Skip to main content

REVIEW article

Front. Microbiol., 26 June 2014
Sec. Microbiotechnology
This article is part of the Research Topic Microorganisms pro- and against cultural heritage View all 5 articles

Application of calcifying bacteria for remediation of stones and cultural heritages

  • 1Department of Biotechnology, Thapar University, Patiala, India
  • 2Department of Civil Engineering, Curtin University, Perth, WA, Australia

Since ages, architects and artists worldwide have focused on usage of durable stones as marble and limestone for construction of beautiful and magnificent historic monuments as European Cathedrals, Roman, and Greek temples, Taj Mahal etc. But survival of these irreplaceable cultural and historical assets is in question these days due to their degradation and deterioration caused by number of biotic and abiotic factors. These causative agents have affected not only the esthetic appearance of these structures, but also lead to deterioration of their strength and durability. The present review emphasizes about different causative agents leading to deterioration and application of microbially induced calcium carbonate precipitation as a novel and potential technology for dealing with these problems. The study also sheds light on benefits of microbial carbonate binders over the traditional agents and future directions.

Introduction

Taking a look at our history, beautiful monuments and sculptures of limestone are seen. Be it European Cathedrals (Milan Cathedral, Italy), Roman and Greek temples, the Taj Mahal and the Pyramids, limestone is everywhere. Numerous limestone and marble quarries encouraged ancient Greek architects to build the Acropolis and Roman architects to build magnificent Forum (Corvo et al., 2000). Limestone, consisting almost entirely of calcite (the most stable polymorph of calcium carbonate) along with a small content of aragonite has been found to be highly durable building material since ages (Graedel, 2000). Though known for its great strength, these materials are highly porous and hydrophilic in nature making them highly susceptible to water (such as acid rain) and environmental pollutants (Tiano et al., 1999). The water carrying harmful and corrosive ions often penetrates into the pores of these stones leading to their deterioration. Architectural and sculptural stones have undergone deterioration due to number of factors such as physical, chemical, and biological weathering (Rodriguez-Navarro and Sebastian, 1996; Wakefield and Jones, 1998; Rodriguez-Navarro and Doehne, 1999). Several environmental pollutants, particulate matters, fly ash, smog and natural causes lead to degradation of these structures (Fernandes, 2006; Chand and Cameotra, 2011). Microorganisms inhabiting these structures, upon interaction with other detrimental biotic and abiotic factors, also promote weathering and corrosion of these building materials (Fernandes, 2006). All these factors are thereby causing great harm to physical and esthetic appearance of such structures. Because of all these reasons, survival of many cultural and historical assets is in threat. One of such examples is the cave of Lascaux in southwest France where infection of Fusarium sp. and other molds deteriorated the floor and banks of main chamber (Rosenbaum, 2006). Paintings in Altamira cave in Santillana del Mar, Spain, and the earliest known Christian paintings adorning Roman catacomb walls have also undergone similar fate.

The problem of deterioration of these historical monuments has fetched the attention of archeologists, geobiologists and bioconservators to preventive and remedial technologies to safeguard these cultural heritage monuments, which is a big challenging task. Many attempts have been made to remediate such structures by application of conservative treatments using organic and inorganic products (Lazzarini and Laurenzi Tabasso, 1986), but these agents have not been as effective as expected due to complex nature of the textures/compositions of materials encountered. Other drawback is that high amounts of organic solvents are often wasted in the environment and in few cases, these treatments even led to detrimental effects on the stone material in context to its texture, physical strength and esthetic appearance (González-Muñoz, 2008). None of the tested conventional treatment methods have proved to be satisfactory for the preservation and consolidation of these deteriorated monuments (Cappitelli et al., 2007; González-Muñoz, 2008) (Table 1). Hence, the durability related issues are causing high impact on national economies as huge sums of money are required for maintenance and repair of such structures. The short comings of conventional methods have encouraged the search and development of new conservation treatments for remediation and protection of these magnificent materials, based on biological methods (Fernandes, 2006).

TABLE 1
www.frontiersin.org

Table 1. Methodologies for eradication of degradative agents of stone works.

Microbial geotechnology, i.e., microbial based technology for civil structures is an emerging discipline of science which has developed immensely in the recent years. Microbially induced carbonate precipitation has successfully emerged as a novel method to protect and remediate decayed building structures and materials. The method of use of bacteria for remediating building materials is mimicry of the nature as many carbonate rocks have been cemented by precipitation of carbonates induced by microbes. This technology of application of bacteria for precipitation of carbonates has been successfully used for solving various durability issues of different construction materials as it is novel and eco—friendly method to protect and restore the decayed construction materials (Dhami et al., 2012, 2013).

In the present review, an attempt has been made to provide an overview of the various agents responsible for deterioration of stone monuments (statues, buildings, paintings etc.) and the current methods for restoration of the important stone works with focus on microbially induced carbonate precipitation as promising technology for bioremediation of such structures. The aim is to highlight the contribution of Applied Microbiology and Biotechnology in successfully solving various problems related to durability issues of historical and important building materials.

Deterioration of Stone Works: Causative Agents

The deterioration of historic monuments and stone works occurs due to numerous factors leading to stone dissolution, staining or color alteration, surface alterations, biocorrosion and transformations into smaller sized crystals etc. (Chand and Cameotra, 2011). In the last decades, alterations have occurred mainly due to microbial biofilm production, deposition of organic and inorganic compounds, formation of black crusts, nitratation, sulphatation and, due to residual hydrocarbons and other organic pollutants in dust (Warscheid and Braams, 2000; Fernandes, 2006; Di Pippo et al., 2009).

Nitrates

Nitrates, originating from the reaction of numerous oxides of nitrogen present in atmosphere (N2O, NO, N2O3, NO2, N2O5) due to pollution formed through oxidation upon reaction with water vapor produces nitrous acid and more abundant nitric acid (HNO3) as final products. These acids result in the formation of acid rain and attack the stone structures causing formation of calcium nitrate salts on the stone buildings (Ranalli et al., 1999).

Sulfates

Sulfates, which originate from oxidation of sulfur dioxide lead to the formation of sulfuric acid (H2SO4) resulting in acid rain. These acid rains cause transformation of insoluble calcium sulfate posing potential risk not only to buildings but also for humans (Ranalli et al., 1999).

Black crusts

Black crusts are normally formed as a result of mixing of gypsum crystals with atmospheric particles (pollen, dusts, spores, particulate matter called smog etc.) (Saiz-Jimenez, 1991; Saiz-Jimenez and Garcia del Cura, 1991). Calcium sulfate salt crusts also accumulate particles of soot originating from fossil fuel consumption and form black crusts (Kumar and Kumar, 1999; Warscheid and Braams, 2000).

Organic matter

Organic matter is ascribed to the lysis of microbial cells and presence of hydrocarbons originating from combustion of oil. This type of deterioration becomes more evident in the buildings located in the open as atmospheric pollution also contributes to add up the degradation process (Ranalli et al., 1999). The formation of all these crusts affect stone's texture, crystal structure, composition, coherence, water uptake and strength.

Microorganisms

Microorganisms (Bacteria, Archaea, Fungi, Algae, Lichens), along with mosses and higher plants, have been reported commonly on stoneworks leading to deterioration of several types of materials as stone works, wood, tapestries, papyrus, canvas, paper etc. (Cappitelli and Sorlini, 2005; McNamara and Mitchell, 2005; Ramírez et al., 2005) (Table 2). These microorganisms are amongst the major players of biodegradation of several stone work buildings. The photolithoautotrophic nature of algae and cyanobacteria facilitate colonization of stone by many other microorganisms (e.g., fungi and bacteria) (Warscheid and Braams, 2000; McNamara and Mitchell, 2005). The nitrifying bacteria (Nitrosomonas spp. and Nitrobacter spp.), capable of excreting nitrous and nitric acid and sulfur-oxidizing bacteria (Thiobacillus spp.) which produce sulfuric acid leads to biocorrosion of the stone material (Gómez-Alarcón et al., 1995; Warscheid and Braams, 2000). The acid formed reacts with stone constituents to produce sulfate-based crusts which upon precipitation in pores of stone cause considerable stress in porewalls. Biocorrosion also occurs by chemoorganothrophic microorganisms, including several bacteria and fungi (Acidithiobacillus ferrooxidans, Bacillus spp., Leptospirillum spp., Aureobasidium spp.) as well as lichens as they excrete organic acids. These acids have been reported to chelate the metal cations (e.g., Fe, Mg, Mn, Si, Al, Ca etc.) from minerals to form complexes which are quite stable with time (Kumar and Kumar, 1999; Warscheid and Braams, 2000; McNamara and Mitchell, 2005; Rawlings, 2005). Physical penetration by lichens and fungi also contributes to degradation. The hyphae of fungus penetrate deeply beneath the stone surface, causing not only mechanical deterioration but also transport of water and nutrients through the stone facilitating colonization of stone interior by bacteria leading to biochemical deterioration (Gómez-Alarcón and de La Torre, 1994).

TABLE 2
www.frontiersin.org

Table 2. Microorganisms and environmental factors involved in biodeterioration of architectural buildings and artworks (Source: Dakal and Cameotra, 2012).

Several attempts have been made to decrease the susceptibility to decay by many conservation treatments which includes application of surface sealing or consolidating agents to the substrate resulting in organic/inorganic precipitation of binding material in the pores of stone (Adeyemi and Gadd, 2005). These stone consolidants reestablish the binding between the grains of degraded stone. To protect the stone from water ingress and weathering agents, water repellents have also been applied. These chemicals have short efficacy due to their chemical composition and thermal expansion coefficient which are quite different from that of the stone (De Muynck et al., 2010). But due to incompatibility problems with the stone, consolidants as well as water repellents have been reported to accelerate decay of the stone material (Clifton and Frohnsdorff, 1982; Delgado Rodrigues, 2001; Moropoulou et al., 2003). Efforts have been made to introduce methods based on CaCO3 precipitation into the pores of limestone by few researchers. Application of saturated solution of calcium hydroxide (Lime-water technique) has been used on degraded stones so as to impart a slight water repellent and consolidating effect (Tiano et al., 1999). But, little success has been achieved till now in consolidation of stone with inorganic materials. This is because of the tendency of these materials to generate shallow and hard crusts due to their poor penetration abilities, growth of precipitated crystals, salts formation and stone particle binding ability (Clifton and Frohnsdorff, 1982).

To overcome the limitations of these conventional treatments, researchers proposed microbially induced calcium carbonate precipitation as an eco-friendly method to protect and restore degraded ornamental stones (Le Metayer-Levrel et al., 1999; Stocks-Fischer et al., 1999; Ramachandran et al., 2001; Ramakrishnan et al., 2001; De Muynck et al., 2008a,b). Although microorganisms have often been associated with detrimental effects on the integrity of stone structures, affecting mineral integrity or exacerbating powerful physical processes of deterioration (Papida et al., 2000), there is an increase of evidence that they could be used to reverse the deterioration processes on historical objects of art (Atlas et al., 1988; Lal Gauri et al., 1989b; Orial et al., 1992; Castanier et al., 1999; Perito et al., 1999; Ranalli et al., 1999).

Microbially Induced Calcium Carbonate Precipitation

Microbially induced calcium carbonate precipitation (MICCP) is a process where an organism creates a local micro-environment, with conditions that permits precipitation of carbonates (Hamilton, 2003). Bacteria isolated from different natural habitats have been reported for their ability to precipitate calcium carbonate both in natural and laboratory conditions (Krumbein, 1979; Rodriguez-Navarro et al., 2003). Precipitation of carbonates varies based on the types of bacteria, abiotic factors such as salinity and composition of the nutrients in various environments (Knorre and Krumbein, 2000; Rivadeneyra et al., 2004). Calcium carbonate precipitation is a chemical process and influenced by four main factors such as the calcium concentration, amount of dissolved inorganic carbon (DIC), availability of nucleation sites and pH (Hammes and Verstraete, 2002). Sufficient calcium and carbonate ions are required for CaCO3 precipitation so that the ion activity product (IAP) exceeds the solubility constant (Kso) Equations (1) and (2). From the comparison of the IAP with the Kso, the saturation state (Ω) of the system can be defined; if Ω > 1, then the system is oversaturated and precipitation is likely to occur as mentioned below by Morse (1983):

Ca2++CO32CaCO3    (1)
Ω=a (Ca2+) a (CO32)/Ksowith        Kso calcite,25° = 4.8×109    (2)

As mentioned previously, the amount of carbonate ions is related to the amount of DIC and pH of a given aquatic system. However, the amount of DIC depends on several environmental parameters like temperature and partial pressure of carbon dioxide. The equilibrium reactions and constants governing the dissolution of CO2 in aqueous media (25°C and 1 atm) are given below in Equations (3)–(6) as suggested by Stumm and Morgan (1981):

CO2(g)CO2(aq)(pKH = 1.468)    (3)
CO2(aq)+H2OH2CO3(pK = 2.84)    (4)
H2CO3H++ HCO3(pK1 = 6.352)    (5)
HCO3 CO32+ H+(pK2 = 10.329)    (6)
With H2CO3 = CO2(aq) + H2CO3    (7)

Hammes and Verstraete (2002) suggested that microorganisms influence precipitation by altering any of the precipitation parameters described above, either separately or in various combinations with one another. MICCP has gained increasing interest in the last 20 years and found to be the primary focus of research in bio geo civil engineering because of its numerous applications.

There are mainly four groups of microorganisms involved in the process, which are: (i) photosynthetic organisms such as cyanobacteria and algae, (ii) sulfate reducing bacteria responsible for dissimilatory reduction of sulfates, (iii) organisms utilizing organic acids, and (iv) organisms that are involved in nitrogen cycle either by ammonification of amino acids/nitrate reduction or hydrolysis of urea (Stocks-Fischer et al., 1999; Hammes and Verstraete, 2002; Jargeat et al., 2003).

In aquatic environments, MICCP is primarily caused by photosynthetic organisms (McConnaughey and Whelan, 1997). Algae and cyanobacterial metabolic processes utilize dissolved CO2 Equation (8), which is in equilibrium with HCO3 and CO32 Equation (9). The removal of CO2 induces a shift in this equilibrium, and results in an increase in pH Equation (10) (Ehrlich, 1998) and in presence of calcium ions, this reaction leads to precipitation of calcium carbonate as mentioned by Hammes and Verstraete (2002) Equation (11).

CO2+H2O(CH2O) + O2    (8)
2HCO3CO2+CO32+H2O    (9)
CO32+H2OHCO3+OH    (10)
Ca2++HCO3+OHCaCO3+2H2O    (11)

Calcium carbonate precipitation via this pathway occurs in sea water, geological formations (Packman et al., 1999; Machel, 2001), in landfill leachates (Maliva et al., 2000) and even during the biological treatment of acid mine drainage (Kaufman et al., 1996). Chiefly, in several of the described examples for this pathway, instead of calcite, dolomite and aragonite are the predominant minerals to precipitate (Packman et al., 1999; Wright, 1999; Warthmann et al., 2000; Machel, 2001).

Calcium carbonates can also be precipitated by heterotrophic organisms, by the production of carbonate or bicarbonate and modification of the environment to favor precipitation (Castanier et al., 1999). The abiotic dissolution of gypsum (CaSO4.2H2O) Equation (12) provides an environment that is rich in both sulfate and calcium ions. In the presence of organic matter and absence of oxygen, sulfate reducing bacteria can reduce sulfate to H2S and release HCO3 Equation (13) (Ehrlich, 1998; Castanier et al., 1999; Wright, 1999). If H2S then degasses from the environment, this results in an increase in pH and favors the precipitation of calcium carbonate Equation (11) (Castanier et al., 1999).

CaSO4·2H2OCa2++SO42+2H2O    (12)
2(CH2O)+SO42HS+HCO3+CO2+H2O    (13)

Third pathway includes bacteria which use organic acids as their only source of carbon and energy wherein some common species of soil bacteria are included. Such acids include oxalate, acetate, citrate, glyoxylate, succinate and malate. The consumption of these acids results in pH increase, which leads to precipitation of carbonates in the presence of calcium ions Equations (14)–(16) (Knorre and Krumbein, 2000; Braissant et al., 2002)

CH3COO+2O2CO2+H2O+OH    (14)
2CO2+OHCO2+HCO3    (15)
2HCO3+Ca2+CaCO3+CO2+H2O    (16)

Numerous heterogenous bacterial groups are linked to this precipitation mechanism. Braissant et al. (2002) speculated that this pathway might be extremely common in natural environments due to the abundance of such low molecular weight acids in the soils (produced by fungi and plants).

Microbially Induced Calcium Carbonate Precipitation Via Urea Hydrolysis

The precipitation of carbonates by bacteria through urea hydrolysis is the most straightforward and easily controlled mechanism of MICCP with precipitation of high amounts of carbonates in less time. Stocks-Fischer et al. (1999) suggested that during microbial urease activity, 1 mol of urea is hydrolyzed intracellularly to 1 mol of ammonia and 1 mol of carbonate Equation (17), which spontaneously hydrolyzes to form additional 1 mol of ammonia and carbonic acid Equation (18). These products equilibrate in water to form bicarbonate, 1 mol of ammonium and hydroxide ions which increases the pH. The above information is mentioned below through equations as reported by Stocks-Fischer et al. (1999)

CO(NH2)2+H2ObacteriaNH2COOH+NH3    (17)
NH2COOH+H2ONH3+H2CO3    (18)
H2CO32H++2CO32    (19)
NH3+H2ONH4++OH    (20)
Ca2++CO32CaCO3(KSP=3.8×109)    (21)

KSP is the solubility product in Equation (21).

The main role of bacteria has been ascribed to their ability to create an alkaline environment through various physiological activities. The surface of bacteria plays an important role in precipitation of calcium (Fortin et al., 1997). At a neutral pH, the metal ions which are positively charged get bound on the surfaces bacteria due to presence of several negatively charged groups which favors heterogenous nucleation (Douglas and Beveridge, 1998; Bäuerlein, 2003). Generally, the precipitation of carbonates on the external surface of bacterial cells occurs by successive stratification (Pentecost and Bauld, 1988; Castanier et al., 1999) and these bacterial cells get embedded in growing carbonate crystals (Rivadeneyra et al., 1998) (Figure 1).

FIGURE 1
www.frontiersin.org

Figure 1. Bacteria serving as nucleation site for CaCO3 precipitation in the substrate particles. Calcium ions in the solution are attracted to the bacterial cell wall due to its negative charge. When urea is added to bacteria, dissolved inorganic carbon (DIC) and ammonium (AMM) are released in the microenvironment of the bacteria. In the presence of calcium ions, this leads to local supersaturation and finally there is precipitation of calcium carbonates which act as binder between loose substrate particles (Source: DeJong et al., 2010).

Biochemical reactions which take place in the urea-CaCl2 medium leading to precipitation of CaCO3 at the cell surface (Stocks-Fischer et al., 1999) and act as binders in between the substrate particles can be listed as:

Ca2++CellCellCa2+    (22)
Cl+HCO3+NH3NH4Cl+CO32    (23)
CellCa2++CO32CellCaCO3    (24)

So, mineralizing activities of microorganisms can now be harnessed positively, making them essential to the existence of ecology of Earth. The use of microbially induced carbonate biominerals is becoming increasingly popular day by day. From removal of heavy metals and radio nucleotides, removal of calcium from wastewater and biodegradation of pollutants, atmospheric CO2 sequestration, modifying the properties of soil and filler in rubber and plastics to fluorescent markers in stationery ink and remediation of building materials, bacterial carbonates are serving many fields (Dhami et al., 2013).

Microbial Carbonates: Remediation of Limestone

Boquet et al. (1973) firstly demonstrated the precipitation of calcium carbonate by soil bacteria under laboratory conditions. Previous researchers showed precipitation of carbonates by marine bacteria only in liquid media while Drew (1911) and Shinano (1972), investigated the carbonate precipitation by soil bacteria on solid media and obtained best results with B4 medium. Among the organisms tested, several Bacillus strains and Pseudomonas aeruginosa were observed to form crystals. Castanier et al. (1999) reported the microbial origin of limestone while Adolphe et al. (1989) further demonstrated the bacterial origin of the calcite crusts and found great resistance against erosion by this calcite layer. Adolphe et al. (1990) applied patent for the treatment of artificial surfaces by surface coatings produced by microorganisms and formed a company “Calcite Bioconcept.” The promising results of “Calcite Bioconcept” encouraged many researchers to look for different approaches for bioremediation of stone by microbial carbonates. First approach was based on usage of different microbes and metabolic pathways or delivery systems to overcome limitations of “Calcite Bioconcept” technique while in second approach, no microbes were applied directly rather inducing macromolecules along with supersaturated solution of calcium carbonate and carbonate precipitation by microbiota inhabiting the stone were investigated.

The carbonate precipitation ability of bacteria had been demonstrated under laboratory but further experiments are required to assess the viability and carbonate precipitation ability of these bacteria in situ. The collaboration between the University of Nantes, the Laboratory for the research of historic monuments (LRMH) and the “Calcite Bioconcept” (Le Metayer-Levrel et al., 1999) led to the optimization and industrialization of this concept. Upon investigating different bacteria, Castanier et al. (1999) reported the highest performance by B. cereus which was further selected for in situ applications (Orial, 2000). This paved way to optimization of the nutrient media with source of proteins for the oxidative deamination of amino acids by aerobiosis and nitrogen source for the dissimilatory reduction of nitrate in anaerobiosis and microaerophilic conditions along with a fungicide to prevent undesirable growth of fungi on the stone (Orial et al., 2002). The first application in situ was carried out in 1993 in Thouars on the tower of the Saint Médard Church. It was reported that presence of the biocalcin reduced water absorption rate to five time s and did not affect the esthetic appearance (Le Metayer-Levrel et al., 1999). But Orial (2000) suggested that after every 10 years a new biocalcin treatment was needed to restore its protective effect. This technology was also applied on limestone statuaries in different climatic environments where it was found to be highly successful even after 4 years of application. Addition of natural pigments into the nutritional medium created a surficial patina with the biodeposition treatment. The pigments integrated into the biocalcin resulted a persistent light coloring to the stone. This technique concealed some newly replaced stones on a monument (Le Metayer-Levrel et al., 1999). Alhough B. cereus was quite effective in bioconsolidation, but the layer of new cement induced was very thin, just a few microns—thick. Formation of endospores and formation of uncontrolled biofilm by Bacillus species provides a drawback in stone conservation. Hence, Rodriguez-Navarro et al. (2003) proposed the use of Myxococcus Xanthus, which is Gram-negative, nonpathogenic soil bacteria. This bacterium is known to induce the precipitation of carbonates, sulfates and phosphates in wide range of solid and liquid media (González-Muñoz et al., 1993, 1996; Ben Omar et al., 1995, 1998; Ben Chekroun et al., 2004; Rodriguez-Navarro et al., 2007). Application of this bacterial suspension on stone specimens showed no fruiting bodies and no uncontrolled bacterial growth. Calcium carbonate precipitation was observed up to a depth of several 100 μm (>500 μm) without plugging or blocking of the pores. Plugging mainly occurs due to biofilm formation through extracellular polymeric substance (EPS) (Tiano et al., 1999).

Tiano et al. (1999) studied the effect of microbial calcite crystals on Pietra di Lecce bioclastic limestone by Micrococcus spp. and Bacillus subtilis and their results showed a significant reduction in water absorption. The authors also commented some negative consequences, such as (i) the formation of new products due to chemical reactions between stone minerals and some by-products originating from the metabolism of bacteria, and (ii) the formation of stained patches because of the growth of air-borne fungi. To avoid such short comings, the authors used some natural and synthetic polypeptides to control the calcite crystal growth in the pores. Use of organic matrix macromolecules (OMM) isolated from Mytilus californianus shells was proposed to induce the precipitation of calcium carbonate within the pores of the stone (Tiano et al., 1992; Tiano, 1995). Slight decrease in porosity and water absorption by capillarity was observed in this case (Tiano, 1995). This method was not much beneficial due to the complexity of isolation procedure as well as less yield of usable product (Tiano et al., 1999). Hence, in place of this bio inducing macromolecules (BIM) rich in aspartic acid groups, Tiano et al. (2006) proposed to use acid functionalized proteins such as polyaspartic acid. Calcium and carbonate ions were supplied for calcite crystal growth, by addition of ammonium carbonate and calcium chloride solution or a solution of saturated bicarbonate. The consolidating effect was observed to be very low compared to ethylsilicates (Tiano et al., 2006). Dick et al. (2006) observed 50% reduction in water absorption by treating limestone cubes with two strains of B. sphaericus (Figure 2).

FIGURE 2
www.frontiersin.org

Figure 2. Colonies of 6 different strains of B. sphaericus and B. lentus on agar plates and their ability to encrust themselves in calcium carbonate (Source: Dick et al., 2006).

To improve the methodologies for delivering bacterial cells to stone surfaces and also to control the side effects of bacteria to the stone, various carrier materials were looked upon. Ranalli et al. (1997) used sepiolite for delivering Desulfovibrio vulgaris and D. desulfuricans, as it provides anaerobic conditions, humidity and shorten the treatment time. Cappitelli et al. (2006) proposed Carbogel as a delivery system for bacteria due to its high retention of viable bacteria and less time to entrap cells (Figure 3). Different methodologies where microbial calcite has been deposited as a layer on surface of stone is presented in Table 3.

FIGURE 3
www.frontiersin.org

Figure 3. Scanning electron microscopy (SEM) observations of Carbogel without (left) and with (right) D. vulgaris subsp. vulgaris ATCC 29579 cells (Source: Cappitelli et al., 2006).

TABLE 3
www.frontiersin.org

Table 3. Overview of different methodologies where microbial calcite has been deposited as a layer on surface of stone.

Precipitation of calcite crystals by fresh water bacteria on limestone significantly reduced the pore sizes of the stone (Zamarreno et al., 2009). Calcite crystals were deposited around and inside open pore spaces. Application of calcite crystals filled 43–49% of the open pore spaces which was 20% higher than the application of the medium alone. De Muynck et al. (2012) reported B. sphaericus to be very efficient strain for consolidation of limestone specimens at range of temperatures (10, 20, 28, 37°C). This isolate led to 64% lower weight loss upon sonication and 46% decreased sorptivity in treated limestone specimens compared to the control specimens. De Muynck et al. (2011) recently applied bacterial calcite in two types of stones: microporous and macroporous. They reported that application of bacterial carbonates is more successful in macroporous stone where it occurs to a larger extent and at greater depths than in microporous stone. It has also been shown on laboratory scale that several bacterial strains (such as Pseudomonas stutzeri, P. aeruginosa, D. vulgaris, and D. desulfuricans) are not only able to denitrify and desulfuricate harmful masonry salts such as nitrate and sulfate (Lal Gauri et al., 1989a; Heselmeyer et al., 1991; Ranalli et al., 1999) but also mineralize organic residues or pollutants like carbohydrates, waxes or hydrocarbons that commonly occur in crusts on stonework (Warscheid et al., 1991; Saiz-Jimenez, 1997; Ranalli et al., 1999).

From the above mentioned applications, microbial concrete seems to bring a new revolution in the civil industry. Use of bacteria to improve the durability of building materials has drawn the attention of research groups all over the world. But several challenges have to be met before acceptance of this technology by conservators.

Limitations and Challenges

Though there are many advantages of MICCP technology for bioremediation of several stone structures but there are a few limitations also. In comparison to chemical treatments, biobased treatments are found to be more complex because the microbial activity depends on many environmental factors such as temperature, pH, concentrations of donors and acceptors of electrons, concentrations and diffusion rates of nutrients and metabolites. Design of experiments for biodeposition treatments require a huge data of the biological processes (growth, biosynthesis, specific enzymatic activities), chemical reactions accompanied with formation of insoluble compounds, physic—chemical processes as precipitation, crystallization, and adhesion.

Due to this complexity, its usage at large-scale has not been so encouraging. The inconvenient application procedures also are major gaps for successful commercialization. The precipitation of carbonates mainly depends on time required for carbonate formation. If precipitation time increases, then the amounts of EPS production increases, and hence plugging but multiple applications of nutrients and usage of carrier materials have significant influence on the total cost of treatment (Le Metayer-Levrel et al., 1999; May, 2005). Production of ammonia during hydrolysis of urea poses environmental as well as leads to discoloration of stone (Sutton et al., 2008; Tobler et al., 2011). Ammonium is also converted to nitric acid due to the action of denitrifying bacteria which results in significant damage to the stone. Additional research is necessary to overcome this problem. As the amounts of carbonate precipitates formed are dependent on amount of calcium added, increased concentration of calcium leads to accumulation of salts and paves way to efflorescence and damage to crystallization. The survival of bacteria within the stone material also influences the extent of calcification. As the laboratory grade nutrient media limit the economical usage of this technology for commercial scales, there is great need to look for alternative economical and cheap medium ingredients as corn steep liquor and lactose mother liquor (Achal et al., 2009, 2010). Large scale production of bacterial cultures is also a hindrance in the path of success of this technology over traditional treatments. The above mentioned concerns limit the use of MICCP for practical applications in various fields in comparison to the traditional methods.

Conclusion

Microbially induced calcium carbonate precipitation technology has been found to be highly promising with potential to successfully remediate and protect several stone structures. The eco–friendly, self-healing and highly durable nature of these bio-binders encourage their biotechnological applications for several purposes. Carbonate formation by this technology has been found to be very easy and convenient. The potential of these bio-binders has brought a new revolution in field of civil engineering but still there has been much to explore in order to bring this environmentally safe, cost effective and convenient technology from lab to field scales. There is need to assess the long term efficacy of microbial carbonates and compared to chemical binders. As the success of this technology needs experts from varying sectors from Microbiologists to Geologists to Civil Engineers, researchers from all around the globe should work together to make this multi-disciplinary research move toward commercial scale applications at a higher pace.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

Achal, V., Mukherjee, A., Basu, P. C., and Reddy, M. S. (2009). Lactose mother liquor as an alternative nutrient source for microbial concrete production by Sporosarcina pasteurii. J. Ind. Microbiol. Biotechnol. 36, 433–438. doi: 10.1007/s10295-008-0514-7

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Achal, V., Mukherjee, A., and Reddy, M. S. (2010). Biocalcification by Sporosarcina pasteurii using Corn steep liquor as nutrient source. J. Ind. Biotechnol. 6, 170–174. doi: 10.1089/ind.2010.6.170

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Adeyemi, A. O., and Gadd, G. M. (2005). Fungal degradation of calcium, lead and silicon—bearing minerals. Biometals 18, 269–281. doi: 10.1007/s10534-005-1539-2

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Adolphe, J. P., Hourimèche, A., Loubière, J. F., Paradas, J., and Soleilhavoup, F. (1989). Les formations carbonatées d'origine bactérienne. Formations continentales d'Afrique du Nord. Bull. Soc. Geol. Fr. 8, 55–62.

Adolphe, J. P., Loubière, J. F., Paradas, J., and Soleilhavoup, F. (1990). Procédé de traitement biologique d'une surface artificielle. European Patent 90400G97.0. (after French patent 8903517, 1989), (France).

Atlas, R. M., Chowdhury, A. N., and Gauri, K. L. (1988). Microbial calcification of gypsum – rock and sulfated marble. Studies in conservation 33, 149–153. doi: 10.1179/sic.1988.33.3.149

CrossRef Full Text

Bäuerlein, E. (2003). Biomineralization of unicellular organisms: an unusual membrane biochemistry for the production of inorganic nano- and microstructures. Angew Chem Int. 42, 614–641. doi: 10.1002/anie.200390176

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Ben Chekroun, K., Rodriguez-Navarro, C., González-Muñoz, M. T., Arias, J. M., Cultrone, G., and Rodriguez-Gallego, M. (2004). Precipitation and growth morphology of calcium carbonate induced by Myxococcus xanthus: implications for recognition of bacterial carbonates. J. Sediment. Res. 74, 868–876. doi: 10.1306/050504740868

CrossRef Full Text

Ben Omar, N., González-Muñoz, M. T., and Peñnalver, J. M. A. (1998). Struvite crystallization on Myxococcus cells. Chemosphere 36, 475–481. doi: 10.1016/S0045-6535(97)10014-5

CrossRef Full Text

Ben Omar, N., Martínez-Cañamero, M., González-Muñoz, M. T., Maria Arias, J., and Huertas, F. (1995). Myxococcus xanthus killed cells as inducers of struvite crystallization. Its possible role in the biomineralization processes. Chemosphere 30, 2387–2396. doi: 10.1016/0045-6535(95)00110-T

CrossRef Full Text

Boquet, E., Boronat, A., and Ramos-Cormenzana, A. (1973). Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246, 527–529. doi: 10.1038/246527a0

CrossRef Full Text

Braissant, O., Verrecchia, E., and Aragno, M. (2002). Is the contribution of bacteria to terrestrial carbon budget greatly underestimated. Naturwissenschaften 89, 366–370. doi: 10.1007/s00114-002-0340-0

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Cappitelli, F., and Sorlini, C. (2005). From papyrus to compact disc: the microbial deterioration of documentary heritage. Cr. Rev. Microbiol. 31, 1–10. doi: 10.1080/10408410490884766

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Cappitelli, F., Lucia Toniolo, L., Sansonetti, A., Gulotta, D., Ranalli, G., Zanardini, E., et al. (2007). Advantages of using microbial technology over traditional chemical technology in removal of black crusts from stone surfaces of historical monuments. Appl. Environ. Microb. 73, 5671–5675. doi: 10.1128/AEM.00394-07

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Cappitelli, F., Zanardini, E., Ranalli, G., Mello, E., Daffonchio, D., and Sorlini, C. (2006). Improved methodology for bioremoval of black crusts on historical stone artworks by use of sulfate—reducing bacteria. Appl. Environ. Microbiol. 72, 3733–3737. doi: 10.1128/AEM.72.5.3733-3737.2006

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Castanier, S., Le Metayer-Levrel, G., and Perthuisot, J. P. (1999). Ca-carbonates precipitation and limestone genesis—the microbiogeologist point of view. Sediment. Geol. 126, 9–23. doi: 10.1016/S0037-0738(99)00028-7

CrossRef Full Text

Chand, T., and Cameotra, S. S. (2011). “Geomicrobiology of heritage monuments and artworks: mechanisms of biodeterioration, bioconservation strategies and applied molecular approaches,” in Bioremediation: Biotechnology, Engineering and Environmental Management (New York, NY: Nova Science Publishers), 233–266.

Clifton, J. R., and Frohnsdorff, G. J. C. (1982). “Stone consolidating materials: a status report,” in Conservation of Historic Stone Buildings and Monuments, ed C. Eisenhart (Washington, DC: National Academy Press), 287–311.

Corvo, F., Reyes, J., Valdes, C., Villaseñor, F., Cuesta, O., Aguilar, D., et al. (2000). Influence of air pollution and humidity on limestone materials degradation in historical buildings located in cities under tropical coastal climates. Water Air Soil Poll. 205, 359–375. doi: 10.1007/s11270-009-0081-1

CrossRef Full Text

Dakal, T. C., and Cameotra, S. S. (2012). Microbially induced deterioration of architectural heritages: routes and mechanisms involved. Environ. Sci. Eur. 24:36. doi: 10.1186/2190-4715-24-36

CrossRef Full Text

De Muynck, W., Cox, K., De Belie, N., and Verstraete, W. (2008a). Bacterial carbonate precipitation as an alternative surface treatment for concrete. Constr. Build. Mater. 22, 875–885. doi: 10.1016/j.conbuildmat.2006.12.011

CrossRef Full Text

De Muynck, W., Debrouwer, D., De Belie, N., and Verstraete, W. (2008b). Bacterial carbonate precipitation improves the durability of cementitious materials. Cem. Concr. Res. 38, 1005–1014. doi: 10.1016/j.cemconres.2008.03.005

CrossRef Full Text

De Muynck, W., Belie, N., and Verstraete, W. (2010). Microbial carbonate precipitation in construction materials: a review. Ecol. Eng. 36, 118–136. doi: 10.1016/j.ecoleng.2009.02.006

CrossRef Full Text

De Muynck, W., Leuridan, S., Van Loo, D., Verbeken, K., Cnudde, V., De Belie, N., et al. (2011). Influence of pore structure on the effectiveness of a biogenic carbonate surface treatment for limestone conservation. Appl. Environ. Microbiol. 77, 6808–6820. doi: 10.1128/AEM.00219-11

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

De Muynck, W., Verbeken, K., De Belie, N., and Verstraete, W. (2012). Influence of temperature on the effectiveness of a biogenic carbonate surface treatment for limestone conservation. Appl. Microbiol. Biotechnol. 97, 1335–1347. doi: 10.1007/s00253-012-3997-0

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

DeJong, J. T., Mortenson, B. M., Martinez, B. C., and Nelson, D. C. (2010). Bio-mediated Soil Improvement. Ecol. Eng. 36, 197–210. doi: 10.1016/j.ecoleng.2008.12.029

CrossRef Full Text

Delgado Rodrigues, J. (2001). “Consolidation of decayed stones. A delicate problem with few practical solutions,” in International Seminar on Historical Constructions, eds P. B. Lourenço and P. Roca (Guimaráes: Guimarães), 3–4.

Dhami, N. K., Mukherjee, A., and Reddy, M. S. (2012). “Biofilm and microbial applications in biomineralized concrete,” in Advanced Topics in Biomineralization, ed Jong Seto (New York, NY: InTech), 137–164.

Dhami, N. K., Mukherjee, A., and Reddy, M. S. (2013). Biomineralization of calcium carbonates and their engineered applications: a review. Front. Microbiol. 4:314. doi: 10.3389/fmicb.2013.00314

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Di Pippo, F., Bohn, A., Congestri, R., De Philippis, R., and Albertano, P. (2009). Capsular polysaccharides of cultured phototrophic biofilms. Biofouling 25, 495–504. doi: 10.1080/08927010902914037

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Dick, J., De Windt, W., De Graef, B., Saveyn, H., Van der Meeren, P., De Belie, N., et al. (2006). Bio-deposition of a calcium carbonate layer on degraded limestone by Bacillus species. Biodegradation 17, 357–367. doi: 10.1007/s10532-005-9006-x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Douglas, S., and Beveridge, T. J. (1998). Mineral formation by bacteria in natural microbial communities. FEMS Microbiol. Ecol. 26, 79–88. doi: 10.1111/j.1574-6941.1998.tb00494.x

CrossRef Full Text

Drew, G. H. (1911). The action of some denitrifying bacteria in tropical and temperate seas, and bacterial precipitation of calcium carbonate in the sea. J. Mar. Biol. Assoc. 9, 142–155. doi: 10.1017/S0025315400073318

CrossRef Full Text

Ehrlich, H. L. (1998). Geomicrobiology: its significance for geology. Earth Sci. Rev. 45, 45–60. doi: 10.1016/S0012-8252(98)00034-8

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Fernandes, P. (2006). Applied microbiology and biotechnology in the conservation of stone cultural heritage materials. Appl. Microbiol. Biotechnol. 73, 291–296. doi: 10.1007/s00253-006-0599-8

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Fortin, D., Ferris, F. G., and Beveridge, T. J. (1997). Surface-mediated mineral development by bacteria. Rev. Mineral. 35, 161–180.

Gómez-Alarcón, G., and de La Torre, M. A. (1994). Mechanisms of microbial corrosion on petrous materials. Microbiologia 10, 111–120.

Pubmed Abstract | Pubmed Full Text

Gómez-Alarcón, G., Cilleros, B., Flores, M., and Lorenzo, J. (1995). Microbial communities and alteration processes in monuments at Alcala de Henares, Spain. Sci. Total Environ. 167, 231–239. doi: 10.1016/0048-9697(95)04584-N

CrossRef Full Text

González-Muñoz, M., Arias, J. M., Montoya, E., and Rodriguez-Gallego, M. (1993). Struvite production by Myxococcus coralloides D. Chemosphere 26, 1881–1887. doi: 10.1016/0045-6535(93)90081-F

CrossRef Full Text

González-Muñoz, M. T., Ben Omar, N., Martinez-Cañamero, M., Rodriguez-Gallego, M., Lopez-Galindo, A., and Arias, J. M. (1996). Struvite and calcite crystallization induced by cellular membranes of Myxococcus xanthus. J. Cryst. Growth 163, 434–439. doi: 10.1016/0022-0248(95)01011-4

CrossRef Full Text

González-Muñoz, M. T. (2008). Bacterial biomineralization applied to the protection- consolidation of ornamental stone: current development and perspectives. Coalition 15, 12–18.

Graedel, T. E. (2000). Mechanisms for the atmospheric corrosion of carbonate stone. J. Electrochemical Soc. 147, 1006–1009. doi: 10.1149/1.1393304

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Gu, J. D. (2003). Microbiological deterioration and degradation of synthetic polymeric materials: recent research advances. Int. Biodeterior. Biodegrad. 52, 69–91. doi: 10.1016/S0964-8305(02)00177-4

CrossRef Full Text

Hamilton, W. A. (2003). Microbially influenced corrosion as a model system for the study of metal microbe interactions: a unifying electron transfer hypothesis. Biofoulin 19, 65–76. doi: 10.1080/0892701021000041078

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Hammes, F., and Verstraete, W. (2002). Key roles of pH and calcium metabolism in microbial carbonate precipitation. Rev. Environ. Sci. Biotechnol. 1, 3–7. doi: 10.1023/A:1015135629155

CrossRef Full Text

Heselmeyer, K., Fisher, U., Krumbein, K. E., and Warscheid, T. (1991). Application of Desulfovibrio vulgaris for the bioconversion of rock gypsum crusts into calcite. Bioforum 1/2, 89.

Jargeat, P., Rekangalt, D., Verner, M. C., Gay, G., Debaud, J. C., Marmeisse, R., et al. (2003). Characterisation and expression analysis of a nitrate transporter and nitrite reductase genes, two members of a gene cluster for nitrate assimilation from the symbiotic basidiomycete Hebeloma cylindrosporum. Curr. Genet. 43, 199–205. doi: 10.1007/s00294-003-0387-2

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Kaufman, E. N., Little, M. H., and Selvaraj, P. T. (1996). Recycling of FGD gypsum to calcium carbonate and elemental sulfur using; mixed sulfate-reducing bacteria with sewage digest as a carbon source. J. Chem. Technol. Biotechnol. 66, 365–374.

Pubmed Abstract | Pubmed Full Text

Knorre, H., and Krumbein, K. E. (2000). “Bacterial calcification,” in Microbial Sediments, eds E. E. Riding and S. M. Awramik (Berlin: Springer–Verlag), 25–31.

Krumbein, W. E. (1979). Photolithotrophic and chemoorganotrophic activity of bacteria and algae as related to beach rock formation and degradation (Gulf of Aqaba, Sinai), Geomicrobiol. J. 1, 139–203. doi: 10.1080/01490457909377729

CrossRef Full Text

Kumar, R., and Kumar, A. V. (1999). Biodeterioration of Stones in Tropical Environments. Los Angeles, CA: The Getty Conservation Institute.

Lal Gauri, K., Chowdhury, A. N., Kulshreshtha, N. P., and Punuru, A. R. (1989a). The sulfation of marble and the tteatment of gypsum crusts. Stud. Conserv. 34, 201–206. doi: 10.1179/sic.1989.34.4.201

CrossRef Full Text

Lal Gauri, K., Kulshreshtha, N., Punuru, A., and Chowdhury, A. (1989b). Rate of decay of marble in laboratory and outdoor exposure. J. Mater. Civ. Eng. 1, 73–85. doi: 10.1061/(ASCE)0899-1561(1989)1:2(73)

CrossRef Full Text

Lazzarini, L., and Laurenzi Tabasso, M. (1986). Il Restauro della Pietra. Padova: CEDAM.

Le Metayer-Levrel, G., Castanier, S., Orial, G., Loubiere, J. F., and Perthuisot, J. P. (1999). Applications of bacterial carbonatogenesis to the protection and regeneration of limestones in buildings and historic patrimony. Sediment. Geol. 126, 25–34. doi: 10.1016/S0037-0738(99)00029-9

CrossRef Full Text

Machel, H. G. (2001). Bacterial and thermochemical sulfate reduction in diagenetic setting. Sediment. Geol. 140, 143–175. doi: 10.1016/S0037-0738(00)00176-7

CrossRef Full Text

Maliva, R. G., Missimer, T. M., Leo, K. C., Statom, R. A., Dupraz, C., Lynn, M., et al. (2000). Unusual calcite stromatolites and pisoids from a landfill leachate collection system. Geology 28, 931–934. doi: 10.1130/0091-7613(2000)28<931:UCSAPF>2.0.CO;2

CrossRef Full Text

May, E. (2005). Biobrush Research Monograph: Novel Approaches to Conserve Our European Heritage. EVK4-CT-2001-00055, (France).

McConnaughey, T. A., and Whelan, J. F. (1997). Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci. Rev. 42, 95–117. doi: 10.1016/S0012-8252(96)00036-0

CrossRef Full Text

McNamara, C. J., and Mitchell, R. (2005). Microbial deterioration of historic stone. Fronti. Ecol. Envir. 3, 445–451. doi: 10.1890/1540-9295(2005)003[0445:MDOHS]2.0.CO;2

CrossRef Full Text

Morse, J. W. (1983). The kinetics of calcium carbonate dissolution and precipitation. Rev. Mineral. MSA Short Course 11, 227–264.

Moropoulou, A., Polikreti, K., Bakolas, A., and Michailidis, P. (2003). Correlation of physicochemical and mechanical properties of historical mortars and classification by multivariate statistics. Cement Concrete Res. 33, 891–898. doi: 10.1016/S0008-8846(02)01088-8

CrossRef Full Text

Orial, G. (2000). La Biomineralisation Appliquée à la Conservation du Patrimoine: Bilan de dix ans D'experimentation. Valladolid: Restaurar la Memoria,.

Orial, G., Castanier, S., Le Metayer, G., and Loubiere, J. F. (1992). “Biomineralization: a new process to protect calcareous stone; applied to historic monuments,” in Biodeterioration of Cultural Property 2: Proceedings of the 2nd International Conference on Biodeterioration of Cultural Property (Yokohama).

Orial, G., Vieweger, T., and Loubiere, J. F. (2002). Les Mortiers Biologiques: une Solution Pour la Conservation de la Sculpture Monumentale en Pierre. New York, NY: Art Biology and Conservation, Metropolitan Museum.

Packman, J. J., Comings, K. J., and Booth, D. B. (1999). “Using turbidity to determine total suspended solids in urbanizing streams in the Puget Lowlands,” in Confronting Uncertainty: Managing Change in Water Resources and the Environment (Vancouver, BC), 27–29.

Papida, S., Murphy, W., and May, E. (2000). “The use of sound velocity determination for the non-destructive estimation of physical and microbial weathering of limestones and dolomites,” in Proceedings of the 9th International Congress on deterioration and Conservation of Stone (Venice), 609–617.

Pentecost, A., and Bauld, J. (1988). Nucleation of calcite on the sheaths of cyanobacteria using a simple diffusion cell. Geomicrobiol. J. 6, 129–135. doi: 10.1080/01490458809377830

CrossRef Full Text

Perito, B., Biagiotti, L., Daly, S., Galizzi, A., Tiano, P., and Mastromei, G. (1999). “Bacterial genes involved in calcite crystal precipitation,” in Of Microbes and Art: The Role of Microbial Communities in the Degradation and Protection of Cultural Heritage, eds O. Ciferri, P. Tiano, and G. Mastromei (New York, NY: Plenum Publishers), 219–230.

Ramachandran, S. K., Ramakrishnan, V., and Bang, S. S. (2001). Remediation of Concrete using Microorganisms. ACI Mater. J. 98, 3–9.

Ramakrishnan, S. K., Panchalan, R. K., and Bang, S. S. (2001). “Improvement of concrete durability by bacterial mineral precipitation,” in Proceedings of 11th International Conference on Fracture (Turin).

Ramírez, J. L., Santana, M. A., Galindo-Castro, I., and Gonzalez, A. (2005). The role of biotechnology in art preservation. Trends Biotechnol. 23, 584–588. doi: 10.1016/j.tibtech.2005.10.004

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Ranalli, G., Chiavarini, M., Guidetti, V., Marsala, F., Matteini, M., Zanardini, E., et al. (1997). The use of microorganisms for the removal of sulphates on artistic stoneworks. Int. Biodeterior. Biodegrad. 40, 255–261. doi: 10.1016/S0964-8305(97)00054-1

CrossRef Full Text

Ranalli, G., Matteini, M., Tosini, I., Zanardini, E., and Sorlini, C. (1999). “Bioremediation of cultural heritage: removal of sulphates, nitrates and organic substances,” in Proceedings of International Conference on Microbiology and Conservation “Of Microbes and Art: The Role of Microbial Communities on the Degradation and Protection of Cultural Heritage,” eds O. Ciferri, P. Tiano, and G. Mastromei (Florence), 231–245.

Rawlings, D. E. (2005). Characteristics and adaptability of iron- and sulfuroxidizing microorganisms used for the recovery of metals from minerals and their concentrates. Microb. Cell Fact. 4, 13–28. doi: 10.1186/1475-2859-4-13

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Rivadeneyra, M. A. G., Delgado, A., Ramos-Cormenzana, A., and Delgado, R. (1998). Biomineralization of carbonates by Halomonas eurihalina in solid and liquid media with different salinities: crystal formation sequence. Res. Microbiol. 149, 277–287. doi: 10.1016/S0923-2508(98)80303-3

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Rivadeneyra, M. A., Parraga, J., Delgado, R., Ramos-Cormenzana, A., and Delgado, G. (2004). Biomineralization of carbonates by Halobacillus trueperi in solid and liquid media with different salinities. FEMS Microbiol. Ecol. 48, 39–46. doi: 10.1016/j.femsec.2003.12.008

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Rodriguez-Navarro, C., and Sebastian, E. (1996). Role of particulate matter from vehicle exhaust on porous building stones (limestone) sulfation. Sci. Total Environ. 187, 79–91. doi: 10.1016/0048-9697(96)05124-8

CrossRef Full Text

Rodriguez-Navarro, C., and Doehne, E. (1999). Salt weathering: influence of evaporation rate, supersaturation and crystallization pattern. Earth Surf. Process. Landf. 24, 191–209. doi: 10.1002/(SICI)1096-9837(199903)24:3<191::AID-ESP942>3.0.CO;2-G

CrossRef Full Text

Rodriguez-Navarro, C., Jimenez-Lopez, C., Rodriguez-Navarro, A., González-Muñoz, M. T. and Rodriguez-Gallego, M. (2007). Bacterially mediated mineralization of vaterite, Geochim. Cosmochim. Acta 71, 1197–1213. doi: 10.1016/j.gca.2006.11.031

CrossRef Full Text

Rodriguez-Navarro, C., Rodriguez-Gallego, M., Ben Chekroun, K., and Gonzalez-Munoz, M. T. (2003). Conservation of ornamental stone by Myxococcus xanthus induced carbonate biomineralization. Appl. Env. Microbiol. 69, 2182–2193. doi: 10.1128/AEM.69.4.2182-2193.2003

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Rosenbaum, M. S. (2006). Field Meeting Report: Bromfield Sand and Gravel Pit, ed Ed Webb (Shropshire: Ludlow).

Saiz-Jimenez, C. (1991). “Characterization of organic compounds in weathered stones,” in Science, Technology and European Cultural Heritage, eds N. S. Baer, C. Sabbioni, and A. I. Sots (Oxford: CEC, Butterworth-Heinemann), 523–526.

Saiz-Jimenez, C. (1997). Biodeterioration vs. biodegradation: the role of microorganisms in the removal of pollutants deposited on historic buidlings. Int. Biodeter. Biodegr. 40, 225–232. doi: 10.1016/S0964-8305(97)00035-8

CrossRef Full Text

Saiz-Jimenez, C., and Garcia del Cura, M. A. (1991). “Sulfated crusts: a microscopic, inorganic and organic analysis,” in Science, Technology and European Cultural Heritage, eds N. S. Baer, C. Sabbioni, and A. I. Sors (Oxford: CEC, Butterworth-Heinemann), 527–530.

Salvadori, O. (2003). The control of biodeterioration. Coalition 6, 16–20.

Shinano, H. (1972). Studies of marine microorganisms taking part in the precipitation of calcium carbonate. Bull. Jpn. Soc. Sci. Fish. 38:717. doi: 10.2331/suisan.38.717

CrossRef Full Text

Stocks-Fischer, S., Galinat, J. K., and Bang, S. S. (1999). Microbiological precipitation of CaCO3. Soil Biol. Biochem. 31, 1563–1571. doi: 10.1016/S0038-0717(99)00082-6

CrossRef Full Text

Stumm, W., and Morgan, J. J. (1981). Aquatic Chemistry, 2nd Edn. NewYork, NY: John Wiley.

Sutton, M., Reis, S., and Baker, S. (2008). “Atmospheric ammonia: detecting emission changes and environmental impact,” in Results of an Expert Workshop Under the Convention on Long-Range Transboundary Air Pollution, ed Samantha (Oxfordshire, UK: Springer), 490.

Tiano, P. (1995). Stone reinforcement by calcite crystal precipitation induced by organic matrix macromolecules. Stud. Conserv. 40, 171–176. doi: 10.1179/sic.1995.40.3.171

CrossRef Full Text

Tiano, P., Addadi, L., and Weiner, S. (1992). “Stone reinforcement by induction of calcite crystals using organic matrix macromolecules: feasibility study,” in 7th International Congress on Deterioration and Conservation of Stone (Lisbon), 1317–1326.

Tiano, P., Biagiotti, L., and Mastromei, G. (1999). Bacterial bio-mediated calcite precipitation for monumental stones conservation: methods of evaluation. J. Microbiol. Methods 36, 139–145. doi: 10.1016/S0167-7012(99)00019-6

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Tiano, P., Cantisani, E., Sutherland, I., and Paget, J. M. (2006). Biomediated reinforcement of weathered calcareous stones. J. Cult. Herit. 7, 49–55. doi: 10.1016/j.culher.2005.10.003

CrossRef Full Text

Tobler, D. J., Cuthbert, M. O., Greswell, R. B., Riley, M. S., Renshaw, J. C., Handley-Sidhu, S., et al. (2011). Comparison of rates of ureolysis between Sporosarcina pasteurii and an indigenous groundwater community under conditions required to precipitate large volumes of calcite. Geochim. Cosmochim. AC. 75, 3290–3301. doi: 10.1016/j.gca.2011.03.023

CrossRef Full Text

Wakefield, R., and Jones, M. (1998). An introduction to stone colonizing micro-organisms and biodeterioration of building stone. Q. J. Eng. Geol. 31, 301–313. doi: 10.1144/GSL.QJEG.1998.031.P4.03

CrossRef Full Text

Warscheid, T., and Braams, J. (2000). Biodeterioration of stone: a review. Int. Biod. Biodegr. 46, 343–368. doi: 10.1016/S0964-8305(00)00109-8

CrossRef Full Text

Warscheid, T., Oelting, M., and Krumbein, W. E. (1991). Physico-chemical aspects of biodeterioration processes on rocks with special regard to organic pollutants. Int. Biodet. 28, 37–48. doi: 10.1016/0265-3036(91)90032-M

CrossRef Full Text

Warthmann, R., Van Lith, Y., Vasconcelos, C., McKenzie, J. A., and Karpoff, M. (2000). Bacterially induced dolomite precipitation in anoxic culture experiments. Geol. 28, 1091–1094. doi: 10.1130/0091-7613(2000)28<1091:BIDPIA>2.0.CO;2

CrossRef Full Text

Wright, D. T. (1999). The role of sulphate-reducing bacteria and cyanobacteria in dolomite formation in distal ephemeral lakes of the Coorong region, South Australia. Sediment. Geol. 126, 147–157. doi: 10.1016/S0037-0738(99)00037-8

CrossRef Full Text

Zamarreno, D. V., Inkpen, R., and May, E. (2009). Carbonate crystals precipitated by freshwater bacteria and their use as a limestone consolidant. Appl. Environ. Microbiol. 75, 5981–5990. doi: 10.1128/AEM.02079-08

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text

Keywords: limestone, microbial carbonates, bacteria, urease, biofilm, extrapolymeric substances, calcite

Citation: Dhami NK, Reddy MS and Mukherjee A (2014) Application of calcifying bacteria for remediation of stones and cultural heritages. Front. Microbiol. 5:304. doi: 10.3389/fmicb.2014.00304

Received: 01 April 2014; Accepted: 03 June 2014;
Published online: 26 June 2014.

Edited by:

Edith Joseph, University of Neuchatel, Switzerland

Reviewed by:

Jun-Jie Zhang, Wuhan Institute of Virology, China
Jose M. Bruno-Barcena, North Carolina State University, USA

Copyright © 2014 Dhami, Reddy and Mukherjee. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: M. Sudhakara Reddy, Department of Biotechnology, Thapar University, Patiala 147004, Punjab, India e-mail: msreddy@thapar.edu

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.