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Current Knowledge on the Fungal Degradation Abilities Profiled Through Biodeteriorative Plate Essays

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Current Knowledge on the Fungal Degradation Abilities Profiled Through Biodeteriorative Plate Essays applied sciences Review Current Knowledge on the Fungal Degradation Abilities Profiled through Biodeteriorative Plate Essays João Trovão 1,* and António Portugal 1,2 1 Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, 3004-531 Coimbra, Portugal; [email protected] 2 Fitolab-Laboratory for Phytopathology, Instituto Pedro Nunes, 3030-199 Coimbra, Portugal * Correspondence: [email protected] Abstract: Fungi are known to contribute to the development of drastic biodeterioration of historical and valuable cultural heritage materials. Understandably, studies in this area are increasingly reliant on modern molecular biology techniques due to the enormous benefits they offer. However, classical culture dependent methodologies still offer the advantage of allowing fungal species biodeteriorative profiles to be studied in great detail. Both the essays available and the results concerning distinct fungal species biodeteriorative profiles obtained by amended plate essays, remain scattered and in need of a deep summarization. As such, the present work attempts to provide an overview of avail- able options for this profiling, while also providing a summary of currently known fungal species putative biodeteriorative abilities solely obtained by the application of these methodologies. Conse- quently, this work also provides a series of checklists that can be helpful to microbiologists, restorers and conservation workers when attempting to safeguard cultural heritage materials worldwide from biodeterioration. Keywords: biodeterioration; cultural heritage; deteriorative action; enzymatic activity; fungi Citation: Trovão, J.; Portugal, A. Current Knowledge on the Fungal Degradation Abilities Profiled through Biodeteriorative Plate Essays. 1. Introduction Appl. Sci. 2021, 11, 4196. https:// The Fungal Kingdom comprises a highly diverse eukaryotic group able to inhabit ev- doi.org/10.3390/app11094196 ery ecological niche available on the Planet [1]. The growth and biological activity of fungal species in cultural heritage materials is known to develop serious damages by means of Academic Editor: Daniela Isola biodeterioration (the undesirable modifications of a valuable material occurring by the ac- tion of living organisms) [2,3]. Fungi are highly versatile, ubiquitous, chemoheterotrophic Received: 26 March 2021 microorganisms, being able to grow in a vast number of materials and contributing to Accepted: 27 April 2021 Published: 5 May 2021 the development of various biodeterioration phenomena [2,3]. Such modifications are a result from fungal species settling, development and exploitation of various organic and Publisher’s Note: MDPI stays neutral inorganic compounds present in historic art-pieces and monuments [2–15]. The fungal with regard to jurisdictional claims in biodeterioration of books, paper, parchment, textiles, photographs, paintings, sculptures published maps and institutional affil- and wooden materials occurs due to the aesthetic modifications, mechanical pressure and iations. exoenzymatic action [2]. Various components of these materials such as cellulose, collagen, linen, glues, inks, waxes and organic binders can be oxidized, hydrolyzed, dissolved, stained or structurally modified as a result of the action of fungal enzymes, pigments and organic acids [2,3,7–11]. A typical and widely known example of these phenomena is known as “foxing”, the development of red-brownish localized spots, hypothesized Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. to be a result from fungal proliferation and metabolization of organic acids, oligosaccha- This article is an open access article rides and proteic compounds that can stain and modify the constituent materials of many distributed under the terms and paper-based and photographic supports [3,8,13]. Another example of microorganism’s conditions of the Creative Commons attack of organic materials is related to the biodeterioration of human remains, mummies Attribution (CC BY) license (https:// and funerary materials, where opportunistic, saprotrophic and highly cellulolytic and creativecommons.org/licenses/by/ proteolytic taxa are able to thrive and trough their actions severely alter them [2,14,15]. 4.0/). Complementarily, historic relics mainly composed of inorganic components such as stone, Appl. Sci. 2021, 11, 4196. https://doi.org/10.3390/app11094196 https://www.mdpi.com/journal/applsci Appl. Sci. 2021, 11, x FOR PEER REVIEW 2 of 37 Appl. Sci. 2021, 11, 4196 2 of 24 them [2,14,15]. Complementarily, historic relics mainly composed of inorganic compo- nents such as stone, frescoes, glass and ceramics can also suffer deep aesthetical, physical frescoes,and chemical glass andmodifications ceramics can resulting also suffer from deep fungal aesthetical, grow and physical action and [2–6,12,16]. chemical In modifi- these cationssupports, resulting deterioration from fungal is caused grow by and hyphae action pe [2netration–6,12,16]. into In thesethe substrate, supports, the deterioration production isand caused release by of hyphae extracellular penetration destructive into the organi substrate,c acids, the enzymes production and metabolites and release and of extra-by the cellularthe formation destructive of distinct organic colored acids, outlines enzymes as anda result metabolites of fungi andhigh by pigment the the contents, formation con- of distincttribution colored to biofilm outlines development as a result and of fungi chemical high pigmentreactions contents, with inorganic contribution compounds to biofilm [2– development6]. and chemical reactions with inorganic compounds [2–6]. DueDue toto thethe knownknown biodeterioration biodeterioration problems problems arising arising from from their their proliferation, proliferation, the the accu- ac- ratecurate species species identification identification and and a consequenta consequent deteriorative deteriorative profiling profiling of of isolates isolates are are crucial crucial stepssteps towardstowards thethe developmentdevelopment andand thethe establishmentestablishment ofof properproper protectiveprotective measuresmeasures forfor thethe diversediverse culturalcultural heritageheritage treasurestreasures aroundaround thethe world.world. WithWith thethe recentrecent developmentdevelopment ofof innovativeinnovative culture culture independent independent methodologies methodologies such such as -omics as -omics technologies, technologies, molecular molecular data isdata becoming is becoming increasingly increasingly more valuable more valuable for the identificationfor the identification of the microbes, of the microbes, the character- the izationcharacterization of their metabolic of their functions metabolic and functions their deteriorative and their byproductsdeteriorative [17 ].byproducts Methodologies [17]. suchMethodologies as metagenomics, such as transcriptomics, metagenomics, metabolomics transcriptomics, and metabolomics proteomics revolutionized and proteomics the fieldrevolutionized and are increasingly the field and allowing are increasingly understanding allowing of microbial understanding diversity, of butmicrobial also species diver- specificsity, but and also holistic species contributions specific and holistic to various contributions materials biodeteriorationto various materials phenomena biodeteriora- [17]. Thesetion phenomena methods are [17]. particularly These methods relevant are considering particularly that relevant traditional considering cultivation that dependent traditional methodologiescultivation dependent hold the methodologies disadvantage ofhold being the unabledisadvantage to correctly of being infer unable microorganism’s to correctly abundanceinfer microorganism’s and only allow abundance the study and ofonly active allow forms, the study failing of toactive provide forms, information failing to pro- re- gardingvide information viable non-culturable regarding viable and non-viablenon-culturab formsle and [17 non-viable–27]. Nonetheless, forms [17–27]. classical Nonethe- culture dependentless, classical methodologies culture dependent still offer methodologie an importants advantagestill offer an when important compared advantage with modern when methodologies,compared with especiallymodern methodologies, when considering especial thatly thewhen isolation considering of microbes that the allows isolation their of naturalmicrobes biodeteriorative allows their natural profiles biodeteriorative to be studied in greatprofiles detail. to be Culture studied media in great plates detail. modified Cul- toture specify media a plates positive modified biodeteriorative to specify ability a positive upon biodeteriorative the microorganism ability development upon the micro- and deteriorativeorganism development action (see and Figure deteriorative1 for examples) action can (see provide Figure valuable 1 for examples) data that can allow provide the evaluationvaluable data of the that microorganism’s allow the evaluation putative of th riskse microorganism’s to cultural heritage putative materials. risks Moreover,to cultural theyheritage also materials. offer a highly Moreover, informative, they also rapid offer and a highly low-cost informative, platform rapid [28] thatand canlow-cost help plat- in a quickform [28] and that focused can decision-makinghelp in a quick and process focused aiming decision-making to protect valuable process artifacts. aimingCurrently, to protect platevaluable assays artifacts. aiming Currently, to identify plate fungal assays deteriorative
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