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Bioremediation of weathered-building stone surfaces
Review
TRENDS in Biotechnology
Vol.24 No.6 June 2006
Bioremediation of weathered-building stone surfaces Alison Webster and Eric May School of Biological Sciences, University of Portsmouth, Portsmouth, Hampshire, PO1 2DY, UK
Atmospheric pollution and weathering of stone surfaces in urban historic buildings frequently results in disfigurement or damage by salt crust formation (often gypsum), presenting opportunities for bioremediation using microorganisms. Conventional techniques for the removal of these salt crusts from stone have several disadvantages: they can cause colour changes; adversely affect the movement of salts within the stone structure; or remove excessive amounts of the original surface. Although microorganisms are commonly associated with detrimental effects to the integrity of stone structures, there is growing evidence that they can be used to treat this type of stone deterioration in objects of historical and cultural significance. In particular, the ability and potential of different microorganisms to either remove sulfate crusts or form sacrificial layers of calcite that consolidate mineral surfaces have been demonstrated. Current research suggests that bioremediation has the potential to offer an additional technology to conservators working to restore stone surfaces in heritage buildings.
damage to stone [9–11]. Stone is hydrophilic, and will take up water from the ground and adjoining stone. Soluble salts from the soil, the atmosphere and applications on the surface can dissolve in this aqueous environment and move through the pores. Highly soluble salts are usually deposited on the surface, and can be brushed off; however, less soluble salts might expand below surface level, ultimately causing the loss of the outer layers [12,13]. Accumulation of sulfates, many derived from the oxidation of sulfur dioxide, is of particular concern. Those techniques that attempt to remove salts from heritage stone artefacts by washing with water are either not practicable or accelerate degradation [14]. Nitrates, which can originate from the numerous oxides of nitrogen present in the atmosphere (N2O, NO, N2O3, NO2, N2O5), can also accumulate but because they have a high solubility they migrate from the surface or are washed away by rain [15]. Thus, unlike sulfates, nitrate accumulation is not a surface phenomenon and has not been the subject of extensive study.
Introduction The term bioremediation covers a range of processes that use microorganisms to return contaminated environments to their original condition. The use of microorganisms or their enzymes to deal with contaminated soils, oil spills or chemical waste are well-developed biotechnologies [1,2] but the application of bioremediation to ameliorate the effects of stone deterioration is less well known. Deterioration of building stone begins from the moment it is quarried due to natural weathering processes [3]. Other factors, sometimes acting synergistically, including crystallization of soluble salts, pollution and biological colonisation can accelerate natural deterioration [4–8]. Whatever the cause of stone deterioration, many buildings require remedial measures to stabilize the surface layer and prevent further loss from external sources. This review offers an insight into how biotechnology research has addressed the needs of conservators working with building stone and considers how far bacterially mediated bioremediation can be used in practice.
Black sulfate crusts Many of the additional factors that accelerate deterioration of stone are still being definitively characterised, and much work has been carried out to highlight the role of biological organisms in the blackening of stone [16,17]. It is, however, the effects of anthropogenic sources of pollution on building stone that are arguably the single most important factor in the production of black discoloration [18]. The burning of fossil fuels has led to an increase in the concentrations of acid gases in the atmosphere and, of these, perhaps the most important is sulfur dioxide. When dissolved in water [19,20], sulphur dioxide forms sulphurous acid, which is oxidised to sulfuric acid; this, in turn, reacts with calcium carbonate to form calcium sulfate, the mineralized form of which is known as gypsum [21]. The formation of gypsum leads to the creation of cavities below the surface because of the migration of calcium ions to the surface [22]. Thus, when the soluble gypsum is washed away it takes with it some of the stone itself, initially causing loss of surface detail but eventually leading to a loss of structural integrity. On the surface of the stone, particulate matter from the atmosphere can combine with gypsum to leave unsightly black crusts [23,24]. Carbonaceous particles were thought to be the most significant element in black crusts but recent work has shown that they also contain a complex mixture of aliphatic and aromatic carboxylic acids and
Stone and soluble salts Internal pressures created by crystallization, hydration and thermal expansion of salts are a significant cause of Corresponding author: May, E. ([email protected]). Available online 2 May 2006
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polycyclic aromatic hydrocarbons [25]. Sabbioni et al. [26] concluded that the oxalate found in these crusts probably originated from a combination of microbial metabolism and protective treatments; formate and acetate anions found in the black crust were believed to be from atmospheric pollutants. Furthermore, Schiavon et al. noted that the types of pollutants found in urban building stones are changing to reflect the atmospheric pollutants of the time [27]. Bioremediation of black sulfated crusts Attempts to restore stone surfaces by removal of black crusts and salts through mechanical stone cleaning has begun to be called into question by some conservators as the effects of past cleaning regimes become more evident [28]. It is clear that such cleaning can result in several types of damage, some of which is immediately apparent (e.g. loss of surface), whereas in other cases the damage might not become apparent for several years, for example, where a single dominant species of microorganism replaces complex established microbiota removed in the cleaning process [29,30]. Indeed, some conservators believe certain surface deterioration should not be removed. For example, patinas (surface layers developed over extended periods by biological and material-related factors) removed from the Parthenon were associated with the best-preserved surfaces and it was therefore recommended that these should remain intact [31]. Thus, the removal of black crusts is problematic for conservators because conventional cleaning techniques can potentially remove a portion of the underlying stone [32]. Skoulikidis and Beloyannis reported that gypsum could be converted back to calcite using carbonate anions in aqueous solution [33]. They found that the gypsum layer was consolidated by the new calcite, which showed similar behaviour to the underlying marble. Although no other authors reported success using purely chemical reactions, the use of microorganisms, a relatively recent technique, has been successful in removing sulfate from black gypsum crusts. Sulfate-reducing bacteria are able to 2C dissociate gypsum into Ca2C and SO2C 4 ions, and the SO4 ions are then reduced by the bacteria, whereas the Ca2C ions react with carbon dioxide to form new calcite [32]: 6CaSO4 C 4H2 O C 6CO2 / 6CaCO3 C 4H2 S C 2S C 11O2 : In 1970, Moncreiff and Hempel [34] described the use of a ‘biological pack’ and the role of microorganisms in a poultice. The first successful application of the anaerobic sulfate reducer Desulfovibrio desulfuricans was reported by Atlas et al. [35] and Gauri and Chowdhury [36]. Heselmeyer et al. applied Desulfovibrio vulgaris to gypsum crusts, which brought about the conversion to calcite [14]. D. desulfuricans was again used by Gauri et al. to remove sulfates from the black crust on marble [37], and Kouzeli, also working with marble, reported good results compared with chemically based pastes [38]. Saiz-Jimenez presented evidence that demonstrated microorganisms removed some of the most abundant components of black crusts, such as gypsum and polycyclic aromatic hydrocarbons [39]; however, he did not consider www.sciencedirect.com
Figure 1. Examples of biorestoration. Left: Marble balcony support arm from a building in Athens undergoing restoration showing black sulfated crusts. Right: detail of a balcony scroll before (top) and after (bottom) application. Removal of black crust is apparent after a single application of sulfate-reducing bacteria, suspended in gel, after 48 hours. Further removal can be achieved with repeat applications and can be tailored to the needs of the conservator.
that microorganisms would be of use in the bioremediation of buildings because of the practical difficulties imposed by factors such as the size of the buildings and the time required. Ranalli et al. [40,15,41], unlike other researchers, have not reported the deposition of calcite but, using D. desulfuricans and D. vulgaris, they demonstrated the successful removal of black crusts from marble. A single application of sulfate-reducing bacteria to an urban marble structure illustrates this ability (Figure 1). Consolidation of stone surfaces The desire to protect and consolidate stone surfaces has a long history, with evidence for Roman use of pastes applied to recently sculpted stone [42]. Traditional methods such as shelter coatings are made from slaked lime (calcium hydroxide), which combines with carbon dioxide in the atmosphere and hardens to form calcium carbonate in a process known as carbonation. The formation of calcium carbonate crystals in the form of calcite is not an immediate process and can take up to 80 days when applied to wall paintings [43]. External shelter coatings, such as limewash, last between 10 and 15 years but because they are subject to the same deterioration processes as the underlying stone, they are eventually washed away and only provide relatively short-term protection [44]. Another method that works with the underlying stone is the generation of a calcium oxalate patina. Surface patinas can be formed, naturally, during time by oxidation of calcite with oxalic acid, and some authors consider a biological origin the most probable cause, for example, those observed at Tarragona Cathedral, Spain [45]; other patinas might be anthropogenic in origin, the result of protective treatments applied in the past [46]. Cezar reported on work that has been carried out in the laboratory to generate calcium oxalate layers, chemically, in a matter of hours rather than years [44]. Biomineralization An alternative to the chemical generation of calcium carbonate is the exploitation of a common phenomenon in living organisms – biomineralization. This activity is
Review
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Figure 2. Crystal production under laboratory conditions. Left: crystal formation by two different bacterial cultures growing on B4 solid medium [48]. Top: unidentified bacteria isolated from a karstic stream. Bottom: Sphingomonas paucimobilis. Crystal formation occurs within 10 hours of inoculation (magnification!400). Right panel is a scanning electron micrograph showing a layer of calcified Pseudomonas putida cells on Portland limestone, following the contours of the underlying substrate. Magnification!5000, BarZ1 mm.
widespread across many phyla, and molecular studies of bone and shell suggest that there might be a common genetic ancestry [47]. Biomineralization by bacteria (Figure 2) has provoked controversy, with some authors believing that crystal production is a purely chemical by-product, whereas others assert that microorganisms are actively involved in the process. Ehrlich [49] defined microbial mineral formation as either ‘active’, involving enzymes or metabolic products, or ‘passive’, where even dead cells can produce minerals. Rivadeneyra et al. propose that the formation of calcium carbonate crystals in the presence of Nesterenkonia halobia involves both biological and inorganic processes [50]. Given that organisms are in contact with the available precursors required for crystal formation, it is perhaps unsurprising that new mineral material is produced on stone, and this has, indeed, been observed in cyanobacteria following invasion of stone and lichens [51,52]. Urzi et al. isolated microorganisms from stone surfaces and found that the majority precipitate CaCO3 in the form of calcite [53]; furthermore, most of the common bacteria associated with building stones can also induce precipitation in the laboratory. Such examples demonstrate the complex inter-relationship between biological organisms and minerals, leading to elements of both destruction and consolidation of the substratum. Biomineralization of stone Although biomineralization has been observed for many years, the potential for its use in stone consolidation has only been explored relatively recently. In 1990, Adolphe and others applied for a European patent for the generation of calcite through the action of bacteria. Orial et al. [54,55] also examined the formation of sacrificial layers by bacteria and considered that it offered a promising avenue for treatment of historic buildings. Le Metayer-Levrel et al. used several different strains of biocalcifying bacteria to promote successful bacterial carbonatogenesis on the surface of limestone buildings, statuary and monuments [56]. A variety of uses have been found for biocalcifying bacteria, as seen in the work of Bang et al. who used Bacillus pasteurii immobilised in www.sciencedirect.com
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polyurethane to fill cracks in concrete [57] and Ramachandran et al. who found that an increase in compressive strength and stiffness can be achieved by combining bacteria with sand in cracks [58]. Rodriguez-Navarro et al. also proposed the use of Myxococcus xanthus in stone conservation and observed newly formed carbonate, which created a cement that adhered strongly to the substratum: the bacteria induced carbonate cementation to a depth of O500 mm and no plugging or blocking of pores was observed [59]. This newly formed carbonate was more resistant to mechanical stress in the form of sonication, possibly because of the incorporation of organic molecules produced by bacterial metabolism into the crystals. This agrees with the work of Morse, who discovered that bacterially induced calcite was less soluble that inorganically produced calcite [60]. Castanier et al. reported the generation of bioconsolidating cement a few micrometres thick, with significant carbonate production occurring within 5–10 days [61]. Limited EPS (extracellular polymeric substances) formation was observed when using buffered media M-3 but small quantities were formed when growing the bacteria using unbuffered M-3, indicating the importance of the choice of pH and media components. The application of microorganisms and a suitable growing media directly to stone surfaces has several potential problems, including the formation of EPS, blocking of pores and promotion of microbial growth on excess media. To avoid some of these problems, Tiano et al. examined carbonatogenesis using organic matrix macromolecules extracted from seashells, a procedure that unfortunately proved complex and produced a low yield of usable product [62]. Further work compared the effects of Mytilus californianus with Ca(OH)2 and CaCl2 in terms of porosity, capillary water absorption and superficial cohesion on Pietra di Lecce and Pietra d’Angera (bioclastic limestone): M. californianus gave the best results [63]. In 1999, Tiano et al. examined methods of evaluating biologically mediated precipitation of calcite using pore dimension, stone strength and colour [64]. Using Pietra di Lecce with Micrococcus sp. and Bacillus subtilis, calcite was identified using X-ray diffraction (XRD) and Fourier transform–infrared spectroscopy (FT-IR) He found there had been a decrease in stone porosity but considered that half of this was probably due to physical obstruction of pores rather than newly precipitated calcite. A side effect of the treatment was the formation of stained patches due to the growth of airborne contaminants exploiting the presence of organic nutrients in the media used to grow the biocalcifying bacteria. Concerns regarding contamination of stone during induced biomineralization led to attempts to define the genetic mechanism as a possible alternative to the direct application of live cells [65]. It is now understood that application of a physical barrier on the stone surface will hinder the movement of salts, which can then build up, leading initially to unsightly discolouration and ultimately to physical damage [66]. Even coatings that permit evaporation can cause problems of salt accumulation and crystallization and, therefore, a protective coating must be sympathetic to the nature of the stone itself. The production of
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a calcium carbonate layer generated by bacteria (Figure 2) might offer a solution to this dilemma because the layer would not block the natural pore structure, thus permitting free passage of soluble salts through the stone. The life of sacrificial layers generated by microorganisms is unclear but because of accelerated aging tests, Le Metayer-Levrel suggests that protection acquired by biomineralization tends to increase with age by offering longer-term resistance to the weathering caused by growth of acid-producing microbial populations [55]. Current work and future prospects Bioremediation is less harsh than the use of environmentally toxic chemicals or aggressive mechanical procedures, which are considered to be destructive methods. Crust removal by microorganisms takes place in a natural way because these microorganisms have an active role in the environment, where they contribute to the closure of biogeochemical cycles or stabilization of dynamic equilibria. However, research issues that have and will continue to be addressed are the effectiveness of these procedures, in addition to appropriate risk analyses, to provide conservators with confidence in the technology. Thus, technology transfer from the scientific community can only be achieved by direct engagement of heritage endusers across national boundaries. Recent research has explored the factors that influence biological precipitation of calcium carbonate. Studies in Spain, France, USA, Italy and the UK have shown that consolidation of stones by biocalcifying bacteria can be controlled by application of safe bacteria that pose little threat to the heritage object [50,56,57,65,67]. Acceptance and satisfactory use of these technologies in conservation practice requires adequate knowledge of the risk factors to the heritage object in addition to conservators handling the active components. There have been concerns about the long-term effects of the applied bacteria and their nutrient media. Such issues are best addressed in systematic studies involving collaboration among scientists and end-users active in conservation practice. Practical application of bioremedial technologies has recently progressed, through the work of two projects funded by the European Community, which also usefully illustrate the differences of approach that have been adopted to evaluate the potential of bioremediation for conservation work: BIOREINFORCE (http://www.ub.es/ rpat/bioreinforce/bioreinforce.htm); and BIOBRUSH (http://www.biobrush.org). The BIOREINFORCE partnership has successfully demonstrated that dead cells from active biocalcifying strains showed a much higher and/or faster production of CaCO3 crystals than less active strains. By elucidating the genetic expression of crystal formation in bacteria, the project aimed to produce bioderived, low-cost, renewable macromolecules that will induce calcification on stones without using living bacterial cells [68]. The novel approach of the BIOBRUSH project was to use live but low-hazard bacteria to link the mineralization processes (that remove salt crusts) to biomineralization (that can consolidate the stone). Bacteria were applied directly to stone surfaces using techniques that minimized the risk to the environment www.sciencedirect.com
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and conservators applying the treatment. Work at the Universities of Milan and Molise, respectively, have demonstrated that multiple short-term applications of aerotolerant sulfate-reducing bacteria, within an appropriate delivery system, can be successful in removing black crusts from marble, both in the laboratory and in situ on buildings [69]. Results suggest that the bioremediation is at least as good as existing methods. Work with biocalcifying bacteria that were isolated from the environment has shown that deposition of a calcite layer can be achieved without significant reduction in porosity or growth of contaminating microorganisms [67]. This approach uses environmental isolates and controlled release of nutrients to minimize an adverse stimulation of microbial growth. Concluding remarks The controlled use of microorganisms as agents of bioremediation offers new approaches for conservators to help preserve, protect and restore building stone. Such techniques are intended to supplement rather than replace existing conservation technologies, which can often be ineffective or toxic to end-users or the environment. In the past 10 years, research has explored the constraints of applying bacteria to stone to remove salt crusts and consolidate the damaged pore structure. Suitable organisms are now known, and the environmental factors have been identified; however, the risks posed by aesthetic and mineral changes are still being addressed. The challenge for the immediate future is to translate a wide range of promising results into the practical technology that has been achieved in other fields of biotechnology. Although the technology is still in its infancy and, therefore, not readily available, the results so far indicate that it promises to offer a viable alternative to those working to preserve our cultural heritage. References 1 Atlas, R.M. (1995) Bioremediation. Chem. Eng. News 73, 32–42 2 Jo¨rdening, H-J. and Winter, J. (2005) Environmental Biotechnology: Concepts and Applications, Wiley-VCH, Weinheim 3 Gauri, K.L. and Bandyopadhyay, J.K. (1999) Carbonate Stone: Chemical Behaviour, Durability, and Conservation, John Wiley & Sons, New York 4 Leysen, L. et al. (1987) A study of the weathering of an historic building. Anal. Chim. Acta 195, 247–255 5 Doornkamp, J.C. and Ibrahim, H.A.M. (1990) Salt weathering. Prog. Phys. Geogr. 14, 335–348 6 Warscheid, T. and Braams, J. (2000) Biodeterioration of stone: a review. International Biodeterioration & Biodegradation 46, 343–368 7 Gaylarde, C. et al. (2003) Microbial impact on building materials: an overview. Materials and Structures 36, 342–352 8 McNamara, C.J. and Mitchell, R. (2005) Microbial deterioration of historic stone. Frontiers in Ecology and the Environment 3, 445–451 9 Rodriguez-Navarro, C. et al. (2000) How does sodium sulfate crystallize? Implications for the decay and testing of building materials. Cement Concrete Res. 30, 1527–1534 10 Rodriguez-Navarro, C. et al. (2002) Effects of ferrocyanide ions on NaCl crystallization in porous stone. J. Cryst. Growth 243, 503–516 11 Papida, S. et al. (2000) Enhancement of physical weathering of building stones by microbial populations. Int. Biodeterior. Biodegradation 46, 305–317 12 Lewin, S. (1989) The susceptibility of calcareous stones to salt decay. In The Conservation of Monuments in the Mediterranean Basin (Zezza, F., ed.), pp. 59–64, Grafo, Brescia
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Bioremediation of weathered-building stone surfaces Alison Webster and Eric May School of Biological Sciences, University of Portsmouth, Portsmouth, Hampshire, PO1 2DY, UK
Atmospheric pollution and weathering of stone surfaces in urban historic buildings frequently results in disfigurement or damage by salt crust formation (often gypsum), presenting opportunities for bioremediation using microorganisms. Conventional techniques for the removal of these salt crusts from stone have several disadvantages: they can cause colour changes; adversely affect the movement of salts within the stone structure; or remove excessive amounts of the original surface. Although microorganisms are commonly associated with detrimental effects to the integrity of stone structures, there is growing evidence that they can be used to treat this type of stone deterioration in objects of historical and cultural significance. In particular, the ability and potential of different microorganisms to either remove sulfate crusts or form sacrificial layers of calcite that consolidate mineral surfaces have been demonstrated. Current research suggests that bioremediation has the potential to offer an additional technology to conservators working to restore stone surfaces in heritage buildings.
damage to stone [9–11]. Stone is hydrophilic, and will take up water from the ground and adjoining stone. Soluble salts from the soil, the atmosphere and applications on the surface can dissolve in this aqueous environment and move through the pores. Highly soluble salts are usually deposited on the surface, and can be brushed off; however, less soluble salts might expand below surface level, ultimately causing the loss of the outer layers [12,13]. Accumulation of sulfates, many derived from the oxidation of sulfur dioxide, is of particular concern. Those techniques that attempt to remove salts from heritage stone artefacts by washing with water are either not practicable or accelerate degradation [14]. Nitrates, which can originate from the numerous oxides of nitrogen present in the atmosphere (N2O, NO, N2O3, NO2, N2O5), can also accumulate but because they have a high solubility they migrate from the surface or are washed away by rain [15]. Thus, unlike sulfates, nitrate accumulation is not a surface phenomenon and has not been the subject of extensive study.
Introduction The term bioremediation covers a range of processes that use microorganisms to return contaminated environments to their original condition. The use of microorganisms or their enzymes to deal with contaminated soils, oil spills or chemical waste are well-developed biotechnologies [1,2] but the application of bioremediation to ameliorate the effects of stone deterioration is less well known. Deterioration of building stone begins from the moment it is quarried due to natural weathering processes [3]. Other factors, sometimes acting synergistically, including crystallization of soluble salts, pollution and biological colonisation can accelerate natural deterioration [4–8]. Whatever the cause of stone deterioration, many buildings require remedial measures to stabilize the surface layer and prevent further loss from external sources. This review offers an insight into how biotechnology research has addressed the needs of conservators working with building stone and considers how far bacterially mediated bioremediation can be used in practice.
Black sulfate crusts Many of the additional factors that accelerate deterioration of stone are still being definitively characterised, and much work has been carried out to highlight the role of biological organisms in the blackening of stone [16,17]. It is, however, the effects of anthropogenic sources of pollution on building stone that are arguably the single most important factor in the production of black discoloration [18]. The burning of fossil fuels has led to an increase in the concentrations of acid gases in the atmosphere and, of these, perhaps the most important is sulfur dioxide. When dissolved in water [19,20], sulphur dioxide forms sulphurous acid, which is oxidised to sulfuric acid; this, in turn, reacts with calcium carbonate to form calcium sulfate, the mineralized form of which is known as gypsum [21]. The formation of gypsum leads to the creation of cavities below the surface because of the migration of calcium ions to the surface [22]. Thus, when the soluble gypsum is washed away it takes with it some of the stone itself, initially causing loss of surface detail but eventually leading to a loss of structural integrity. On the surface of the stone, particulate matter from the atmosphere can combine with gypsum to leave unsightly black crusts [23,24]. Carbonaceous particles were thought to be the most significant element in black crusts but recent work has shown that they also contain a complex mixture of aliphatic and aromatic carboxylic acids and
Stone and soluble salts Internal pressures created by crystallization, hydration and thermal expansion of salts are a significant cause of Corresponding author: May, E. ([email protected]). Available online 2 May 2006
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polycyclic aromatic hydrocarbons [25]. Sabbioni et al. [26] concluded that the oxalate found in these crusts probably originated from a combination of microbial metabolism and protective treatments; formate and acetate anions found in the black crust were believed to be from atmospheric pollutants. Furthermore, Schiavon et al. noted that the types of pollutants found in urban building stones are changing to reflect the atmospheric pollutants of the time [27]. Bioremediation of black sulfated crusts Attempts to restore stone surfaces by removal of black crusts and salts through mechanical stone cleaning has begun to be called into question by some conservators as the effects of past cleaning regimes become more evident [28]. It is clear that such cleaning can result in several types of damage, some of which is immediately apparent (e.g. loss of surface), whereas in other cases the damage might not become apparent for several years, for example, where a single dominant species of microorganism replaces complex established microbiota removed in the cleaning process [29,30]. Indeed, some conservators believe certain surface deterioration should not be removed. For example, patinas (surface layers developed over extended periods by biological and material-related factors) removed from the Parthenon were associated with the best-preserved surfaces and it was therefore recommended that these should remain intact [31]. Thus, the removal of black crusts is problematic for conservators because conventional cleaning techniques can potentially remove a portion of the underlying stone [32]. Skoulikidis and Beloyannis reported that gypsum could be converted back to calcite using carbonate anions in aqueous solution [33]. They found that the gypsum layer was consolidated by the new calcite, which showed similar behaviour to the underlying marble. Although no other authors reported success using purely chemical reactions, the use of microorganisms, a relatively recent technique, has been successful in removing sulfate from black gypsum crusts. Sulfate-reducing bacteria are able to 2C dissociate gypsum into Ca2C and SO2C 4 ions, and the SO4 ions are then reduced by the bacteria, whereas the Ca2C ions react with carbon dioxide to form new calcite [32]: 6CaSO4 C 4H2 O C 6CO2 / 6CaCO3 C 4H2 S C 2S C 11O2 : In 1970, Moncreiff and Hempel [34] described the use of a ‘biological pack’ and the role of microorganisms in a poultice. The first successful application of the anaerobic sulfate reducer Desulfovibrio desulfuricans was reported by Atlas et al. [35] and Gauri and Chowdhury [36]. Heselmeyer et al. applied Desulfovibrio vulgaris to gypsum crusts, which brought about the conversion to calcite [14]. D. desulfuricans was again used by Gauri et al. to remove sulfates from the black crust on marble [37], and Kouzeli, also working with marble, reported good results compared with chemically based pastes [38]. Saiz-Jimenez presented evidence that demonstrated microorganisms removed some of the most abundant components of black crusts, such as gypsum and polycyclic aromatic hydrocarbons [39]; however, he did not consider www.sciencedirect.com
Figure 1. Examples of biorestoration. Left: Marble balcony support arm from a building in Athens undergoing restoration showing black sulfated crusts. Right: detail of a balcony scroll before (top) and after (bottom) application. Removal of black crust is apparent after a single application of sulfate-reducing bacteria, suspended in gel, after 48 hours. Further removal can be achieved with repeat applications and can be tailored to the needs of the conservator.
that microorganisms would be of use in the bioremediation of buildings because of the practical difficulties imposed by factors such as the size of the buildings and the time required. Ranalli et al. [40,15,41], unlike other researchers, have not reported the deposition of calcite but, using D. desulfuricans and D. vulgaris, they demonstrated the successful removal of black crusts from marble. A single application of sulfate-reducing bacteria to an urban marble structure illustrates this ability (Figure 1). Consolidation of stone surfaces The desire to protect and consolidate stone surfaces has a long history, with evidence for Roman use of pastes applied to recently sculpted stone [42]. Traditional methods such as shelter coatings are made from slaked lime (calcium hydroxide), which combines with carbon dioxide in the atmosphere and hardens to form calcium carbonate in a process known as carbonation. The formation of calcium carbonate crystals in the form of calcite is not an immediate process and can take up to 80 days when applied to wall paintings [43]. External shelter coatings, such as limewash, last between 10 and 15 years but because they are subject to the same deterioration processes as the underlying stone, they are eventually washed away and only provide relatively short-term protection [44]. Another method that works with the underlying stone is the generation of a calcium oxalate patina. Surface patinas can be formed, naturally, during time by oxidation of calcite with oxalic acid, and some authors consider a biological origin the most probable cause, for example, those observed at Tarragona Cathedral, Spain [45]; other patinas might be anthropogenic in origin, the result of protective treatments applied in the past [46]. Cezar reported on work that has been carried out in the laboratory to generate calcium oxalate layers, chemically, in a matter of hours rather than years [44]. Biomineralization An alternative to the chemical generation of calcium carbonate is the exploitation of a common phenomenon in living organisms – biomineralization. This activity is
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Figure 2. Crystal production under laboratory conditions. Left: crystal formation by two different bacterial cultures growing on B4 solid medium [48]. Top: unidentified bacteria isolated from a karstic stream. Bottom: Sphingomonas paucimobilis. Crystal formation occurs within 10 hours of inoculation (magnification!400). Right panel is a scanning electron micrograph showing a layer of calcified Pseudomonas putida cells on Portland limestone, following the contours of the underlying substrate. Magnification!5000, BarZ1 mm.
widespread across many phyla, and molecular studies of bone and shell suggest that there might be a common genetic ancestry [47]. Biomineralization by bacteria (Figure 2) has provoked controversy, with some authors believing that crystal production is a purely chemical by-product, whereas others assert that microorganisms are actively involved in the process. Ehrlich [49] defined microbial mineral formation as either ‘active’, involving enzymes or metabolic products, or ‘passive’, where even dead cells can produce minerals. Rivadeneyra et al. propose that the formation of calcium carbonate crystals in the presence of Nesterenkonia halobia involves both biological and inorganic processes [50]. Given that organisms are in contact with the available precursors required for crystal formation, it is perhaps unsurprising that new mineral material is produced on stone, and this has, indeed, been observed in cyanobacteria following invasion of stone and lichens [51,52]. Urzi et al. isolated microorganisms from stone surfaces and found that the majority precipitate CaCO3 in the form of calcite [53]; furthermore, most of the common bacteria associated with building stones can also induce precipitation in the laboratory. Such examples demonstrate the complex inter-relationship between biological organisms and minerals, leading to elements of both destruction and consolidation of the substratum. Biomineralization of stone Although biomineralization has been observed for many years, the potential for its use in stone consolidation has only been explored relatively recently. In 1990, Adolphe and others applied for a European patent for the generation of calcite through the action of bacteria. Orial et al. [54,55] also examined the formation of sacrificial layers by bacteria and considered that it offered a promising avenue for treatment of historic buildings. Le Metayer-Levrel et al. used several different strains of biocalcifying bacteria to promote successful bacterial carbonatogenesis on the surface of limestone buildings, statuary and monuments [56]. A variety of uses have been found for biocalcifying bacteria, as seen in the work of Bang et al. who used Bacillus pasteurii immobilised in www.sciencedirect.com
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polyurethane to fill cracks in concrete [57] and Ramachandran et al. who found that an increase in compressive strength and stiffness can be achieved by combining bacteria with sand in cracks [58]. Rodriguez-Navarro et al. also proposed the use of Myxococcus xanthus in stone conservation and observed newly formed carbonate, which created a cement that adhered strongly to the substratum: the bacteria induced carbonate cementation to a depth of O500 mm and no plugging or blocking of pores was observed [59]. This newly formed carbonate was more resistant to mechanical stress in the form of sonication, possibly because of the incorporation of organic molecules produced by bacterial metabolism into the crystals. This agrees with the work of Morse, who discovered that bacterially induced calcite was less soluble that inorganically produced calcite [60]. Castanier et al. reported the generation of bioconsolidating cement a few micrometres thick, with significant carbonate production occurring within 5–10 days [61]. Limited EPS (extracellular polymeric substances) formation was observed when using buffered media M-3 but small quantities were formed when growing the bacteria using unbuffered M-3, indicating the importance of the choice of pH and media components. The application of microorganisms and a suitable growing media directly to stone surfaces has several potential problems, including the formation of EPS, blocking of pores and promotion of microbial growth on excess media. To avoid some of these problems, Tiano et al. examined carbonatogenesis using organic matrix macromolecules extracted from seashells, a procedure that unfortunately proved complex and produced a low yield of usable product [62]. Further work compared the effects of Mytilus californianus with Ca(OH)2 and CaCl2 in terms of porosity, capillary water absorption and superficial cohesion on Pietra di Lecce and Pietra d’Angera (bioclastic limestone): M. californianus gave the best results [63]. In 1999, Tiano et al. examined methods of evaluating biologically mediated precipitation of calcite using pore dimension, stone strength and colour [64]. Using Pietra di Lecce with Micrococcus sp. and Bacillus subtilis, calcite was identified using X-ray diffraction (XRD) and Fourier transform–infrared spectroscopy (FT-IR) He found there had been a decrease in stone porosity but considered that half of this was probably due to physical obstruction of pores rather than newly precipitated calcite. A side effect of the treatment was the formation of stained patches due to the growth of airborne contaminants exploiting the presence of organic nutrients in the media used to grow the biocalcifying bacteria. Concerns regarding contamination of stone during induced biomineralization led to attempts to define the genetic mechanism as a possible alternative to the direct application of live cells [65]. It is now understood that application of a physical barrier on the stone surface will hinder the movement of salts, which can then build up, leading initially to unsightly discolouration and ultimately to physical damage [66]. Even coatings that permit evaporation can cause problems of salt accumulation and crystallization and, therefore, a protective coating must be sympathetic to the nature of the stone itself. The production of
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a calcium carbonate layer generated by bacteria (Figure 2) might offer a solution to this dilemma because the layer would not block the natural pore structure, thus permitting free passage of soluble salts through the stone. The life of sacrificial layers generated by microorganisms is unclear but because of accelerated aging tests, Le Metayer-Levrel suggests that protection acquired by biomineralization tends to increase with age by offering longer-term resistance to the weathering caused by growth of acid-producing microbial populations [55]. Current work and future prospects Bioremediation is less harsh than the use of environmentally toxic chemicals or aggressive mechanical procedures, which are considered to be destructive methods. Crust removal by microorganisms takes place in a natural way because these microorganisms have an active role in the environment, where they contribute to the closure of biogeochemical cycles or stabilization of dynamic equilibria. However, research issues that have and will continue to be addressed are the effectiveness of these procedures, in addition to appropriate risk analyses, to provide conservators with confidence in the technology. Thus, technology transfer from the scientific community can only be achieved by direct engagement of heritage endusers across national boundaries. Recent research has explored the factors that influence biological precipitation of calcium carbonate. Studies in Spain, France, USA, Italy and the UK have shown that consolidation of stones by biocalcifying bacteria can be controlled by application of safe bacteria that pose little threat to the heritage object [50,56,57,65,67]. Acceptance and satisfactory use of these technologies in conservation practice requires adequate knowledge of the risk factors to the heritage object in addition to conservators handling the active components. There have been concerns about the long-term effects of the applied bacteria and their nutrient media. Such issues are best addressed in systematic studies involving collaboration among scientists and end-users active in conservation practice. Practical application of bioremedial technologies has recently progressed, through the work of two projects funded by the European Community, which also usefully illustrate the differences of approach that have been adopted to evaluate the potential of bioremediation for conservation work: BIOREINFORCE (http://www.ub.es/ rpat/bioreinforce/bioreinforce.htm); and BIOBRUSH (http://www.biobrush.org). The BIOREINFORCE partnership has successfully demonstrated that dead cells from active biocalcifying strains showed a much higher and/or faster production of CaCO3 crystals than less active strains. By elucidating the genetic expression of crystal formation in bacteria, the project aimed to produce bioderived, low-cost, renewable macromolecules that will induce calcification on stones without using living bacterial cells [68]. The novel approach of the BIOBRUSH project was to use live but low-hazard bacteria to link the mineralization processes (that remove salt crusts) to biomineralization (that can consolidate the stone). Bacteria were applied directly to stone surfaces using techniques that minimized the risk to the environment www.sciencedirect.com
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and conservators applying the treatment. Work at the Universities of Milan and Molise, respectively, have demonstrated that multiple short-term applications of aerotolerant sulfate-reducing bacteria, within an appropriate delivery system, can be successful in removing black crusts from marble, both in the laboratory and in situ on buildings [69]. Results suggest that the bioremediation is at least as good as existing methods. Work with biocalcifying bacteria that were isolated from the environment has shown that deposition of a calcite layer can be achieved without significant reduction in porosity or growth of contaminating microorganisms [67]. This approach uses environmental isolates and controlled release of nutrients to minimize an adverse stimulation of microbial growth. Concluding remarks The controlled use of microorganisms as agents of bioremediation offers new approaches for conservators to help preserve, protect and restore building stone. Such techniques are intended to supplement rather than replace existing conservation technologies, which can often be ineffective or toxic to end-users or the environment. In the past 10 years, research has explored the constraints of applying bacteria to stone to remove salt crusts and consolidate the damaged pore structure. Suitable organisms are now known, and the environmental factors have been identified; however, the risks posed by aesthetic and mineral changes are still being addressed. The challenge for the immediate future is to translate a wide range of promising results into the practical technology that has been achieved in other fields of biotechnology. Although the technology is still in its infancy and, therefore, not readily available, the results so far indicate that it promises to offer a viable alternative to those working to preserve our cultural heritage. References 1 Atlas, R.M. (1995) Bioremediation. Chem. Eng. News 73, 32–42 2 Jo¨rdening, H-J. and Winter, J. (2005) Environmental Biotechnology: Concepts and Applications, Wiley-VCH, Weinheim 3 Gauri, K.L. and Bandyopadhyay, J.K. (1999) Carbonate Stone: Chemical Behaviour, Durability, and Conservation, John Wiley & Sons, New York 4 Leysen, L. et al. (1987) A study of the weathering of an historic building. Anal. Chim. Acta 195, 247–255 5 Doornkamp, J.C. and Ibrahim, H.A.M. (1990) Salt weathering. Prog. Phys. Geogr. 14, 335–348 6 Warscheid, T. and Braams, J. (2000) Biodeterioration of stone: a review. International Biodeterioration & Biodegradation 46, 343–368 7 Gaylarde, C. et al. (2003) Microbial impact on building materials: an overview. Materials and Structures 36, 342–352 8 McNamara, C.J. and Mitchell, R. (2005) Microbial deterioration of historic stone. Frontiers in Ecology and the Environment 3, 445–451 9 Rodriguez-Navarro, C. et al. (2000) How does sodium sulfate crystallize? Implications for the decay and testing of building materials. Cement Concrete Res. 30, 1527–1534 10 Rodriguez-Navarro, C. et al. (2002) Effects of ferrocyanide ions on NaCl crystallization in porous stone. J. Cryst. Growth 243, 503–516 11 Papida, S. et al. (2000) Enhancement of physical weathering of building stones by microbial populations. Int. Biodeterior. Biodegradation 46, 305–317 12 Lewin, S. (1989) The susceptibility of calcareous stones to salt decay. In The Conservation of Monuments in the Mediterranean Basin (Zezza, F., ed.), pp. 59–64, Grafo, Brescia
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