great proportion of undetermined taxa was retrieved) and accounting for 100% of the fungal entries in 40 out of 74 sites. The other two phyla identified were Basidiomycota (1–6%), more abundant in C-NHE, and Mucoromycota, reaching a maximum value (2.35%) in C-NHE (Figure 2A).
The entries were distributed in 39 orders. Eurotiales and Hypocreales were the most represented ones, together accounting for more than half of total fungal diversity. Pleosporales, Capnodiales, Sordariales, and Chaetothyriales were also well represented orders within Ascomycota. Basidiomycota accounted for a maximum of around 6% of all taxa, with Agaricales, Helotiales, and Saccharomycetales being the most abundant ones accordingly. Mucorales was the most abundant order within the phylum Mucoromycota.
The accuracy in taxa determination varied among the different papers analyzed, with many entries identified only at genus level. In fact, a total of 107 out of 378 entries (28.3%) referred to genera not determined at the species level, and it was not possible to quantify the number of possible different species belonging to these genera within different papers. A total of 61 genera (35.2%) were represented by a single species. Aspergillus and Penicillium (order Eurotiales) were the most frequently recorded genera and were represented by a greater number of species, 40 and 46, respectively, present in 44 (59.4%) and 32 (43.2%) sites, which increased to 54 (73%) and 51 (68.9%) when those sites where the genera were reported as undetermined at the species level were also considered. Their contribution to the total number of records was significant, with 219 (18.1%) and 154 (12.7%) records, respectively. Other genera frequently recorded were Alternaria and Fusarium with seven species each; Acremonium, Cladosporium, and Trichoderma with six species; Curvularia and Talaromyces with five species; and Chaetomium with four species.

3.2. The Geographic Distribution of the Study Sites

The data came from 107 monuments, grouped in 74 sites and distributed among 19 different countries. The countries where they were reported as well as the different number of sites were graphically represented in Figure 3.

3.3. Isolation and Identification Methods

A dominance of culture-based methods associated with morphological identification (58%) and target regions sequencing (31%) was recorded, the latter has become progressively dominant since the 2000s. The culture media used varied depending on the research purposes and included Czapek Dox agar (CZ), malt extract agar (MEA), malt agar (MA), potato dextrose agar (PDA), Sabouraud dextrose agar (SAB), and oatmeal agar (OA) among the most frequently used. The use of mycological agar (MYC), Cook’s Rose Bengal (CRB), and yeast peptone dextrose (YPD) was sporadic. Data on growth temperature and incubation time were frequently missing, accounting for 31.25% (Figure 4A, green) and 54.12% (Figure 4B, green) of all papers, respectively. This trend was particularly evident in the earliest papers where more attention was paid to fungal species than to the conditions used to isolate them (e.g., [40,47,84,88]). The most frequent temperature settings were 25 °C (35%) and within the range 27–32 °C (21.25%). When reported, the incubation frequently corresponded to 7 days (31.76%) (Figure 4B). When isolated strains were identified by molecular approaches, the identification was performed targeting different barcoding regions, such as the complete internal transcribed spacer (ITS), a part of it (ITS1), portions of 18S (SSU), 26S (LSU), and β-tubulin.

3.4. Distribution of Fungal Entries in Different Environments

The distribution of the sites among the environmental categories revealed a predominance of wall painting recorded in C-NHE, which alone accounted for 54% of the sites. The hypogean environments accounted for 36.5% of the sites, distributed between C-HE (18.9%) and NC-HE (17.6%). The remaining two categories, SC-NHE and O-SPE, were less represented, comprising 4.1% and 5.4% of the sites, respectively.
The cluster analysis at the level of different sites resulted in a general dispersion, with no distinct clusters retrieved. Several clusters consisted of one or few sites highly different one to each other (13-11-14-3-15-10-9-7-12). Other clusters (4-5-6) were slightly more similar to each other and contained many entries (Figure 5).
The contingency table highlighted that the obtained clusters did not have a strong correlation with the suggested environmental categories (Table 2). However, some clusters showed some affinities: cluster 15 with cat. 4 (SC-NHE) (aff. index 17); cluster 6 with cat. 5 (O-SPE) (aff. index 12.8); clusters 2,4,5 with cat. 3 (C-NHE) (aff. indexes 8.1, 9, and 6.2, respectively); cluster 4 with cat. 2 (NC-HE) (aff. index 5.9); cluster 1 with cat. 1 (C-HE) (aff. index 8.2).
When the correlation among different entries was analyzed, very scattered results were retrieved (Figure S1). However, some entries or combinations of them showed some affinities (specificity and fidelity above 0.5) with certain clusters such as Alternaria alternata with cluster 2 (Indval Index = 0.75); Acrothecium sp. and Penicillium sp. with cluster 4 (Indval Index = 0.70 and 0.66, respectively); Parengyodontium album and Rhinocladiella-like with cluster 5 (Indval Index = 0.70 and 0. 64); Actinomucor elegans, Penicillium pancosmium, Acremoniella atra, Alternaria angustiovoidea, Scolecobasidium anomalum, Scolecobasidium lascauxensis, when considered in combination, the entries Trichoderma sp. and Verticillium sp. with cluster 1 (Indval Index = 0.70, 0.70, 0.70, 0.70, 0.70, and 0.70, respectively); and Akanthomyces lecanii with cluster 9 (Indval Index = 0.93).

4. Discussion

4.1. The Fungal Data Set

Even if fungi have been suggested as secondary colonizers of painted mural substrates, they are among the most common microbial life-forms present in these environments and the primary cause of their biodeterioration [1,13,14]. The wide biodiversity observed confirms the potential key role of fungi in such colonization process and suggests a combination of causes that can favor their growth. Their broad enzymatic activities allow them to grow on every type of material, or wherever they find organic matter. Fungi recorded belonged to species generally reported from natural environments like soils, plants, and air where they live as saprotrophs, as well as plant and animal parasites and pathogens. A detailed survey of their diversity and distribution should become a prerequisite before any restoration measures in order to prevent further damages [39]. Most records belonged to Ascomycota, with Eurotiales being the most common order, due to the prevalence of Aspergillus and Penicillium genera. The former was one of the most frequently isolated genera, with A. flavus and A. niger among the more frequently recorded species. As reported in the literature, even from the first older papers in this field, these two genera, along with Alternaria, Fusarium, Cladosporium, Mortierella, Chaetomium, and Acremonium, are among the most common deteriogens of such paintings [1,11,15,31,39,46,62,78,87,91]. These taxa are ubiquitous, and their frequent occurrence is due to the production of numerous conidia, which are widespread in the environment because they are easily dispersed by air. A diversity of filamentous fungi, with the most predominant genera Penicillium, Cladosporium, Aspergillus, and Trichoderma, were also isolated from mural paintings of the Parish Church of Santo Aleixo (Portugal). Their dehydrogenase activity was determined, as an indicator of the presence of metabolic active cells to allow a deeper insight on the deteriogenic role of the isolates [19].
Species of these genera were recorded on indoor frescoes in numerous monasteries in Romania, possibly favored by the organic components and vegetal pigments used, as well as high moisture levels caused by frequent rainwater penetration, which also resulted in the formation of efflorescences [55]. Cladosporium species can cope in a variety of harsh environmental conditions thanks to their low nutritional requirements (i.e., in oligotrophic conditions). Otherwise, Chaetomium species are proteolytic and cellulolytic ascomycetes, favored by nutrient-rich substrates [22,65,117]. They were reported as the most frequent microfungi on the frescoes of the St. Damian Monastery in Assisi (Italy) [46] and on frescoes in a Serbian church [22]. Furthermore, a community of Aspergillus, Penicillium, Cladosporium, and Chaetomium species was recorded from Medieval wall paintings in Styria (Austria), forming spots of different colors [39]. This group of genera was dominant on two deteriorating frescos in St Clare’s Refectory of the Monastery of St Damian in Assisi [46].
Hypocreales was the second most abundant order, accounting for 18% of total fungal diversity, within which Acremonium, Trichoderma, and Fusarium were among the most common genera. Hypocreales is one of the largest orders of filamentous ascomycetes and exhibits a broad range of ecologies, ranging from plant-associated nutritional modes to animal pathogens (e.g., insect pathogens) and mycoparasites [118]. Neocosmospora solani, recorded in Thailand, India, Japan, and France; Simplicillium lamellicola, recorded in Russia; and Clonostachys rosea [48,58], recorded in Japan, are examples of mycoparasitic species, while Parengiodontium album is an insect parasite and was recorded in several countries (Germany, Russia, Romania, Austria, Italy, and England) [109]. The recurrent presence of mites and insects pointed out their possible role in spreading fungi on painted surfaces [46,119].
Finally, the plant pathogen species Fusarium oxysporum has been shown to produce an extracellular pinkish pigment that disfigures and aesthetically damages colonized mural paintings and stone surfaces with permanent stains [78].
Phylum Basidiomycota was present with several occasional species, mostly represented by one or two records, and comprises litter, soil, and wood-saprotrophs, ectomycorrhizal, epiphyte, and plant-pathogen species. Their occurrence must be regarded as sporadic, potentially aided by root penetration. The possible role of roots as a carrier for rhizosphere microorganisms, like a dripping line for water condensation, and as an organic carbon source by root exudates has been hypothesized [57,120]. In any case, a Basidiomycete was also recorded at the entrance of Roman catacombs [121], possibly due to spores carried by water infiltrations and germinating using organic nutrients from the soil and/or the phototrophic biofilm.
Mucoromycota was present with few species and records, and black meristematic fungi were rarely recorded as well. These latter may grow on a wide range of substrates and are resistant to a variety of environmental stresses, as well as being widely distributed epi- and endolithically on monuments [122,123]. Although the biodiversity of black fungi on historical monuments is not fully elucidated, recent samplings indicate that they are also present on wall paintings and that their rare finding could be linked to the isolation protocols used, generally favoring fast-growing species [124]. Two new species of the genus Neodevrisia have been found in the restricted sampling area of the Vallerano cave and another, still undescribed, from Maijishan grottoes [45,99,108]. Scolecobasidium lascauxensis and S. anomalus were isolated and described from black stains in Lascaux Cave, France [85,115], while the chaetothyrialean black fungi Cladophialophora, Exophiala, and Phialophora have been reported from different sites [23,24,42,98].
Yeasts have been rarely reported, such as Saccharomycetales (Ascomycota) that usually grow by individual yeast cells or Rhodotorula spp. (Basidiomycota) often linked to pink/orange stains due to the release of carotenoids [19,93].
Among those more commonly reported, some species such as those belonging to the genera Alternaria, Fusarium, Aspergillus, Penicillium, and Cladosporium may be responsible for annoying allergic and toxic reactions suffered by conservationists and visitors [81,125,126]. Alternaria alternata is a very common fungal species, frequently recorded on frescoes. Its spores are recognized as common powerful aeroallergens, and indoor environments offer higher levels of exposure to this risk than open-air [59,127]. Records of Fusarium species have also been reported, such as F. solani in the Lascaux caves [97] and F. oxysporum in many sites. They are mainly plant pathogens, but they can also be the causal agents of human mycoses [97,128,129]. Some Aspergillus species are pathogenic to humans and animals and are responsible for clinical manifestations (https://www.aspergillus.org.uk/species-archive/, 29 December 2021). Among these, A. fumigatus is a human pathogenic fungus recorded on frescoes within different environments (3,11,22,29,42,49,70,71), causing infections in humans which can be fatal in immunocompromised patients (61). Aspergillus flavus has been frequently recorded in monasteries, churches, temples, caves, and tombs, mostly due to their numerous aerosolized spores. It mainly grows in the soil, but it is also a facultative and opportunistic pathogen of both animals and plants, producing mycotoxins that are highly harmful to humans [130].
In light of the above, the identification of the species deteriorating wall painting is needed for the protection of restorers and visitors. However, the temperature values characterizing confined and semi-confined sites are generally too low for potential pathogenic fungi. In fact, truly thermophilic fungi which cannot grow at temperatures below 20 °C are not active in these environments, at least during winter in temperate regions.

4.2. Geographic Distribution

Considering the geographic distribution of the data, just one site among the studied paintings comes from the Americas (the Cathedral of Havana at Cuba) [82]. The highest number of records was from Europe, with 70 monuments, mostly representative of hypogean environments and of churches and historical buildings, with a considerable prevalence of Italian monuments (39). A total of 26 monuments were from Asia, while the 13 African ones were all from Egypt.
This distribution arises from the old tradition of people of the Euro-Mediterranean area of using such artistic expression, starting from the old prehistoric caves to the Etruscan and Greek-Roman traditions until the consolidated use both in the decoration of Christian churches and historical buildings [2]. In the case of the Egyptian area, the recorded taxa derived from the old tombs of the Pharaohs [54,72,73,77,78], and similarly in East Asia, the tradition is mainly found in kings’ and Emperors’ tombs [23,24,25,38]. Most of the ancient paintings in buildings do not exist anymore, due to frequent rebuilt or remake of the materials [131].
Our results suggest that the monuments studied were often confined to restricted geographic areas. In any case a wider geographic distribution than that recorded may be possible, as a number of sites may have escaped the search. In fact, even if formally available on the web and on the major repositories, because of the language barriers, some studies could not be taken into account.

4.3. Isolation and Identification Methods

Culture-based methods favor the growth of microorganisms best fitting with the laboratory conditions used (namely, culture media, temperatures, and incubation times). In this study, we found that the most frequent experimental settings were favorable to fast-growing, highly-sporulating fungi, with the use of culture media rich in easily accessible carbon sources, alongside short incubation times and optimal growth temperatures favoring their sporulation. Otherwise, lower growth temperatures (≤20 °C), wide temperature ranges, different isolation media, and a longer incubation time could enlarge the detectable culturable fraction.
Since the early 2000s, molecular phylogenetic methods have highlighted the limitations of morphological identification, allowing us to gain a better understanding of the kingdom of Fungi [132]. Nowadays, the identification by barcode regions sequencing is a common practice. Even if the nuclear ITS region has been recognized as a fungal barcode, its discriminating power changes within the taxonomical groups, and other/more barcode regions are often necessary to have a reliable identification [133]. This is the case of the identification of species within large groups, as Fusarium, Penicillium, Aspergillus, and Cladosporium genera, where cryptic species can be detected only by sequencing multiple molecular markers [134].
In detail, Fusarium species determination has been best made with the combined phylogeny of protein coding genes such as elongation factor (TEF1), RNA polymerase (RPB2) and the partial β-tubulin (BT2) gene [134]. To discriminate between Penicillium and Aspergillus species, β-tubulin (BT2) and calmodulin (cmdA) genes have been proposed as secondary barcodes, respectively [135,136]. While the most phylogenetic informative markers for Cladosporium were TEF1 and actin gene (actA), ITS sequences being identical for species of the same complex [137,138].
The correct identification of strains is required in order to provide restorers more information about strains’ ecology and degradative potential. In this light, standardized identification protocols should be implemented.
High throughput sequencing methods have recently been applied to cultural heritage purposes. These methods represent a powerful tool to define the whole fungal diversity present but not necessarily to deepen the mechanisms and the main actors of the deterioration phenomena [139]. The combination of culture-based and molecular methods should be used for a better understanding of deterioration processes. Indeed, pure cultured microorganisms represent the key to uncover settlers’ physiological and ecological traits, as well as representing a resource for many in silico applications and barcoded identifications [123,124].

4.4. Distribution of Taxa in the Different Environments

The most prevalent sites were confined non-hypogean environments, which are characterized by varied thermo-hygrometric temperatures and air movement. Hypogean (both confined and non-confined), where nutrients and humidity can favor fungal growth were represented as well.
Temperature and relative humidity are among the environmental parameters most important to microbial colonization capability, and in the case of heterotrophs, a certain amount of nutrients is also needed [4,140]. It is well known that fungi rapidly grow when relative humidity is higher than 65% and when a certain quantity of nutrients is available. The low values of temperatures, even if are not favorable for microbial growth by themselves, have a positive effect in contributing to increase in humidity, favoring water condensation on surfaces. Walls, especially in hypogean environments, generally provide these requirements [1]. Temperatures in confined environments are generally more stable than in non-confined environments, where daily and seasonal changes may occur, with ranges that have effects on microbial settlement. Elevated moisture values and stable temperatures have been reported as ideally suited to promote microbial growth on surfaces in catacombs sites [7,94,141]. Indeed, the highest risk occurs when high humidity is coupled with high temperature values, and negative effects of rising temperatures arise only if their highest values can strongly influence the humidity values [142]. In the case of hypogea, the underground conditions favor the maintaining of humidity.
Air movement differences between confined, semi-confined, and non-confined environments were expected to alter the number and type of fungal species recorded as well as incoming nutrients from the outside environment. A great proportion of entries in the database belonged to soil and litter dwellers such as saprotrophs, producing numerous spores that are well adapted to air-borne dispersal, and therefore, air ventilation may have a significant impact on the risk of contamination [143]. The more limited air volume movement of confined mural paintings compared to semi-confined ones was suggested to decrease the number of air-borne dust particles, with biofilm communities relying more on internal interactions between different microorganisms than on the external organic inputs [17]. Among the first aerobiological studies, Savulescu and Ionita reported a greater number of isolates inside the studied monasteries than outside of them, probably due to a more favorable microclimate inside the church, which favors the development of microorganisms [55]. Pangallo and colleagues proposed for the first time a comparative analysis of the microbial component of paintings and the surrounding air to gather information on the origin of fungal contamination [70]. Aside from the importance of aerobiological studies for the conservation and prevention of microbial attacks on indoor painted surfaces [144], these studies have received little attention. In light of the large number of fungal species potentially harmful for restorers and visitors, constant monitoring of air spore quality and concentration, as well as the use of air filters to reduce fungal spores concentrations, would be required for site conservation [62,101,144,145].
Significant correlations between the different taxa and the various environmental categories have not been recorded. Indeed, such data is not the result of the absence of a correlation between fungal growths and environmental conditions but can be consequence of several other influencing conditions that hide it. In fact, many are the ecological requirements that shape the ecological niches of the different species (i.e., the limiting factors), but the most conditioning factors are those that result in a quantity proximal to the upper or lower tolerance limit of an organism [146]. Then, for the various sites examined, some factors may become more relevant if their values are closer to the tolerance limit of certain organism, but this does not mean that other parameters do not play a role [147].
Indeed, our results may be influenced by the wide number of taxa in the wide geographic distribution of sites and by the different methodologies used to characterize the fungal diversity. In fact, different sampling techniques and isolation conditions were used within the studies we analyzed. Other factors that allow fungi to thrive and/or survive in a variety of conditions are their wide nutritional versatility and range of adaptations. The presence of numerous genera that are widespread and highly sporulating and hence present in all the environmental categories must also be considered. The absence of evident correlations could have been determined by the absence of distinct boundaries between the categories identified, with overlapping microclimatic conditions which could have resulted in overlaps within their respective microbial communities. Finally, the heterogeneity of the data, with taxa identified at the genus or species level, may have resulted in dispersed clusters and hampered the ability to demonstrate any relationship.
This result seems to be in line with other studies. The influence of environmental factors such as temperature, relative humidity, and the opening or closure of the temples was not evident for fungal growths on wall paintings of 12 archaeological sites in the central and western parts of Thailand [76]. Furthermore, a stronger relationship with the age of five caves in China than with the environmental conditions, such as temperature and relative humidity, was proposed to explain the observed differences in fungal communities [64]. In two distinct mural paintings, instead, the differences recorded in the microbial communities were associated to the different organic input origin (i.e., wine cellar evaporation, and insect exuvia/excrements) and the microclimatic conditions. The more humid conditions favored the growth of actinomycetes, bacteria, and dark-pigmented fungi, while the other showed a biofilm, mainly dominated by xerotolerant and patchy growing sporulating fungi [17]. Differences in fungal communities were also recorded on mural paintings of two subterranean ancient Chinese tombs dating back over 1700 years, mostly due to variations in interior temperature and relative humidity as well as to their history and drawing techniques used [51].
Other significant concerns could be related to the identification of the isolated species, which was initially based solely on morphological observation. Indeed, phylogenetic molecular approaches are nowadays routinely applied, providing a universal tool for accurately identifying fungal species.
New methodologies such as omics techniques are now available; however, they rarely provide information at species or genus level, and there is no guarantee that the recorded taxa are actively growing. Moreover, culture-dependent approaches may not provide a real picture of the microbial diversity actively growing at the sampling time. This is because not all fungi actively growing on the deteriorated substrates can grow under laboratory conditions, and fungi growing under laboratory conditions may not actively grow on the sampled surfaces. Therefore, a combination of culture-based and molecular approaches may be needed to gain a clear picture of the actual biodiversity present on the painted surfaces as well as to have strains to investigate their potential degradative roles.

5. Conclusions

This study contributes to illustrate the high fungal diversity on wall paintings and raises awareness about the fungal threat on the deterioration of such artworks. Ascomycota was the most common phylum, with Eurotiales and Hypocreales as the most common orders. Statistical analyses did not enhance core communities that can be considered characteristics of different environmental categories of sites hosting wall paintings. Our results were likely due to the heterogeneity and fragmentation of the data in the databases, the dispersed geographical area considered, and the complexity of factors which can condition the biological growths. It is therefore crucial to cover the knowledge gaps through (i) international collaborations, (ii) enlarging the isolation and cultivation protocols as to easily detect also strains different from fast growing ones, and (iii) standardizing the identification protocols. Standardizing and improving the site descriptions (e.g., repeated microclimatic data) could allow for possible relations between site and their settlers and for further comparisons among different environmental conditions.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app12062988/s1, Figure S1: Cluster analysis on the Jaccard distance of the distribution of the different entries retrieved from the papers analyzed; Table S1: List of all the references associated to each site defined in the analyses.

Author Contributions

Conceptualization, L.Z. and G.C.; methodology, L.Z., F.C., D.I. and G.C.; data curation, L.Z., F.C., D.I. and G.C.; writing—original draft preparation, L.Z. and F.C.; writing—review and editing, L.Z., F.C., D.I. and G.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Authors wish to acknowledge Giulio Zangari (Department of Sciences, University of ‘Roma Tre’) for his support in some statistical elaborations. Authors wish to acknowledge Giulia Corsetti Antonini and Matt Hudson for the revision of the English language.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. PRISMA flow diagram of the search process.
Figure 1. PRISMA flow diagram of the search process.
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Figure 2. Taxonomic composition of the fungal diversity recorded on wall paintings on the total dataset and in relation to the different environments, at (A) phylum and (B) order level.
Figure 2. Taxonomic composition of the fungal diversity recorded on wall paintings on the total dataset and in relation to the different environments, at (A) phylum and (B) order level.
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Figure 3. Geographic distribution of the reviewed study’s 107 monuments. Nations are indicated with the international alpha-3 code: ITA: Italy, EGY: Egypt, THA: Thailand, PRT: Portugal, CHN: China, ROU: Romania, AUT: Austria, GER: Germany, JAP: Japan, IND: India, RUS: Russian Federation, ESP: Spain, SRB: Republic of Serbia, CUB: Cuba, FRA: France, KOR: Republic of Korea, SVK: Slovak Republic, CHE: Swiss, GBR: Great Britain. In the blue rectangle Cuba.
Figure 3. Geographic distribution of the reviewed study’s 107 monuments. Nations are indicated with the international alpha-3 code: ITA: Italy, EGY: Egypt, THA: Thailand, PRT: Portugal, CHN: China, ROU: Romania, AUT: Austria, GER: Germany, JAP: Japan, IND: India, RUS: Russian Federation, ESP: Spain, SRB: Republic of Serbia, CUB: Cuba, FRA: France, KOR: Republic of Korea, SVK: Slovak Republic, CHE: Swiss, GBR: Great Britain. In the blue rectangle Cuba.
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Figure 4. Values/ranges of (A) growth temperature and (B) incubation time recorded in culture-based protocols.
Figure 4. Values/ranges of (A) growth temperature and (B) incubation time recorded in culture-based protocols.
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Figure 5. Cluster dendrogram. Cluster analysis on the Jaccard distance of the composition at the level of the different sites. Sites belonged to the following categories: Site1–Site14 C-HE; Site15–Site27 NC-HE; Site 28–Site67 C-NHE; Site 68–Site70 SC-NHE; Site 71–Site74 O-SPE. The references associated to each site are reported in Supplementary Table S1.
Figure 5. Cluster dendrogram. Cluster analysis on the Jaccard distance of the composition at the level of the different sites. Sites belonged to the following categories: Site1–Site14 C-HE; Site15–Site27 NC-HE; Site 28–Site67 C-NHE; Site 68–Site70 SC-NHE; Site 71–Site74 O-SPE. The references associated to each site are reported in Supplementary Table S1.
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Table
Table 1. List of the fungal entries retrieved from the different papers grouped by genera, in association with the corresponding references and the environmental categories where they have been registered.
Table 1. List of the fungal entries retrieved from the different papers grouped by genera, in association with the corresponding references and the environmental categories where they have been registered.
GenusFungal NameReferencesEnvironment
AcremoniellaAcremoniella atra[21]C-NHE
AcremoniumAcremonium camptosporum[37]NC-HE
Acremonium charticola[38,39,40,41]NC-HE, C-NHE
Acremonium masseei[23,25]C-HE
Acremonium murorum
(syn. Gliomastix murorum)		[23,24,25,28,32]C-HE, NC-HE
Acremonium rutilum
(syn. A. roseum)		[21]C-NHE
Acremonium cf. rutilum[39]C-NHE
Acremonium sp.[23,38,39,40,41,42,43,44,45,46,47]C-HE, NC-HE, C-NHE
AcrodontiumAcrodontium crateriforme[48]C-NHE
AcrophialophoraAcrophialophora fusispora
(syn. A. nainiana)		[28,32]NC-HE
AcrostalagmusAcrostalagmus luteoalbus
(syn. Verticillium lateritium)		[49]C-NHE
AcrotheciumAcrothecium sp.[50]O-SPE
ActinomucorActinomucor elegans[51]C-HE
AkanthomycesAkanthomyces lecanii
(syn. Verticillium lecanii)		[39,43,52]NC-HE, C-NHE
AllophomaAllophoma labilis
(syn. Phoma labilis)		[53]SC-NHE
AlternariaAlternaria alternata
(syn. A. tenuis and Ulocladium alternariae)		[21,26,28,29,31,32,40,46,49,51,53,54,55,56,57,58,59]All environments
Alternaria angustiovoidea[60]C-NHE
Alternaria chartarum
(syn. Ulocladium chartarum)		[21,61]C-NHE
Alternaria dianthi[31]C-NHE
Alternaria longipes[31]C-NHE
Alternaria longissima[28,31,32]NC-HE, C-NHE
Alternaria oudemansii
(syn. Ulocladium oudemansii)		[62]NC-HE, C-NHE
Alternaria tenuissima[21,22,24,31,46,57,63]NC-HE, C-NHE, O-SPE
Alternaria sp.
(syn. Ulocladium sp.)		[10,11,21,23,26,38,41,46,64,65]C-HE, NC-HE, C-NHE, O-SPE
AmphinemaAmphinema sp.[66]C-NHE
AmyloporiaAmyloporia sinuosa
(syn. Antrodia sinuosa)		[11]C-NHE
AntrodiaAntrodia sp.[66]C-NHE
ApiotrichumApiotrichum sp.
(syn. Hyalodendron sp.)		[43]C-NHE
ArachnomycesArachnomyces sp.[45]NC-HE
ArmillariaArmillaria sp.[66]C-NHE
ArthriniumArthrinium arundinis[40]C-NHE
Arthrinium phaeospermum
(syn. Papularia sphaerosperma)		[28,32]NC-HE
Arthrinium sp.[46,65]C-NHE; O-SPE
ArthrobotrysArthrobotrys sp.[23]C-HE
AscochytaAscochyta medicaginicola
(syn. Phoma medicaginis)		[20,56]O-SPE
Ascochyta sp.[63]C-NHE
AscotrichaAscotricha guamensis[32]NC-HE
AspergillusAspergillus aeneus[67]SC-NHE
Aspergillus amstelodami
(syn. Eurotium amstelodami)		[46,55,63]C-NHE
Aspergillus aureolatus[20,56]O-SPE
Aspergillus auricomus[22]O-SPE
Aspergillus candidus[28,32,39,68]C-HE, NC-HE, C-NHE
Aspergillus clavatus[37]C-HE
Aspergillus creber[20,56]O-SPE
Aspergillus echinulatus[21]C-NHE
Aspergillus europaeus[20,56]O-SPE
Aspergillus fischeri
(syn. Neosartorya fischeri)		[62]NC-HE; C-NHE
Aspergillus flavipes[20,56]O-SPE
Aspergillus flavus
(syn. A. oryzae)		[10,17,20,28,30,31,32,56,57,68,69,70,71,72,73,74,75]C-HE, NC-HE, C-NHE, O-SPE
Aspergillus fumigatus[30,31,38,46,61,76,77,78,79]C-HE, NC-HE, C-NHE
Aspergillus glaucus group[79]C-NHE
Aspergillus ivoriensis[67]SC-NHE
Aspergillus japonicus[78]C-HE
Aspergillus melleus[67]SC-NHE
Aspergillus multicolor[67]SC-NHE
Aspergillus nidulans
(syn. Emericella nidulans)		[28,30,31,32,46,51,61,70,71,78]C-HE, NC-HE, C-NHE
Aspergillus niger[10,17,19,20,28,30,31,32,49,50,53,54,55,56,72,74,75,77,80,81,82]All environments
Aspergillus niger group[46]C-NHE
Aspergillus ochraceus[38,49,67]C-HE, C-NHE, SC-NHE
Aspergillus ostianus[20,56,67]SC-NHE, O-SPE
Aspergillus pallidofulvus[20,56]O-SPE
Aspergillus parasiticus[20,56]O-SPE
Aspergillus penicilloides[83]C-HE
Aspergillus petrakii[67]SC-NHE
Aspergillus proliferans[28,32]NC-HE
Aspergillus protuberus[67]SC-NHE
Aspergillus puniceus[67]SC-NHE
Aspergillus repens[21,41]C-NHE
Aspergillus restrictus[63,84]C-HE, C-NHE
Aspergillus sclerotiorum[76]C-NHE
Aspergillus spectabilis
(syn. Emericella spectabilis)		[67]SC-NHE
Aspergillus stellatus
(syn. Emericella variecolor)		[67]SC-NHE
Aspergillus sydowii[28,32,39,51,52,62,69]C-HE, NC-HE, C-NHE
Aspergillus terreus[29,30,31,32,78]C-HE, NC-HE, C-NHE
Aspergillus unguis[76]C-NHE
Aspergillus ustus[46,67]C-NHE, SC-NHE
Aspergillus versicolor[17,28,31,32,39,41,43,46,49,51,55,61,67,68,69,70,71,78,82,84,85,86]C-HE, NC-HE, C-NHE, SC-NHE
Aspergillus wentii[28,31,32]NC-HE, C-NHE
Aspergillus sp.[11,18,19,22,23,24,27,44,45,46,50,64,66,69,75,77,82,87,88,89,90,91,92,93,94,95]C-HE, NC-HE, C-NHE, O-SPE
AureobasidiumAureobasidium pullulans[31,41,43,45,49,52,57]NC-HE, C-NHE
BeauveriaBeauveria bassiana[48]C-NHE
Beauveria sp.[45,52]NC-HE, C-NHE
BisporaBispora sp.[65]O-SPE
BjerkanderaBjerkandera adusta[77]C-NHE
BlastobotrysBlastobotrys aristatus[39]C-NHE
BlastomycesBlastomyces sp.[84]C-HE
BotryotrichumBotryotrichum atrogriseum[17,55,59]NC-HE, C-NHE
Botryotricum domesticum[60]C-NHE
Botryotrichum murorum
(syn. Chaetomium murorum)		[20,21,46,55,56]C-NHE, O-SPE
BotrytisBotrytis cinerea[40,41,43,46,69]C-NHE
BrunneochlamydosporiumBrunneochlamydosporium nepalense (syn. Acremonium nepalense)[38,85]C-HE
BurgoaBurgoa sp.[23]C-HE
CandidaCandida takamatsuzukensis[23,96]C-HE
Candida tumulicola[23,96]C-HE
Candida sp.[23,24,65]C-HE, NC-HE
CaproniaCapronia coronata[85]C-HE
CephalotrichumCephalotrichum verrucisporum
(syn. Doratomyces verrucisporus)		[23,24]C-HE
Cephalotrichum sp.
(syn. Doratomyces sp.)		[23,24]C-HE
CephalosporiumCephalosporium sp.[88,90]C-NHE
ChaetomiumChaetomium ancistrocladum[20,56]O-SPE
Chaetomium elatum[40]C-NHE
Chaetomium globosum[21,22,26,31,32,38,41,46,51,55]C-HE, NC-HE, C-NHE, O-SPE
Chaetomium piluliferum
(syn. Botryotrichum piluliferum)		[21,55]C-NHE
Chaetomium sp.[9,22,27,31,39,40,43,46,65,70,71,72]NC-HE, C-NHE, O-SPE
ChondrostereumChondrostereum sp.[66]C-NHE
ChrysosporiumChrysosporium pseudomerdarium[85]C-HE
Chrysosporium sp.[47,52,62,97]C-HE, NC-HE, C-NHE, O-SPE
CircinellaCircinella muscae
(syn. Circinella sydowii)		[55]C-NHE
CladophialophoraCladophialophora tumulicola[24,98]C-HE
CladosporiumCladosporium cladosporioides[22,28,29,30,31,32,38,41,46,49,51,57,59,68,69,85,99,100]C-HE, NC-HE, C-NHE, O-SPE
Cladosporium cucumerinum[46,49,51]C-HE, C-NHE
Cladosporium herbarum[21,28,31,32,39,46,51,55,58,63,82]C-HE, NC-HE, C-NHE
Cladosporium macrocarpum[60]NC-HE
Cladosporium sphaerospermum[5,7,9,22,28,31,32,39,40,41,42,43,46,48,51,52,62,63,69]C-HE, NC-HE, C-NHE, O-SPE
Cladosporium uredinicola[20,56]O-SPE
Cladosporium xylophilum[60]C-NHE
Cladosporium sp.[15,18,19,22,23,27,42,43,44,45,52,58,62,64,65,66,71,75,77,80,82,86,87,90,91,94,101,102,103]All environments
ClonostachysClonostachys rosea
(syn. Gliocladium roseum)		[58]C-HE
CochliobolusCochliobolus geniculatus (syn. Curvulata geniculata)[32,76]NC-HE, C-NHE
CollariellaCollariella bostrychodes (syn. Chaetomium bostrychodes)[28,32]NC-HE
ColtriciaColtricia sp.[66]C-NHE
CoprinellusCoprinellus aokii
(syn. Coprinus aokii)		[67]SC-NHE
CoprinopsisCoprinopsis atramentaria[38]C-HE
Coprinopsis cothurnata (syn. Coprinus cothurnatus)[63]C-NHE
CordycepsCordyceps farinosa
(syn. Isaria farinosa)		[68]C-HE
CoriolopsisCoriolopsis sp.[66]C-NHE
CunninghamellaCunninghamella echinulata[9,28,32,40,55]NC-HE, C-NHE
Cunninghamella elegans[38]C-HE
Cunninghamella sp.[23,24]C-HE
CurvulariaCurvularia australiensis
(syn. Drechslera australiensis)		[28,29,30,31,32]NC-HE, C-NHE
Curvularia hawaiiensis
(syn. Drechslera hawaiiensis)		[28,29,30,31,32]NC-HE, C-NHE
Curvularia lunata[28,30,31,32,76,83]NC-HE, C-NHE
Curvularia pallescens[29,30,31,32]NC-HE, C-NHE
Curvularia spicifera
(syn. Drechslera spicifera)		[46]C-NHE
Curvularia sp.[75]C-NHE
CutaneotrichosporonCutaneotrichosporon mucoides
(syn. Trichosporon mucoides)		[63]C-NHE
CylindrocarponCylindrocarpon sp.[23,24]C-HE
CyphellophoraCyphellophora olivacea[42]C-HE
Cyphellophora sp.[42]C-HE
CyphellostereumCyphellostereum sp.[66]C-NHE
CystodermaCystoderma sp.[66]C-NHE
DevriesiaDevriesia sp.[45]NC-HE
DichotomophilusDichotomophilus indicus
(syn. Chaetomium indicum)		[55]C-NHE
DidymellaDidymella glomerata
(syn. Phoma glomerata)		[21,40]C-NHE
DipodascusDipodascus geotrichum[55]C-NHE
Dipodascus sp.
(syn. Geotrichum sp.)		[47,75]NC-HE, C-NHE
DiscostromaDiscostroma corticola
(syn. Seimatosporium lichenicola)		[20,56]O-SPE
DrechsleraDrechslera sp.[65]O-SPE
EmericellaEmericella ruber[31]C-NHE
Emericella sp.[49,75]C-HE, C-NHE
EngyodontiumEngyodontium sp.[45,69]C-HE, NC-HE, C-NHE
EpicoccumEpicoccum nigrum
(syn. Epicoccum purpurascens)		[20,28,31,32,46,49,56,58]C-HE, NC-HE, C-NHE, O-SPE
Epicoccum sp.[27,65,87,90]C-HE, NC-HE, C-NHE, O-SPE
EurotiumEurotium halophilicum[104]C-NHE
Eurotium herbariorum[68]C-HE
Eurotium sp.[47,65,89,92]C-HE, NC-HE, C-NHE
ExophialaExophiala angulospora[42,98]C-HE
Exophiala moniliae[85]C-HE
Exophiala sp.[23,42]C-HE
FomitopsisFomitopsis vinosa[63]C-NHE
FusariumFusarium chlamydosporum[51]C-HE
Fusarium culmorum[31]C-NHE
Fusarium equiseti[53]SC-NHE
Fusarium fujikuroi
(syn. F. moniliforme)		[29,30,32,74]C-HE, NC-HE
Fusarium oxysporum[23,28,31,32,38,46,49,58,67,73,105]C-HE, NC-HE, C-NHE, SC-NHE
Fusarium proliferatum[77]C-NHE
Fusarium sporotrichioides[38]C-HE
Fusarium sp.[10,23,24,27,31,39,43,47,62,64,82,91,94,106]C-HE, NC-HE, C-NHE
FuscoporiaFuscoporia sp.[66]C-NHE
FusidiumFusidium viride[48]C-NHE
GanodermaGanoderma sp.[66]C-NHE
GliomastixGliomastix tumulicola
(syn. Acremonium tumulicola)		[23,25]C-HE
Gliomastix sp.[58,97]C-HE
GloiotheleGloiothele sp.[66]C-NHE
HelminthosporiumHelminthosporium sp.[65,75,82]C-NHE, O-SPE
HumicolaHumicola fuscoatra[49]C-NHE
Humicola udagawae[38]C-HE
Humicola sp.[31]C-NHE
HyphodontiaHyphodontia alutaria[66]C-NHE
Hyphodontia sp.[66]C-NHE
HyphodontiellaHyphodontiella sp.[66]C-NHE
HypholomaHypholoma sp.[66]C-NHE
IdriellaIdriella sp.[58]C-HE
KendrickiellaKendrickiella phycomyces[23,24,107]C-HE
KerniaKernia geniculotricha[67]SC-NHE
Kernia hippocrepida[67]SC-NHE
LactariusLactarius sp.[66]C-NHE
LecanicilliumLecanicillium psalliotae[38,59]C-HE, NC-HE
Lecanicillium sp.[68]C-HE
LeptobacilliumLeptobacillium muralicola[37]NC-HE
LeptosphaeriaLeptosphaeria sp.[65]O-SPE
LeptosphaerulinaLeptosphaerulina sp.[64]NC-HE
MacrophominaMacrophomina phaseolina[28,31,32]NC-HE
MalbrancheaMalbranchea sp.[46]C-NHE
MammariaMammaria echinobotryoides[83]C-HE
MemnoniellaMemnoniella sp.[31]C-NHE
MetapochoniaMetapochonia bulbillosa
(syn. Verticillium bulbillosum)		[47]C-HE, NC-HE
Metapochonia suchlasporia
(syn. Verticillium suchlasporium)		[52]NC-HE, C-NHE
MeyerozymaMeyerozyma guilliermondii[60]NC-HE
MicroascusMicroascus brevicaulis
(syn. Scopulariopsis brevicaulis)		[21,52,68]C-HE, NC-HE, C-NHE
Microascus chartarum
(syn. Scopulariopsis chartarum)		[62]NC-HE, C-NHE
Microascus cirrosus[67]SC-NHE
Microascus sp.[68]C-HE
MicrodochiumMicrodochium lycopodinum[38]C-HE
MoniliniaMonilinia sp.
(syn. Monilia sp.)		[82]C-NHE
MonocilliumMonocillium-like[23]C-HE
MonodictysMonodictys castaneae
(syn. Stemphylium macrosporoideum)		[21]C-NHE
Monodictys sp.[31,58]C-HE, C-NHE
MortierellMortierella alpina[47]NC-HE
Mortierella ambigua[38]C-HE
Mortierella parvispora
(syn. M. gracilis)		[31]C-NHE
Mortierella sp.[47,58]C-HE, NC-HE
MucorMucor plumbeus
(syn. M. spinosus)		[21]C-NHE
Mucor racemosus
(syn. M. globosus)		[28,32,47,60]NC-HE
Mucor silvaticus[28,32]NC-HE
Mucor sp.[23,46,58,64,82,93]C-HE, NC-HE, C-NHE
MyxotrichumMyxotrichum stipitatum[46]C-NHE
Myxotrichum sp.[46]C-NHE
NectriaNectria sp.[15]C-NHE
NeocosmosporaNeocosmospora solani
(syn. Fusarium solani)		[23,28,31,76,97,105]C-HE, NC-HE, C-NHE
NeodevriesiaNeodevriesia modesta
(syn. Devriesia modesta)		[99,108]O-SPE
Neodevriesia simplex
(syn. Devriesia simplex)		[99,108]O-SPE
Neodevriesia sp.[45]NC-HE
NeosartoryaNeosartorya sp.[62]NC-HE, C-NHE
NeosetophomaNeosetophoma cerealis
(syn. Coniothyrium cerealis)		[69]C-NHE
NeurosporaNeurospora intermedia[76]C-NHE
Neurospora sp.[82]C-NHE
NigrosporaNigrospora oryzae
(syn. N. sphaerica)		[28,32,82]C-HE, NC-HE, C-NHE
Nigrospora sp.[28,82]NC-HE, C-NHE
OidiodendronOidiodendron cereale[69]C-NHE
Oidiodendron tenuissimum[49]C-NHE
OphiostomaOphiostoma sp.[23]C-HE
PaecilomycesPaecilomyces variotii[28,29,30,31,32,61]NC-HE, C-NHE
Paecilomyces sp.[27,46,68,75,82,97]C-HE, NC-HE, C-NHE
ParengyodontiumParengyodontium album
(syn. Beauveria alba, Tritirachium album, and Engyodontium album)		[9,21,39,40,41,42,43,48,52,59,68,94,103,109,110,111]C-HE, NC-HE, C-NHE
PenicilliumPenicillium aethiopicum[67]SC-NHE
Penicillium albicans[93]C-NHE
Penicillium aurantiogriseum
(syn. P. verrucosum var. cyclopium)		[9,41,43,51]C-HE, C-NHE
Penicillium brevicompactum[39,40,46,68,69,94]C-HE, NC-HE, C-NHE
Penicillium camemberti[93]C-NHE
Penicillium canescens
(syn. P. raciborski)		[40,93]C-NHE
Penicillium carneum[67]SC-NHE
Penicillium chrysogenum
(syn. P. notatum)		[9,21,40,41,46,51,54,60,67,69,81,87,93,112,113]C-HE, NC-HE, C-NHE, SC-NHE
Penicillium citreonigrum
(syn. P. citreoviride)		[22,58]C-HE, O-SPE
Penicillium citrinum[31,32,40,58,76,93]C-HE, NC-HE, C-NHE
Penicillium commune[51,53,68,93]C-HE, C-NHE, SC-NHE
Penicillium concentricum[67]SC-NHE
Penicillium coprobium[67]SC-NHE
Penicillium corylophilum[44,91]C-NHE
Penicillium daleae[91]C-NHE
Penicillium decumbens[9,40,93]C-NHE
Penicillium dierckxii
(syn. P. fellutanum)		[46]C-NHE
Penicillium digitatum[66]C-NHE
Penicillium dipodomyicola[67]SC-NHE
Penicillium expansum[46,49]C-NHE
Penicillium fuscoglaucum[60]C-NHE
Penicillium glabrum
(syn. P. frequentans)		[9,39,46,49,66,93,94]NC-HE, C-NHE
Penicillium granulatum[31]C-NHE
Penicillium griseofulvum[46,56,57,67]C-NHE, SC-NHE
Penicillium herquei[46]C-NHE
Penicillium italicum[53]SC-NHE
Penicillium javanicum
(syn. Eupenicillium javanicum)		[62]NC-HE, C-NHE
Penicillium lanosum[20,56,100]NC-HE, O-SPE
Penicillium lilacinum[21,55]C-NHE
Penicillium meleagrinum[38,69]C-HE, C-NHE
Penicillium miczynskii[47]SC-NHE
Penicillium olsonii[51]C-HE
Penicillium oxalicum[49,58]C-HE, C-NHE
Penicillium pancosmium[38]C-HE
Penicillium paneum[23,67,114]C-HE, SC-NHE
Penicillium polonicum[51]C-HE
Penicillium purpurescens[31]C-NHE
Penicillium purpurogenum[69,93]C-NHE
Penicillium restrictum[93]C-NHE
Penicillium simplicissimum (syn. P. janthinellum)[58,93]C-HE, C-NHE
Penicillium spinulosum
(syn. P. nigricans)		[9,40,84]C-HE, C-NHE
Penicillium thomii[93]C-NHE
Penicillium turbatum[53]SC-NHE
Penicillium verrucosum[39,46]C-NHE
Penicillium vulpinum[67]SC-NHE
Penicillium sp.[11,15,18,19,23,24,26,28,31,43,44,45,46,47,48,58,61,64,66,70,75,77,78,80,82,86,88,89,90,91,94,101]C-HE, NC-HE, C-NHE
PestalotiaPestalotia sp.[26]C-NHE
PhialophoraPhialophora sp.[23,24,43,47]C-HE, C-NHE
PhlebiaPhlebia sp.[66]C-NHE
PholiotaPholiota sp.[66]C-NHE
PhomaPhoma sp.[23,31]C-HE, C-NHE
PhysalacriaPhysalacria sp.[66]C-NHE
PleosporaPleospora sp.[65]O-SPE
PostiaPostia sp.[66]C-NHE
PreussiaPreussia terricola[68]C-HE
Preussia sp.[68]C-HE
PseudogymnoascusPseudogymnoascus pannorum
(syn. Geomyces pannorum and Chrysosporium pannorum)		[39,43,48]C-NHE
PseudozymaPseudozyma prolifica[51]C-HE
PurpureocilliumPurpureocillium lilacinus
(syn. Paecilomyces lilacinus)		[19,38,49]C-HE, C-NHE
PyrenophoraPyrenophora biseptata
(syn. Drechslera biseptata)		[28,32]NC-HE
RadulomycesRadulomyces sp.[66]C-NHE
RhinocladiellaRhinocladiella-like[23]C-HE
RhizoctoniaRhizoctonia solani (syn. Thanatephorus cucumeris)[20,28,32,56]NC-HE, O-SPE
RhizopusRhizopus stolonifer
(syn. R. nigricans)		[28,31,32,53,57,73,74]C-HE, NC-HE, C-NHE
Rhizopus sp.[27,101]NC-HE, C-NHE
RhodotorulaRhodotorula glutinis[49]C-NHE
Rhodotorula mucilaginosa[66]C-NHE
Rhodotorula sp.[15,18,66,69,80,91]C-NHE
RussulaRussula sp.[66]C-NHE
SagenomellaSagenomella griseoviridis[24]C-HE
Sagenomella striatispora[24]C-HE
Sagenomella sp.[44]NC-HE
SarocladiumSarocladium bacillisporum
(syn. Acremonium bacillisporum)		[94]NC-HE
Sarocladium kiliense
(syn. Acremonium kiliense)		[21,52]NC-HE, C-NHE
Sarocladium strictum
(syn. Acremonium cfr. strictum)		[23,52]C-HE, NC-HE, C-NHE
SchizophyllumSchizophyllum commune[64]C-NHE
Schizophyllum sp.[67]C-NHE
SchizoporaSchizopora paradoxa
(syn. Hyphodontia paradoxa)		[64]C-NHE
ScolecobasidiumScolecobasidium anomalum
(syn. Ochroconis anomala)		[115]C-HE
Scolecobasidium lascauxensis[85,115]C-HE
Scolecobasidium tshawytschae
(syn. Ochroconis tshawytschae		[46]C-NHE
ScopulariopsisScopulariopsis brevicaulis[21,55]C-NHE
Scopulariopsis fusca[39]C-NHE
Scopulariopsis sp.[46,47,81,90]NC-HE, C-NHE
ScytalidiumScytalidium sp.[70,71]C-NHE
SimplicilliumSimplicillium lamellicola
(syn. Verticillium lamellicola)		[48]C-NHE
SkeletocutisSkeletocutis sp.[67]C-NHE
SordariaSordaria humana[28,32]NC-HE
SphaerostilbellaSphaerostilbella sp.
(syn. Gliocladium sp.)		[23,93,97]C-HE, C-NHE
SporothrixSporothrix sp.[44,91]NC-HE, C-NHE
SporotrichumSporotrichum sp.[41,43]C-NHE
StachybotrysStachybotrys chartarum
(syn. S. atra)		[21,31,48,54,84]NC-HE, C-NHE
Stachybotrys cylindrosporus[21]C-NHE
Stachybotrys echinatus
(syn. Memnoniella echinata)		[28,31,32]NC-HE
Stachybotrys sp.[9,27,31]NC-HE, C-NHE
StagonosporopsisStagonosporopsis lupini[60]C-NHE
StemphyliumStemphylium botryosum[41]C-NHE
Stemphylium pyriforme[55]C-NHE
Stemphylium sp.[93]C-NHE
StereumStereum sp.[66]C-NHE
SyncephalastrumSyncephalastrum sp.[75]C-NHE
TalaromycesTalaromyces aculeatus[51]C-HE
Talaromyces flavus[38,69]C-HE
Talaromyces pinophilus
(syn. Penicillium pinophilum)		[54,94]C-HE, NC-HE
Talaromyces rugulosus
(syn. Penicillium rugulosum)		[68,69,113]C-HE, C-NHE
Talaromyces variabilis
(syn. Penicillium variabile)		[69]C-NHE
ThysanoreaThysanorea papuana[85]C-HE
TilletiopsisTilletiopsis sp.[69]C-NHE
TorrubiellaTorrubiella alba
(syn. Lecanicillium aranearum)		[94]NC-HE
Torrubiella sp.[68,94]C-HE, NC-HE
TorulaTorula herbarum[55]C-NHE
Torula sp.[46]C-NHE
TricharinaTricharina sp.[64]NC-HE
TrichocladiumTrichocladium asperum[68]C-HE
TrichodermaTrichoderma harzianum[29,30,31,32,69]NC-HE, C-NHE
Trichoderma sect. Longibrachiatum[23,105]C-HE
Trichoderma virens
(syn. Gliocladium virens)		[58]C-HE
Trichoderma viride[23,55,58]C-HE, C-NHE
Trichoderma sp.[19,23,24,31,44,47,75,82,85,95,97]C-HE, NC-HE, C-NHE
TrichotheciumTrichothecium indicum
(syn. Acremonium indicum)		[28,31,32]NC-HE
Trichothecium roseum[21,92]C-NHE
TritirachiumTritirachium sp.[67,82]C-HE, C-NHE
TubariaTubaria sp.[66]C-NHE
TyromycesTyromyces sp.[66]C-NHE
UmbelopsisUmbelopsis ramanniana
(syn. Mortierella ramanniana)		[39,47]NC-HE, C-NHE
VenturiaVenturia carpophila
(syn. Cladosporium carpophilum)		[32]NC-HE
VerticilliumVerticillium alboatrum[32]NC-HE
Verticillium sp.[23,48,52,58,97]C-HE, NC-HE, C-NHE
WallemiaWallemia sebi[63]C-NHE
Wallemia sp.[92]C-NHE
WesterdykellaWesterdykella sp.[64]NC-HE
XylodonXylodon nespoli[66]C-NHE
Xylodon nothofagi[66]C-NHE
Xylodon raduloides[66]C-NHE
ZygosporiumZygosporium masoni[23]C-HE
Basidiomycota (Phylum)[64]NC-HE
Black meristematic fungi[5,99,116]NC-HE, O-SPE
Chaetomiaceae (Family)[64]NC-HE
Filobasidiales[64]NC-HE
Hyaline sterile mycelia[62]NC-HE, C-NHE
Melanized sterile mycelia[62]NC-HE, C-NHE
Pezizomycotina (Subphylum)[64]NC-HE
Undetermined dark pigmented fungi[17]O-SPE
Undetermined yeasts[46]C-NHE
Uredinales (Order)[65]O-SPE
Ustilaginales (Order)[65]O-SPE
Table
Table 2. Contingency table and affinity indices. (A) Contingency table between the obtained clusters and the environmental categories to which they are correlated and (B) their relative affinity indices.
Table 2. Contingency table and affinity indices. (A) Contingency table between the obtained clusters and the environmental categories to which they are correlated and (B) their relative affinity indices.
(A)Contingency Table
Clusters
131114361582451109712
Environmental categoriesC-HE 1 5323
NC-HE 2 11611 1
C-NHE1111 211137 11 1
SC-NHE 1 11
O-SPE 2 11
(B)Affinity Indices
Clusters
131114361582451109712
Environmental categoriesC-HE 1.82 4.81.371.468.2
NC-HE 3.93 1.310.215.890.390.98 3.93
C-NHE1.281.281.280.64 1.7118.986.25 1.281.28 1.28
SC-NHE 17 10.71
O-SPE 12.8 0.670.53
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Zucconi, L.; Canini, F.; Isola, D.; Caneva, G. Fungi Affecting Wall Paintings of Historical Value: A Worldwide Meta-Analysis of Their Detected Diversity. Appl. Sci. 2022, 12, 2988. https://doi.org/10.3390/app12062988

AMA Style

Zucconi L, Canini F, Isola D, Caneva G. Fungi Affecting Wall Paintings of Historical Value: A Worldwide Meta-Analysis of Their Detected Diversity. Applied Sciences. 2022; 12(6):2988. https://doi.org/10.3390/app12062988

Chicago/Turabian Style

Zucconi, Laura, Fabiana Canini, Daniela Isola, and Giulia Caneva. 2022. "Fungi Affecting Wall Paintings of Historical Value: A Worldwide Meta-Analysis of Their Detected Diversity" Applied Sciences 12, no. 6: 2988. https://doi.org/10.3390/app12062988

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