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Biodeterioration Of Historic Buildings In Latin America

CC Gaylarde & PM Gaylarde1

Dept. Biophysics & 1MIRCEN, Federal Uni Rio Grande do Sul, Porto Alegre, Brazil

Summary: Buildings of cultural heritage are discolored and degraded by the growth and activity of living organisms. Microorganisms form biofilms on the surfaces of stone and painted buildings, with resulting aesthetic and structural damage. The organisms involved are bacteria (including actinomycetes and cyanobacteria), fungi and algae, but protozoa and other small animals are also found. The interactions between these organisms can enhance or retard the overall rate of degradation. In addition, microorganisms within the structure (endoliths) may cause damage. These may grow in cracks and pores within the materials and may bore into rocks such as limestone. True endoliths, present within the rock itself, rather than in voids in the rock, are found in materials such as soapstone and are predominantly bacterial. A review of work on microbial biofilms on buildings of historic interest in various Latin American countries is presented and the microbial activities which lead to degradation of the structures are described.

Keywords. Biodeterioration, cultural heritage, microorganisms, weathering

1 INTRODUCTION Both historic and modern buildings are subject to the deteriorative and degradative action of the environment and living organisms, normally referred to as "weathering". Biological and abiotic processes can occur concurrently, each contributing to the overall deleterious effects, and it can be difficult to determine the contribution of each. However, there is no doubt that biological growths have considerable impact on the soundness of structural materials.

Fig. 1. Mosses and higher plants growing on limestone building of the Mayan civilization at Sayil, Yucatan, Mexico

The destructive effects of mosses and higher plants are readily recognized. The root structures penetrate and disrupt the structure of the building (Fig. 1), but plant growth occurs only after a "protosoil" has been produced by the growth and degradative activity of other organisms, less obvious to the naked eye - microorganisms. These form so-called "biofilms" on any humid surface, even if a water layer is not detectable; such biofilms, apart from serving to prepare the surface for plant growth, can themselves have considerable impact on building materials. The problems associated with microorganisms are not familiar to architects and engineers, and are generally disregarded by them; however, microbial activities are potential threats to the maintenance of modern buildings, as well as historic and cultural property. The activities of microorganisms in biofilms are shown in Table 1. Since the organisms are present on the surface of the materials, their activities are localized and concentrated at these points.

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Table 1. The effects of microbial activities on historic buildings

Observed effect Microbial activity Material(s) Major microorganisms Discoloration Physical presence All Algae, cyanobacteria, fungi Retention of water Physical presence,

EPS All All

Stimulation of growth of heterotrophic and higher organisms

Physical presence Clean surfaces Algae, photosynthetic bacteria, including cyanobacteria

Breakdown of material Hydrolytic enzymes Wood, painted surfaces

Fungi, bacteria

Disaggregation of material

Filamentous growth form

Stone, concrete, mortar, wood

Fungi, actinomycetes, cyanobacteria, algae, lichens

Formation of patinas Oxidation of translocated cations

Stone Iron and manganese oxidising bacteria; fungi, cyanobacteria

Degradation (“Corrosion”)

Acid production Stone, concrete, mortar

Fungi, bacteria, lichens

Weakening and dissolution of structure

Mobilisation and chelation of ions

Stone, brick, concrete, mortar

All

Alkaline dissolution Uptake of H+ ions by cells

Stone Algae, cyanobacteria

Disruption of layered silicates

Liberation of polyols (e.g. glycerol, polysaccharides)

Mica, soapstone

All

Microbial biofilms, complex associations of microscopic organisms and their metabolic products, may be visible or invisible to the naked eye. Almost all surfaces can be so colonized (Koestler et al., 1985; Griffin et al., 1991). "Soiling" and discoloration of buildings is usually evidence of a biofilm, but even invisible biofilms can be a threat to the structure, producing acids and other substances (see Table 1), which can degrade the surfaces of mineral materials and cause spalling (flaking) of surface coatings. The rate of colonization is determined by environmental, as well as biological, factors. Temperature, humidity, light intensity and the physico-chemical nature of the surface of the material all play an important role. Generally, hard, polished stone of low porosity is more resistant to the degradative attack of microorganisms, but all rocks are susceptible to biofilm formation. The various types of stone used in historic constructions in Latin America are shown in Table 2, with examples of the important cultural sites built using these materials.

Table 2. Rocks used as constructional materials in historic buildings in Latin America (LA)

Rock type Examples Porosity (%)

Other relevant characteristics

Examples of constructions Fig. No.

Siliceous Quartzite 1-2

Very hard, acid Minas Gerais churches, Brazil.

Granite/ Gneiss

1 Hard, acid Machu Picchu, Peru. Cuzco cathedral, Peru

2

Sandstone 5-30 Variable durability, acid

Colonial buildings in LA

Soapstone 0.5-5 Soft, basic, acid-resistant

Minas Gerais churches; Statue of Christ, Rio, Brazil.

3, 4

Slate

0.5-5

Basic

Quilmes, Argentina; Tiwanako, Bolivia; Colonial buildings in LA.

5

Limestone Limestone 2-20 Basic Mayan constructions in the Yucatan peninsula, Mexico; colonial buildings, Cartagena, Colombia.

1, 6

Marble 0.5-2 Basic Funerary monuments. 7

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Fig. 2. The Inca site of Machu Picchu, Peru.

Fig. 3. The Church of Bom Jesus, Congonhas, Minas Gerais, Brazil. The unpainted part of the church façade is of

quartzite and soapstone. The statues of the prophets are carved in soapstone.

Fig. 4. Statue of Christ, Corcovado, Rio de Janeiro, Brazil. The concrete statue is covered with a soapstone mosaic.

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Fig. 5. Skulls set into wall at Tiwanaco, Bolivia. Note orange-yellow lichen on left hand side.

Fig. 6. Limestone carving on a Mayan building at Chichen Itza, Mexico.

Fig. 7. Marble tombstone with intense black biofilm in churchyard in Minas Gerais.

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Historic buildings have obviously survived for centuries and it may be suggested that they therefore have an inherent resistance to decay processes. Of course, they are normally subject to renovation and repair over the years. However, environmental conditions have changed recently in such a way as to increase the activities of biofilms on mineral surfaces. The effect of industrialization on weathering has been discussed by Winkler (1976). Layers of organic pollutants may act as nutrients for the growth of heterotrophic microorganisms (bacteria and fungi), thus accelerating both aesthetic and physico-chemical deterioration (May et al., 1993; Saiz-Jimenez, 1995). The adsorbed pollutants include fatty acids and aliphatic and aromatic hydrocarbons (Saiz-Jimenez, 1995; Zanardini et al., 2000), which modify the nature of the stone surface. Increased inputs of sulfur and nitrogen, as acid rain, and trace elements from particulates can also stimulate microbial growth.

Coatings such as plaster and paint also modify the stone surface. Paints and varnishes reduce the ingress of water and can be protective, but they also lead to the retention of water once present under the coating, and this accelerates internal degradation. A similar situation can occur beneath patinas, surface layers of inorganic oxides, whose formation can be induced by microorganisms (Krumbein et al., 1987). Painted surfaces are subject to microbial deterioration, the organic constituents of the paint frequently acting as food for the cells.

Salts of organic acids, produced by microbial cells during their normal metabolic processes, can mobilize cations from within the stone, causing degradation (Petersen et al., 1988, Saiz-Jimenez, 1994). It has been suggested that iron-chelating compounds (siderophores) produced by living cells can induce microfissures in the stone surface (Krumbein & Schönborn-Krumbein, 1987).

The majority of information on biodeterioration of ancient buildings comes from research in Europe, even though the processes are more rapid under tropical and sub-tropical conditions. We report here the microorganisms in biofilms on historic buildings in the Latin American countries of Bolivia, Brazil, Colombia, Equador, Mexico and Peru, and their potential for biodeterioration.

2 EXPERIMENTAL Samples of biofilms were taken from the surfaces of various historic buildings in Bolivia, Brazil, Colombia, Equador, Mexico and Peru, using the non-destructive adhesive tape sampling method of Gaylarde & Gaylarde (1998), and fungi and phototrophic microorganisms (algae and cyanobacteria) were identified by culture and microscopic analysis. Fungi were identified both on algal and fungal media (Shirakawa et al., 2001). Bacteria, actinomycetes and protozoa were noted in cultures on algal media, but were only identified by morphology, where possible. In addition, samples of degraded rock from both natural sites and buildings were taken to study the role of microorganisms in fissures and within the structure of the rock (endoliths).

3 RESULTS AND DISCUSSION The major groups of microorganisms detected in the superficial biofilms are cyanobacteria and fungi. There is no significant difference between similar buildings in different countries, but there is a difference in the major types of microorganisms detected on different materials (Table 3), which has also been reported by other authors (Tomaselli et al., 2000). These organisms are able to survive the continual drying and rehydration occurring on exposed building surfaces. Although some, such as the alga, Trentepohlia, produce specialized survival cells, the major microbial genera detected, Gloeocapsa, Synechocystis, Cladosporium and Aureobasidium, grow in our laboratory cultures from their vegetative forms, collected from the walls on adhesive tape and stored under dry conditions prior to culture. This ability to survive extreme and prolonged desiccation is an essential characteristic of cells which colonize walls exposed to the external environment. Many of the organisms produce pigments for protection against uv and these can cause the staining seen on exposed surfaces of buildings. Algae and cyanobacteria are always intrinsically coloured when active, and generally assume a grey/black coloration when dead. The most prevalent fungi are dark-pigmented types and the actinomycete genus Geodermatophilus is also typically pigmented. Thus the principal microorganisms detected on these historic buildings cause aesthetic deterioration of the surface (discoloration). However, they can also actively degrade the materials.

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Table 3. Main types of organisms detected on the surfaces of historic buildings in Latin America

Group Characteristics of cells detected Most common occurrence*

Fig. No.

Pleurocapsales Single-celled or colonial cyanobacteria, often darkly pigmented

L, S, M 8

Gloeocapsa Single-celled or colonial cyanobacteria, encapsulated, cells and/or capsules often coloured pink, purple or brown

L, P 9

Synechocystis Single-celled or colonial cyanobacteria, sometimes in coloured mucilage

P, S 9

Oscillatoriales Filamentous cyanobacteria, with or without a sheath, generally green or brown

P 10

Scytonemataceae Filamentous cyanobacteria, sheathed, often dark brown

P 11

Nostocaceae Filamentous cyanobacteria, embedded in mucilage, often brown or grey/blue

G, P 12

Actinomycetes, Streptomyces, Nocardia, Geodermatophilus

Filamentous bactéria. Geodermatophilus frequently pink or brown coloured

All 13

Cladosporium Dark pigmented filamentous fungus All 14

Aureobasidium “Black yeast” P

Trentepohlia Filamentous green alga, often orange, brown, or pink in mass

P, G 15

Chlorella, Chlorococcum Coccoid green algae P

*L (limestone), S (soapstone), G (granite), M (mortar), P (painted or otherwise coated) surfaces

Fig. 8. Pleurocapsales group Fig. 9. Gloeocapsa (purple) and Synechocystis genera

Fig. 10 Oscillatoriales group. Fig. 11. Scytonemataceae group

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Fig. 12. Colonies of the cyanobacterial group Nostocaceae, growing endolithically in a granite church in Parati,

Brazil.

Fig. 13. Actinomycetes growing as a white layer on an internal wall at the Mayan site of Uxmal, Mexico.

Fig. 14. The filamentous fungus, Cladosporium. The spore-bearing head is shown here.

Fig. 15. The filamentous alga Trentepohlia, showing brown/red oil droplets inside cells.

Degradation of siliceous minerals. The ability of the microorganisms found on these surfaces to survive desiccation indicates that they produce osmotic protectants, polyols, which partially replace water in the cell cytoplasm. Glycerol has long been known to cause the expansion of micaceous minerals. Glycerol and other polyols, such as glucose and high molecular weight polysaccharides, form complexes by hydrogen bonding in between the laminar polysiloxane crystal planes of micaceous minerals. This causes expansion and mechanical stresses, which may degrade the rock, and ions bound within the structure may become more accessible to chemical attack. The polyols present in high concentrations in desiccation-resistant organisms such as those found on the historic buildings in this study can thus be responsible for weakening of the structure of siliceous materials. These chemicals protect the cells against freezing, desiccation and excess salt. Our studies show that Gloeocapsa, Scytonema, Aureobasidium and Cladosporium from paint will grow on media with up to 20% (w/v) added NaCl. Unpublished observations on samples from mortar collected at a site with severe salting in Europe, showed a much wider range of salt tolerant genera, including slime moulds, protozoa and rotifers. The role of polyols in biodegradation of siliceous materials has not previously been suggested in the literature.

It is commonly stated that siliceous rocks are degraded by biologically produced acids (Strzelczyk, 1981; Petersen et al., 1988). However, Bennett et al. (1988) showed that organic acids, in general, do not increase the dissolution of silica. In the presence only of citrate, salicylate, or oxalate anions, the dissolution increased with pH over the tested pH range of 3 to 7. Anions of α-dicarboxylic acids (e.g. citrate) will form cyclic hydrogen bonded complexes with the superficial hydroxyl groups of quartz. The dissolution of silica will be accelerated by increased hydroxyl ion concentrations, which attack the Si-O-Si linkage and this reaction will almost certainly be favoured by the presence of polyols, which will additionally increase the solubility of these products. Thus polyols and complex organic anions can attack siliceous minerals under alkaline conditions. Silica dissolution under these conditions will also be increased by the formation of covalent siloxanes and hydrogen-bonded complexes with α-hydroxy acids (eg salicylate) and α-phenolic diols (eg humic acids, pyrocatechol), all of which are produced by microbial activity (Iler, 1979).

The siliceous mineral, soapstone, is a soft stone that is very resistant to acid and has been used to construct tanks for the storage of strong mineral acids. Its main component is talc, Mg3Si4O10(OH)2. This stone has been extensively used in the historical monuments of Minas Gerais, Brazil (Fig. 2). It has an alkaline reaction, generally pH 9 or a little higher. Silicon and aluminium are mobilized at pH values above pH 9·5 and phototrophs can increase their immediate environment to above pH 11 by the action of ionic pumps (Miller et al. 1990). The resulting stone degradation can produce catastrophic sloughing of surface layers when the organisms are present within the material as endoliths. This is shown in Fig. 16, where microorganisms growing within the soapstone nfaçade of a church in Ouro Preto, Brazil, have caused spalling of the surface. The principal microorganisms detected in the deeper part the soapstone sample were the cyanobacterial genus Synechococcus and actinomycetesnn.

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Fig. 16. Spalling soapstone, showing green growth of (mainly) cyanobacteria deeper than the whitened spalled layer. The red coloration is patina.

Degradation of carbonates. Limestone may be biodegraded by bacterial, fungal and algal acids (Koestler et al., 1985 Grant, 1982; May et al, 1993) and by mechanical penetration by filamentous fungi and phototrophs (Hoffmann, 1989; Ortega-Calvo et al., 1991). Dark pigmented mitosporic fungi, or “black yeasts”, can also actively penetrate limestone, causing "biopitting" (Sterflinger & Krumbein, 1997).

Hoffmann (1989), in his review of algae in terrestrial habitats, states that cyanobacteria capable of boring into limestone are of the genera Gloeocapsa, Stigonema, Chroococcus, Aphanocapsa and Schizothrix.. All of these genera, apart from Schizothrix, are found on the historic buildings in our study.

The mechanism of boring is unknown. Cyanobacterial cells on limestone can often be seen, in electron micrographs, to be covered with calcareous deposits (Ascaso et al., 1998; Ortega-Morales et al., 2000), which suggests the migration of calcium from neighboring sites. Phototrophs deposit CaCO3 in the light and solubilize it at night because of changing bicarbonate concentrations. This process has been well studied in the coccoid cyanobacterium Synechococcus GL24. These spherical cells possess on their external surface a so-called S-layer, which binds calcium ions at negatively charged sites (Schultze et al., 1994). The bound calcium complexes with carbonate ions at pH values above 8.3. Even if the pH of the stone surface is not so high, it is elevated to these levels by phototrophic activity, whereby OH- ions are released and concentrated around the cells (Miller et al., 1990), raising the local pH. Cells of Synechococcus can become encrusted with calcite within 8h in a suitable environment and must continually shed patches of mineralized S-layer to remain viable (Douglas & Beveridge, 1998). Mobilization of calcium ions by such metabolic activity and ion transport, in addition to the trapping of released particles of calcite, either of biotic or abiotic origen, in the gelatinous cyanobacterial sheath (Pentecost, 1988), is an important mechanism of limestone degradation by cyanobacteria and algae.

4 CONCLUSIONS Pigmented microorganisms, bacteria, fungi and algae, cause discoloration on the surface of buildings of historic and cultural importance. In addition, they can directly cause degradation of the materials through various metabolic activities. This biodeterioration and biodegradation is not prevented by surface coatings on stone buildings, since these coatings, themselves, are subject to microbial growth. Although hard, smooth and less porous surfaces, such as basalt or varnished stone, are more resistant to microbial colonization, they can still be attacked by many microorganisms. The resultant biofilms should be removed regularly, using non-abrasive and environmentally safe methods, to reduce the impact of microbial activities.

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