Abstract
Precipitation of calcium carbonate minerals by bacteria, the so-called bacterial carbonatogenesis, is a promising method for the consolidation of decayed stone. Despite extensive laboratory testing that has demonstrated the efficacy of this method, little is, however, known regarding the medium- and/or long-term performance of this bacterial conservation treatment once applied in situ, on stone buildings. Here, we report on the evaluation of the performance of bacterial consolidation treatments applied in three different historical buildings placed in an urban environment and built using a highly porous, easily decayed calcarenite stone. Peeling tape tests show a significant long-lasting (up to four years) strength improvement following treatment with either a Myxococcus xanthus bacterial culture or a sterile nutritional solution that selectively activates the carbonatogenic bacteria inhabiting the stone. Total color changes, measured before and after treatment using a spectrophotometer, are systematically below the acceptable value of ΔE ≤ 5. Culture-dependent analysis of the microbiota shows that 100% of the culturable bacteria collected before and after treatment is carbonatogenic, and the total count of fungi spores remains constant or diminishes, while the population of acid-producing bacteria decreases over time after treatment application. Culture-independent microbial analyses show that no deleterious microbiota develops after treatment, being carbonate-producing Proteobacteria, Firmicutes and Actinobacteria the most abundant phyla both before and after treatment. Overall these results show that the in situ application of the bacterial consolidation method shows no detrimental side effects and is highly effective in the medium- and long-term.
Acknowledgments
This work was financially supported by the Spanish Government (Grant CGL2012-35992), the Junta de Andalucía (Research Groups RNM-179 and BIO-103, and Projects P11-RNM-7550 and P08-RNM-3943), and the Instituto FCICOP de Conservación y Restauración de Bienes Culturales (ICON-FCICOP). We thank the Centro de Instrumentación Científica (CIC; University of Granada) for assistance with SEM-EDS analyses. We thank E. Ruiz-Agudo for her help with the mapping of lithotypes and weathering forms of the Hospital Real, and J. Gallego Roca for kindly providing the blueprints of this building. We also thank the personnel of Tarma S.L. for their help during treatments application at the Capilla Real.
References
1. StrzelczykAB. Stone. In: RoseAH, editor. Microbial biodeterioration. London: Academic Press, 1981:61–80.Search in Google Scholar
2. DoehneE, PriceC. Stone conservation: an overview of current research, 2nd ed. Los Angeles, CA: The Getty Conservation Institute, 2010.Search in Google Scholar
3. SebastianE, Rodriguez-NavarroC. Alteración y conservación de materiales pétreos ornamentales: antecedentes y estado actual de conocimientos. Ingeniería Civil1995;96:167–78.Search in Google Scholar
4. Rodriguez-NavarroC, DoehneE. Salt weathering: influence of evaporation rate, supersaturation and crystallization pattern. Earth Surf Process Landforms1999;24:191–209.Search in Google Scholar
5. Rodriguez-NavarroC, SebastianE. Role of particulate matter from vehicle exhaust on porous building stones (limestone) sulfation. Sci Total Environ1996;187:79–91.Search in Google Scholar
6. Saiz-JimenezC. Biodeterioration of stone in historic buildings and monuments. In: LlewellynGC, editor. Biodeterioration research, vol. 4. New York: Plenum Press, 1994:587–604.Search in Google Scholar
7. WarscheidT, BraamsJ. Biodeterioration of stone: a review. Int Biodeter Biodegrad2000;46:343–68.Search in Google Scholar
8. WinklerEM. Stone in architecture. Berlin: Springer-Verlag, 1994.Search in Google Scholar
9. SmithBG, WhalleyB, FassinaV. Elusive solution to monumental decay. New Sci1988;118:49–53.Search in Google Scholar
10. LazzariniL, TabassoML. Il restauro della pietra. Padova: Cedam, 1986.Search in Google Scholar
11. HorieCV. Materials for conservation: organic consolidants, adhesives and coatings. London: Butterworths, 1987.Search in Google Scholar
12. ChelazziD, PoggiG, JaidarY, ToccafondiN, GiorgiR, BaglioniP. Hydroxide nanoparticles for cultural heritage: consolidation and protection of wall paintings and carbonate materials. J Colloid Interface Sci2013;392:42–9.Search in Google Scholar
13. GiorgiR, BaglioniM, BertiD, BaglioniP. New methodologies for the conservation of cultural heritage: micellar solutions, microemulsions, and hydroxide nanoparticles. Acc Chem Res2010;43:695–704.Search in Google Scholar
14. HansenE, DoehneE, FidlerJ, LarsonJ, MartinB, MatteiniM, et al. A review of selected inorganic consolidants and protective treatments for porous calcareous materials. Rev Conserv2003;4:13–25.Search in Google Scholar
15. Rodriguez-NavarroC, SuzukiA, Ruiz-AgudoE. Alcohol dispersions of calcium hydroxide nanoparticles for stone conservation. Langmuir2013;29:11457–70.Search in Google Scholar
16. PriceC, RossK, WhiteG. A further appraisal of the ‘lime technique’ for limestone consolidation, using a radioactive tracer. Stud Conserv1988;33:178–86.Search in Google Scholar
17. WheelerG. Alkoxysilanes and the consolidation of stone. Los Angeles, CA: The Getty Conservation Institute, 2005.Search in Google Scholar
18. MosqueraMJ, PozoJ, EsquiviasL. Stress during drying of two stone consolidants applied in monumental conservation. J Sol Gel Sci Technol2003;26:1227–31.Search in Google Scholar
19. CastanierS, Le Métayer-LevrelG, OrialG, LoubièreJF, PerthuisotJP. Bacterial carbonatogenesis and applications to preservation and restoration of historic property. In: CiferriO, TianoP, MastromeiG, editors. Of microbes and art: the role of microbial communities in the degradation and protection of cultural heritage. New York: Plenum, 2000:201–16.Search in Google Scholar
20. Rodriguez-NavarroC, Rodriguez-GallegoM, Ben ChekrounK, Gonzalez-MuñozMT. Conservation of ornamental stone by Myxococcus xanthus-induced carbonate biomineralization. Appl Environm Microbiol2003;69:2182–93.Search in Google Scholar
21. TianoP, BiagiottiL, MastromeiG. Bacterially bio-mediated calcite precipitation for monumental stones conservation: methods of evaluation. J Microbiol Methods1999;36:139–45.Search in Google Scholar
22. WebsterA, MayE. Bioremediation of weathered-building stone surfaces. Trends Biotechnol2006;24:255–60.Search in Google Scholar
23. De MuynckW, De BelieN, VerstraeteW. Microbial carbonate precipitation in construction materials: a review. Ecol Eng2010;36:118–36.Search in Google Scholar
24. ZamarreñoDV, InkpenR, MayE. Carbonate crystals precipitated by freshwater bacteria and their use as a limestone consolidant. Appl Environm Microbiol2009;75:5981–90.Search in Google Scholar
25. Gonzalez-MuñozMT. Bacterial biomineralization applied to the protection consolidation of ornamental stone: current development and perspectives. Coalition2008;15:12–18.Search in Google Scholar
26. Rodriguez-NavarroC, JroundiF, SchiroM, Ruiz-AgudoE, Gonzalez-MuñozMT. Influence of substrate mineralogy on bacterial mineralization of calcium carbonate: implications for stone conservation. Appl Environm Microbiol2012;78:4017–29.Search in Google Scholar
27. EhrlichHL. Geomicrobiology, 4th ed. New York: Marcel Dekker, 2002.Search in Google Scholar
28. Jimenez-LopezC, RomanekCS, BazylinskiDA. Magnetite as a prokaryotic biomarker: A review. J Geophys Res Biogeosci2010;115:2156–202.Search in Google Scholar
29. Rodriguez-NavarroC, Jimenez-LopezC, Rodriguez-NavarroA, Gonzalez-MuñozMT, Rodriguez-GallegoM. Bacterially mediated mineralization of vaterite. Geochim Cosmochim Acta2007;71:1197–213.Search in Google Scholar
30. González-MuñozMT, Rodriguez-NavarroC, Martínez-RuizF, AriasJM, MerrounML, Rodriguez-GallegoM. Bacterial biomineralization: new insights from myxococcus-induced mineral precipitation. Geol Soc London Sp Pub2011;336:31–50.Search in Google Scholar
31. JroundiF, Gonzalez-MuñozMT, Garcia-BuenoA, Rodriguez-NavarroC. Consolidation of archaeological gypsum plaster by bacterial biomineralization of calcium carbonate. Acta Biomater2014;10:3844–54.Search in Google Scholar
32. BoquetE, BoronatA, Ramos-CormenzanaA. Production of calcite (calcium carbonate) crystals by soil bacteria is a common phenomenon. Nature1973;246:527–9.Search in Google Scholar
33. CastanierS, Le Métayer-LevrelG, PerthuisotJP. Ca-carbonates precipitation and limestone genesis – the microbiologist point of view. Sediment Geol1999;126:9–23.Search in Google Scholar
34. OrialG, CastanierS, Le Métayer-LevrelG, LoubiereJF. The biomineralization: a new process to protect calcareous stone applied to historic monuments. In: KtoishiH, AraiT, YamanoK, editors. Proceeding of the 2nd international conference on biodeterioration of cultural property. Yokohama: Yamano, 1993:98–116.Search in Google Scholar
35. Rodriguez-NavarroC, Gonzalez-MuñozMT, Jimenez-LopezC, Rodriguez-GallegoM. Bioprotection. In: ReitnerJ, ThielV, editors. Encyclopedia of Geobiology. Berlin: Springer, 2011:185–9.Search in Google Scholar
36. Jimenez-LopezC, Rodriguez-NavarroC, PiñarG, Carrillo-RosúaFJ, Rodriguez-GallegoM, Gonzalez-MuñozMT. Consolidation of degraded ornamental porous limestone by calcium carbonate precipitation induced by the microbiota inhabiting the stone. Chemosphere2007;68:1929-36.Search in Google Scholar
37. Jimenez-LopezC, JroundiF, PascoliniC, Rodriguez-NavarroC, PiñarG, Rodriguez-GallegoM, et al. Consolidation of quarry calcarenite by calcium carbonate precipitation induced by bacteria activated among the microbiota inhabiting the stone. Int Biodeter Biodegrad2008;62:352–63.Search in Google Scholar
38. Gonzalez-MuñozMT, Rodriguez-NavarroC, Jimenez-LopezC, Rodriguez-GallegoM. Method and product for protecting and reinforcing construction and ornamental materials. Spanish patent WO 2008/009771 A1; 2008.Search in Google Scholar
39. JroundiF, Fernandez-VivasA, Rodriguez-NavarroC, BedmarEJ, Gonzalez-MuñozMT. Bioconservation of deteriorated monumental calcarenite stone and identification of bacteria with carbonatogenic activity. Microb Ecol2010;60:39–54.Search in Google Scholar
40. EttenauerJ, PiñarG, SterlingerK, Gonzalez-MuñozF, JroundiF. Molecular monitoring of the microbial dynamics occurring on historical limestone buildings during and after the in situ application of different bio-consolidation treatments. Sci Total Environm2011;409:5337–52.Search in Google Scholar
41. Rodriguez-NavarroC. Causas y mecanismos de alteración de los materiales calcáreos de las catedrales de Granada y Jaén. PhD Thesis. Granada: University of Granada; 1994.Search in Google Scholar
42. JroundiF, Gonzalez-MuñozMT, Rodriguez-NavarroC, Martin-PeinadoB, Martin-PeinadoJ. Conservation of carbonate stone by means of bacterial carbonatogenesis: evaluation of in situ treatments. In: KouiM, KoutsoukosP, ZezzaF, editors. Proceedings of the 8th international symposium on the conservation of monuments in the Mediterranean basin. Patras: Technical Chamber of Greece, 2013:159–71.Search in Google Scholar
43. DráckýM, LesákJ, RescicS, SlízkováZ, TianoP, ValachJ. Standardization of peeling tests for assessing the cohesion and consolidation characteristics of historic stone surfaces. Mater Struc2012;45:505–20.Search in Google Scholar
44. BenaventeD, Martinez-VerdúF, BernabeuA, VigueiraV, FortR, García del CuraMA, et al. Influence of surface roughness on color changes in building stones. Color Res Appl2003;28:343–51.Search in Google Scholar
45. HughR, LeifsonE. The taxonomic significance of fermentative versus oxidative metabolism of carbohydrates by various gram-negative rods. J Bacteriol1953;66:24–6.Search in Google Scholar
46. SorianoS, WalkerN. Isolation of ammonia-oxidizing autotrophic bacteria. J Bacteriol1968;31:493–7.Search in Google Scholar
47. AleenMIH, AalexanderM. Cell-free nitrification by nitrobacter. J Bacteriol1958;76:510–14.Search in Google Scholar
48. JohnsonW, PeckHD. Coupling of phosphorylation and carbon dioxide fixation in extracts of thiobacillus thioparus. J Bacteriol1965;89:1041–50.Search in Google Scholar
49. Schabereiter-GurtnerC, PiñarG, LubitzW, RöllekeS. An advanced molecular strategy to identify bacterial communities on art objects. J Microbiol Methods2001;45:77–87.Search in Google Scholar
50. Le Métayer-LevrelG, CastanierS, OrialG, LoubièreJF, PerthuisotJP. Applications of bacterial carbonatogenesis to the protection and regeneration of limestones in buildings and historic patrimony. Sedimentary Geol1999;126:25–34.Search in Google Scholar
51. SasseHR, SnethlageR. Methods for the evaluation of stone conservation treatments. In: BaerNS, SnethlageR, editors. Saving our architectural heritage: the conservation of historic stone structures. New York: John Wiley & Sons, 1997:223–43.Search in Google Scholar
52. AdolpheJP, LoubièreJF, ParadasJ, SoleilhavoupF. Procédé de traitement biologique d’une surface artificielle. European patent 90400G97.0; 1990.Search in Google Scholar
53. UrziC, Garcia-VallesM, VendrellM, PerniceA. Biomineralization processes on rock and monument surfaces observed in field and laboratory conditions. Geomicrobiol J1999;16:39–54.Search in Google Scholar
54. Ortega-MoralesBO. Cyanobacterial diversity and ecology on historic monuments in Latin America. Rev Latinoam Microbiol2006;48:188–95.Search in Google Scholar
55. GaylardeCC, RodríguezCH, Navarro-NoyaYE, Ortega-MoralesB. Microbial biofilms on the sandstone monuments of the Angkor Wat complex, Cambodia. Curr Microbiol2012;64:85–92.Search in Google Scholar
56. YanF, GeQ, LiQ, YuM, ZhuX, PanJ. Analysis of microbial community on the surface of the historic stone and nearby rock samples in Yungang Grottoes. Acta Microbiol Sinica2012;52:629–36.Search in Google Scholar
©2015 by Birkhäuser Verlag
Articles in the same Issue
- Frontmatter
- Editorial Note
- The Relevance of Maintenance and Monitoring in Architectural Conservation
- Stone Consolidation by Bacterial Carbonatogenesis: Evaluation of in situ Applications
- Subjective Sensation of Color Differences – Determination of Thresholds Depending on Color Tones and Resolution
- Consolidation and Strengthening of Historical Masonry by Means of Mineral Grouts: Grout Development
- Consolidation and Strengthening of Historical Masonry by Means of Mineral Grouts: Modeling Structural Behavior of Grouted Three-Leaf Masonry
Articles in the same Issue
- Frontmatter
- Editorial Note
- The Relevance of Maintenance and Monitoring in Architectural Conservation
- Stone Consolidation by Bacterial Carbonatogenesis: Evaluation of in situ Applications
- Subjective Sensation of Color Differences – Determination of Thresholds Depending on Color Tones and Resolution
- Consolidation and Strengthening of Historical Masonry by Means of Mineral Grouts: Grout Development
- Consolidation and Strengthening of Historical Masonry by Means of Mineral Grouts: Modeling Structural Behavior of Grouted Three-Leaf Masonry