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Black Fungi on Stone-Built Heritage: Comparison
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Please note this is a comparison between Version 1 by Filomena De Leo and Version 2 by Vivi Li.

Black Fungi are one of the main group of microorganisms responsible for the biodeterioration of stone cultural heritage artifacts. The term “bColack fungi” refers to a very huge group of dematiaceous fungi, unrelated phylogenetically, which have in common the presence of melanin in the cell wall that confers an olive brown appearance to the colony. Another common characteristic is the ability to withstand hostile environments such as scarcity of nutrients, high solar irradiation, scarcity of water, high osmolarity, and low pHonization pattern, taxonomy, and methods to eradicate their settlement are discussed here.

  • stone cultural heritage
  • black fungi
  • MCF
  • biodeterioration
  • control

1. Background

Stonework, such as artistic sculptures, historical buildings, monuments, archaeological sites, caves, etc., are ubiquitous across the globe, being an expression of culture, religion, aesthetics, and building techniques of populations, typical of certain historical construction periods. Due to their unicity and intrinsic value, ensuring the integrity of stone-built heritage for posterity is a critical issue. The study of biodeterioration of cultural heritage is a hot topic of broad interest to the researcher’s community and the implementation of safeguard measures is one of the main goals. All materials are subjected to a natural weathering, and “biodeterioration” of stones should be considered as an integral part of bio-geo-morphogenesis [1][2][3][4]. The term “biodeterioration” defines any irreversible transformation of inorganic or organic material with economic, commercial, historic, and artistic loss caused by macro- and micro-organisms [5].
“Biodeterioration” is a very complex matter and conservators should also take into account whether the observed biologically driven phenomena can even be considered positive for the artifact.
In fact, in some cases, the presence of subaerial biofilm (SABs) may have a protective effect on the surface [6]; on the other hand, SABs developed at the interface between rock surface and air is considered the main cause of biodeterioration of stone monuments [7][8].
Microbial biodeterioration of stones is often associated with the presence of a complex community formed by chemoorganotrophic microorganisms (bacteria and microfungi) and autotrophic microorganisms (such as algae and cyanobacteria and to lesser extent autotrophic bacteria) usually embedded in an extracellular matrix EPS (in which are present DNA, enzymes, pigments, lipids, proteins, etc.). Microbial cells in the EPS show a typical biofilm lifestyle that confers resistance to hostile environments and reinforces the attachment of microorganisms on the surface [6][9].
The prevalence of one or more group of microorganisms depends on numerous factors which include the intrinsic characteristics of the material (such as lithotype, porosity, roughness, and state of preservation) that affect its “bioreceptivity” sensu Guillitte [10]. The species composition can vary greatly depending on climatic and microclimatic conditions such as temperature, solar irradiation, shining, nutrient and water availability, and, last but not least, the characteristics of species involved [6]. However, microbial colonization is a very dynamic process in time and space, that is the result of the interactions between microbial species and substrates. It varies continuously during the year following the seasons, and it is also under the influence of the dispersion ability of propagules in the air [11][12][13].
In recent years, much knowledge has been gained about rock-inhabiting black fungi, and important issues concerning their taxonomy, physiology, phylogeny, and weathering processes [14] have been clarified. However, the majority of studies concerned black fungi from natural environments [4][7][15].
In the field of cultural heritage, most reviews had as a topic the biodeterioration of stone caused by fungi in general [6][16][17]; some have focused on the microbial and fungal deterioration of various type of substrata (both organic and inorganic such as textile, parchment, wood, paper, metals, and stone) used for artworks [18]; few concerned exclusively black fungi as a cause of biodeterioration of stone monuments [19][20].

2. Black Fungi and Stone Monuments: An Intimate Connection

Beginning in the 1990s, black fungi were described as one of the most likely groups of microorganisms responsible for the biodeterioration of the stone monuments [21][22][23][24] and it was confirmed in the following decades [6][18][25][26]. The term “black fungi” refers to a very huge group of dematiaceous fungi, unrelated phylogenetically, which have in common the presence of melanin in the cell wall that confers an olive brown appearance to the colony [27]. Another common characteristic is the ability to withstand hostile environments such as scarcity of nutrients, high solar irradiation, scarcity of water, high osmolarity, and low pH [15][19][28]. As reported by Gueidan et al. [29] the ancestors of black fungi were well adapted to live in oligotrophic environments such as rock surfaces or sub-surfaces, and currently they can also grow in anthropogenic habitats such as glass, silicon, organic surfaces, metals [30], or consolidants applied on the stone [9]. Their resilience is related to the extremotolerant or even polyextremotolerant characteristics of the species. The stress-tolerance is due to different factors such as: pigmentation, and in particular melanins production; mycosporine-like substances; morphological and metabolic versatility; meristematic development; and oligotrophy [31][32][33]. All these characteristics make them very suitable for colonizing outdoor rocks and built stones due to the fact that those surfaces can be exposed to extreme environments [17][18][19]. This group of fungi includes (a) fast growing hyphomycetes of epiphytic origin, recognizable under microscope by the presence of typical conidiophores and spores; (b) pleomorphic hyphomycetes that include the “black yeasts”, showing a yeast-like form, and the so-called “black meristematic fungi” with a Torula-like growth pattern (Figure 1).
Applsci 12 03969 g001 550
Figure 1. Main morphological characteristic traits of MicroColonial Fungi, MCF. Dark black colonies due to the melanin production as seen (a) for the unidentified strain MC 655 on different cultural media after 1 month of incubation. (b–d) characteristic meristematic pattern of growth described also as Torula-like hyphae observed under Light Microscope. Bar is 10 μm.
Hyphomycetes and black yeasts are ubiquitous and widespread all over the world in very different habitats (e.g., soil, fresh water, sea, plants, animals, and humans) [27][34], while the meristematic black fungi, mostly isolated from stone or natural rocks, can be considered the true stone-inhabiting fungi [19][20][35][36]. In the literature, many of black fungi are reported as RIF (rock inhabiting fungi) to emphasize that the “rock” is their preferred or exclusive habitat. However, this terminology does not include their main features such as melanin production, pleomorphism, or meristematic development; for this reason, rwesearchers do not use it in this context. In the frame of cultural heritage the acronym MCF (MicroColonial Fungi) as first employed by Staley [37] is widely used for their description. It refers to the typical black cauliform-like colonies visible on the rocks and stones. Humidity may affect the settlement of MCF on the stone artifacts as unique inhabitants or as associated with other stone colonizers. In fact, in lower or sheltered parts near the ground, where there is a sufficient availability of water, MCF are strictly associated with phototrophic microorganisms with whom, however, they do not establish a symbiotic relationship (Figure 2); in harsh, dry micro-environmental conditions, MCF become the unique colonizers [38][39][40].
Applsci 12 03969 g002 550
Figure 2. Close association between MCF and phototrophic microorganisms. (a) Association seen directly on a marble sample. Magnification 400X and (b) after growth in the isolation medium PDA: Chlorella-like alga and Coniosporium apollinis MC 728. Magnification 80X.
Black fungi are currently classified in the Phylum of Ascomycota in the Class of Dothideomycetes and Eurotiomycetes, mainly in the order of Capnodiales, Dothideales, Chaetothyriales, Pleosporales and Cladosporiales, and Mycocaliciales [14][20][41][42]. In Table 1 are listed the genera of black fungi identified through molecular analyses that from 1997 up to date have been related to the biodeterioration of stone monuments.
Table 1. Genera of black fungi isolated from stone monuments in the period from 1997–2022 in association with visible alterations.
Class/Order Genera * Substrate Environmental and Climatic Features Alterations Associated to Fungal Colonization Refs
Dothideomycetes incertae sedis Coniosporium Calcarenite, granite, limestone, marble Mediterranean climate, urban environment Grayish-black patina, pitting, black spots, greenish to dark green patina, crater shaped lesions, chipping, exfoliation, sugaring, crumbling, superficial deposit, and biofilm [36][38][43][44][45][46][47][48][49]
Dothideomycetes/Capnodiales incertae sedis Capnobotryella Limestone, marble Mediterranean climate,

continental climate, and urban environment		 Black spots, crater shaped lesions, chipping, exfoliation, sugaring, crumbling, pitting, superficial deposit, and biofilm formation [45][48][50][51][52]
Constantinomyces Sandstone Urban environment, temperate climate Discolorations, patina [53]
Pseudotaeniolina Marble, sandstone Mediterranean climate, arid and desert climate Biological green patina [54][55][56]
Dothideomycetes/Capnodiales Aeminium Limestone Temperate climate Black discoloration with salt efflorescence [57]
Dothideomycetes/Cladosporiales Cladosporium Calcarenite, granite, limestone, marble, plaster, sandstone, tufa Ubiquitous worldwide distribution in indoor environments and outdoor Dark alterations, black spots, black patinas, detachment of marble grains, light grayish patina, crater shaped lesions, chipping, exfoliation, sugaring, crumbling, pitting, superficial deposit, biofilm, black crusts, green biofilm with salt efflorescence, stone erosion and disintegration, and discoloration [26][39][46][48][49][58][59][60][61][62][63][64][65][66][67]
Verrucocladosporium Limestone, marble, sandstone Mediterranean climate, temperate climate, and urban environment Black patina, discoloration [36][53]
Dothideomycetes/Dothideales Aureobasidium Granite, limestone, marble,

plaster, sandstone		 Urban environment, Mediterranean climate, temperate climate, indoor environment, and urban environment Black patina, black spots, detachments, superficial deposit, biofilm, discolorations with or without salt efflorescence, black crusts, and stone erosion and disintegration [36][39][45][49][53][63][64][65][68]
Dothideomycetes/Mycosphaerellales Salinomyces Marble, sandstone Mediterranean climate Black patina [36]
Neocatenulostroma Limestone, sandstone Temperate climate, urban environment Discolorations and/or patina, structural damage [53]
Neodevresia Limestone, marble, plaster, tufa Mediterranean climate Black patina, discolorations, structural damage [36][53][55][63]
Saxophila Marble Mediterranean climate Black patina [36]
Vermiconidia Limestone, marble, travertine Mediterranean climate, urban environment Black patina Neodevriesia sardiniae[36]
CCFEE 6202 KP791765 Dothideomycetes/Neophaeothecales Neophaeotheca Marble Mediterranean climate Black patina [
Neodevriesia sardiniae CCFEE 621036]
KP791766 Dothideomycetes/Pleosporales Alternaria Calcarenite, granite, limestone, marble, plaster, tufa Ubiquitous worldwide distribution in indoor environments and outdoor Black spots, black patina, detachment of marble grains, greenish to dark green patina, biofilm, black crusts, green-black patina; and blackish patina [39]
Saxophila tyrrhenica[46][49 CCFEE 5935][58][59][60][63][64][66][67]
KP791764 Epicoccum Granite, limestone, marble Urban environment, mediterranean climate, and temperate climate Black spots, black patinas, detachment, superficial deposit, biofilm, blackish patina, green biofilm, and dark and green biofilm with salt efflorescence [39][45][49][60][64]
Aeminium ludgeri E12 MG938054 Phoma Calcarenite, granite, limestone, marble, plaster, tufa Mediterranean climate, temperate climate, urban environment, continental-cold climate, and indoor and outdoor environments Black spots, black patinas, detachment of marble grains; color changes, crater shaped lesions, chipping and exfoliation, sugaring, crumbling, pitting, superficial deposit, biofilm, and black crusts [39][46][48][49][58][63]
Aeminium ludgeri E16 MG938061 Dothideomycetes/Venturiales Ochroconis Calcarenite Subterranean environment Black patina
Neocatenulostroma sp. CR1[69]
KY111907 Eurotiomycetes incertae sedis
ConstantinomycesSarcinomyces Marble Mediterranean climate Black spots [70]
Eurotiomycetes/Chaetothyriales Cyphellophora sp. Plaster Mediterranean climate Black/grayish patina [63]
Exophiala Calcarenite, limestone, marble,

sandstone		 Mediterranean climate, urban environment, temperate climate, and hypogean environment Dark alterations, black spots, black patinas, detachment of marble grains, discolorations, and visible structural damage [26][36][39][45][53][71]
Lithophila Limestone, marble Mediterranean climate, urban environment, and

dry continental climate		 Black spots, black patinas, detachment of marble grains [36][39][72]
Knufia Limestone, marble, sandstone

travertine		 Mediterranean climate, urban environment, continental temperate climate, and dry continental climate Black and grey spots, dark macropitting, biopitting, crater shaped lesions, chipping, exfoliation, sugaring, crumbling, discolorations, patina, and visible structural damage [36][40][43][45][48][53][72][73][74]
Rhinocladiella Marble Mediterranean climate Black spots, crater shaped lesions, chipping and exfoliation, sugaring, crumbling, and pitting [48]
Eurotiomycetes/Mycocaliciales Mycocalicium Marble Mediterranean climate, urban environment Black spots, crater shaped lesions, chipping and exfoliation, sugaring, crumbling, and pitting [45][48]
* According to the current taxonomic nomenclature.
In manuscripts published prior to 1999, black meristematic fungal species that were identified without molecular analyses, such as Hormonema dematioides, Lichenothelia sp. and Hortaea werneckii, Trimmatostroma sp., are listed among the most abundant fungal species present in arid and semiarid environments in association with biodeterioration of stone monuments [3]. The molecular analyses introduced at the end of the 20th century considerably increased the knowledge about the taxonomy of the black fungi isolated from stone monuments and allowed the description of twenty-six new species and three new genera. The new species and genera described are listed below: Sarcinomyces petricola Wollenzien and de Hoog [73]; S. sideticae Sert and Sterflinger [70]; Coniosporium apollinis Sterflinger, C. perforans Sterflinger [43]; C. uncinatum De Leo, Urzì and de Hoog [44]; C. sumbulii Sert and Sterflinger [47]; Phaeococcomyces chersonesos Bogomolova and Minter [74]; Pseudotaeniolina globosa De Leo, Urzì and de Hoog [54]; Capnobotryella antaliensis Sert and Sterflinger [50]; C. erdogani Sert and Sterflinger; C. kiziroglui Sert and Sterflinger [51]; Ochroconis lascauxensis Nováková and Martin-Sanchez; O. anomala Nováková and Martin-Sanchez [69]; Knufia marmoricola Onofri and Zucconi, K. vaticanii Zucconi and Onofri; K. karalitana Isola and Onofri; K. mediterranea Selbmann and Zucconi [36]; K. calcarecola Su, Sun and Xiang [72]; Exophiala bonarie Isola and Zucconi; Vermiconia calcicola de Hoog and Onofri [36]; Devriesia simplex Selbmann and Zucconi; D. modesta Isola and Zucconi [55]; and D. sardiniae Isola and de Hoog [36]. Three new genera and 4 species were also introduced as new: Saxophila tyrrenica Selbmann and de Hoog, Lithophila guttulata Selbmann and Isola [36], L. catenulata Su, Sun and Xiang [72], and Aeminium ludgeri Trovão, Tiago and Portugal [57]. Over the years, some of the above mentioned genera and species were reclassified: in particular, Sarcinomyces petricola and Phaecoccomyces chersonesos resulted identical, and they were reclassified as Knufia petricola [75][76]; Coniosporium perforans is now a synonym with Knufia perforans [76]; Devriesia species and Vermiconia species were included, respectively, in the new genera of Neodevriesia [77] and Vermiconidia [41]. Hao et al. [78] proposed a revision of the genus Ochroconis that was established as synonymous with the sister genus of Scolecobasidium. However, this taxonomic accommodation has been refused by Samerpitak et al. [79][80] on the basis of phylogenetic analyses and because the old generic name Scolecobasidium is considered of doubtful identity for the ambiguity of type specimens; therefore, the genus Ochroconis that is also characterized by oligotrophism and mesophilia was maintained. However, many questions regarding the taxonomy and phylogeny of black fungi are still unresolved and further studies are required, especially to clarify the taxonomical position and phylogeny of many species of incertae sedis and of strains that are preserved in the mycological collections and are not yet identified (Figure 3, Table 2).
Applsci 12 03969 g003 550
Figure 3. Phylogenetic tree (Neighbour-joining, Kimura two-parameters) showing the genetic divergence among ITS rDNA sequences of meristematic black fungi retrieved from GenBank database (https://www.ncbi.nlm.nih.gov/nucleotide accessed on 14 February 2022) and listed in Table 2.
Table 2.
ITS rDNA sequences of representative MCF isolated from stone monuments aligned in
Figure 3
.
Taxon Strain ITS rDNA
Capnobotryella antalyensis MA 4615 AJ972858
Capnobotryella antalyensis MA 4624 AJ972850
Capnobotryella antalyensis MA 4766 AJ972851
Capnobotryella antalyensis MA 4775 AJ972860
Capnobotryella isilogui MA 3619 AM746201
Capnobotryella erdogani MA 4625 AJ972857
Capnobotryella kirizoglui MA 4899 AJ972859
Capnobotryella sp. MA 4701 AJ972856
Capnobotryella sp. MA 4697 AJ972855
Capnobotryella sp. MA 3615 AM746203
Neodevriesia modesta CCFEE 5672 KF309984
Neodevriesia simplex CCFEE 5681 KF309985
sp.
CR21
KY111911
Pseudaeniolina globosa DPS10 MH396690
Pseudotaeniolina globosa CBS109889 NR136960
Pseudotaeniolina globosa CCFEE5734 KF309976
Vermiconidia calcicola CBS 140080 NR_145012
Vermiconidia calcicola CCFEE 5780 KP791761
Vermiconidia flagrans CCFEE 5922 KP791753
Coniosporium uncinatum CBS 100219 AJ244270
Coniosporium apollinis CBS 100213 AJ244271
Coniosporium apollinis CBS 352.97 NR159787
Coniosporium apollinis CBS 100216 AJ244272
Coniosporium apollinis QIIIa MH023395
Lithophila catenulata BJ10118 JN650519
Lithophila guttulata M1 MW361305
Lithophila guttulata CCFEE 5884 KP791768
Lithophila guttulata CCFEE 5907 KP791773
Knufia mediterranea CCFEE 5738 KP791791
Knufia mediterranea CCFEE 6211 KP791793
Knufia vaticanii CCFEE 5939 KP791780
Knufia calcarecola SL11033 JQ354925
Knufia calcarecola CGMCC 3.17222 KP174862
Knufia marmoricola CCFEE 5895 KP791775
Knufia marmoricola CCFEE 5716 KP791786
Knufia perforans CBS 885.95 AJ244230
Knufia karalitana CCFEE 5732 KP791782
Knufia karalitana CCFEE 5929 KP791783
Knufia petricola CCFEE 726.95 KC978746
Knufia petricola CBS 600.93 KC978744
Knufia petricola IMI38917 AJ507323
Knufia petricola D1 JF749183
Knufia petricola M4 FJ556910
Knufia sp. QIIa MH023393
Knufia sp. QIIb MH023394

3. How to Control Black Fungi

Very little is said regarding the effectiveness of treatments against black fungi. Black fungi, especially meristematic ones, are very difficult to eradicate and tend to be one of the first colonizers after cleaning procedures.  In order to achieve protection of an artifact, both indirect and direct methods should be implemented. Direct treatments aiming to kill/reduce black fungi on the stone should be different on the basis of their colonization pattern (diffuse patina, spot-like colonization, or intercrystalline growth) and on the characteristics of the environment.  Among the potential methods commonly used to control biodeterioration, physical methods such as mechanical removal and UV and heat shock treatments[81][82], are not very effective against black fungi[83][84]. Regarding chemical methods, in laboratory conditions, classical biocides (e.g., Preventol RI 50, Biotin R, RocimaTM 103) are still the most effective [83][85] and in the field they produce efficient results during cleaning procedures. Plant based extracts show a scarce effectiveness against fungi, and this difficult group of microorganisms is not even taken into account to assess their activity[86]. Nanoparticles are commonly used as biocides due to their activity against algae, cyanobacteria, and most bacteria, but they are not really satisfactory against black fungi. Protective coatings with antifouling properties may have various effects. In fact, TiO2 based coatings, pure or doped with Ag, show a good effect but are limited to a short/medium term after application [86]. However, in both laboratory and field conditions, after treatments with titania-based coatings, black fungi are the first to recolonize the stone surface in dry environments, while algae first appears in damping walls[63]. Very recently, in laboratory conditions, cholinium@Il based coatings have shown that the use of Il’s with a 12 C chains and DBS as anion in combination with nanosilica coatings (e.g., Nano Estel) could be effective against the colonization of black fungi for a period of time over 30 months [87]. One possible explanation of this scarce effectiveness of most treatments against black fungi is that they possess a genetic resistance to environmental stresses, as reported the previous paragraphs. Therefore, the different mechanisms concurring to the stress protection response may interfere to the biocidal treatments. Understanding the cause of their resilience could improve the strategies for their control.

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