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Microbial deterioration and sustainable conservation of stone monuments and buildings

Nature Sustainability volume 3, pages 991–1004 (2020)Cite this article

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Abstract

Geomicrobially induced deterioration of stone monuments and buildings contributes to a considerable loss of world cultural heritage, especially when exposed to a changing climate or environment. The active biodeterioration processes typically involve biochemical activities and cooperation among functional microorganisms in epilithic biofilms, which assimilate mineral nutrients and metabolize anthropogenic pollutants through biogeochemical cycles. Development of any effective mitigation strategies requires the comprehensive understanding of such processes. We focus on how microbes contribute to the biodeterioration processes through their activities and biogeochemical cycles of elements, discuss biochemical mechanisms involved and provide innovative strategies for sustainable conservation of stone monuments and buildings.

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Fig. 1: Examples of biodeterioration of cultural heritage caused by microbial colonization.

J.-D.G. and X.L. (a–k)

Fig. 2: Formation and succession of epilithic biofilms on the stone surface.
Fig. 3: Human activities and biogeochemical cycles associated with the biodeterioration of stone heritage.

J.-D.G. and X.L

Fig. 4: Mechanisms of the biodeterioration of stone materials.

J.-D.G. and X.L

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References

  1. Dornieden, T., Gorbushina, A. & Krumbein, W. Biodecay of cultural heritage as a space/time-related ecological situation—an evaluation of a series of studies. Int. Biodeterior. Biodegrad. 46, 261–270 (2000).

    CAS  Google Scholar 

  2. Warscheid, T. et al. Studies on the temporal development of microbial infection of different types of sedimentary rocks and its effect on the alteration of the physico-chemical properties in building materials. In Conservation of stone and other materials: Proc. of the International RILEM/UNESCO congress held at the UNESCO headquarters (ed. Thiel, M.-J.) 303–310 (E. & F.N. Spon Ltd, 1993).

  3. Gadd, G. M. Geomicrobiology of the built environment. Nat. Microbiol. 2, 16275 (2017).

    CAS  Google Scholar 

  4. Pinna, D. Coping with Biological Growth on Stone Heritage Objects: Methods, Products, Applications, and Perspectives (Apple Academic Press, 2017).

  5. Onofri, S., Zucconi, L., Isola, D. & Selbmann, L. Rock-inhabiting fungi and their role in deterioration of stone monuments in the Mediterranean area. Plant Biosyst. 148, 384–391 (2014).

    Google Scholar 

  6. Villa, F., Stewart, P. S., Klapper, I., Jacob, J. M. & Cappitelli, F. Subaerial biofilms on outdoor stone monuments: changing the perspective toward an ecological framework. BioScience 66, 285–294 (2016).

    Google Scholar 

  7. Warscheid, T. & Braams, J. Biodeterioration of stone: a review. Int. Biodeterior. Biodegrad. 46, 343–368 (2000).

    CAS  Google Scholar 

  8. Saiz-Jimenez, C. Biogeochemistry of weathering processes in monuments. Geomicrobiol. J. 16, 27–37 (1999).

    CAS  Google Scholar 

  9. Chen, J., Blume, H.-P. & Beyer, L. Weathering of rocks induced by lichen colonization — a review. Catena 39, 121–146 (2000).

    CAS  Google Scholar 

  10. Martino, P. D. What about biofilms on the surface of stone monuments? Open Conf. Proc. J. 6, 14–28 (2016).

    Google Scholar 

  11. Gu, J.-D., Ford, T. E. & Mitchell, R. in Uhlig’s Corrosion Handbook 3rd edn (ed. Revie, R. W.) 351–363 (Wiley, 2011).

  12. Polynov, B. The first stages of soil formation on massive crystaline rocks. Pochvovedeniye 7, 325–339 (1945).

    Google Scholar 

  13. Vernadskiy, V. Geochemical Essays (Ocherki geokhimii) (Leningrad State Publishing House, 1927).

  14. Krasil’nikov, N. The role of microorganisms in the weathering of rocks. Mikrobiologiya 18, 318–323 (1949).

    Google Scholar 

  15. Yarilova, Y. A. The role of lithophilous lichens in the weathering of massive crystalline rocks. Pochvovedeniye 3, 533–548 (1947).

    Google Scholar 

  16. Pochon, J., Tardieux, P., Lajudie, J. & Charpentier, M. Degradation des temples d’Angkor et processus biologiques. Ann. Inst. Pasteur 98, 457–461 (1960).

    Google Scholar 

  17. Pochon, J. & Jaton, C. in Biodeterioration of Materials (eds. Wolters, A. H. & Elphich, C. C.) 258–268 (Elsevier, 1968).

  18. Pochon, J. & Jaton, C. The role of microbiological agencies in the deterioration of stone. Chem. Ind. 9, 1587–1589 (1967).

    Google Scholar 

  19. Paquet, J. Contribution a l’etude de la maladie de la pierre: new hypothese sur les causes des transferts et des concentrations de sulfate produisant les effets foliants. Mon. His. France 10, 73–88 (1964).

    Google Scholar 

  20. Hueck, H. in Biodeterioration of Materials. Microbiological and Allied Aspects (eds Walters, A. H. & Elphick, J. J.) 6–12 (Elsevier Publishing Co. Ltd, 1968).

  21. Gaylarde, P. & Gaylarde, C. Deterioration of siliceous stone monuments in Latin America: microorganisms and mechanisms. Corros. Rev. 22, 395–416 (2004).

    CAS  Google Scholar 

  22. Uchida, E., Ogawa, Y., Maeda, N. & Nakagawa, T. Deterioration of stone materials in the Angkor monuments, Cambodia. Eng. Geol. 55, 101–112 (2000).

    Google Scholar 

  23. Caneva, G., Bartoli, F., Savo, V., Futagami, Y. & Strona, G. Combining statistical tools and ecological assessments in the study of biodeterioration patterns of stone temples in Angkor (Cambodia). Sci. Rep. 6, 32601 (2016).

    CAS  Google Scholar 

  24. Meng, H., Katayama, Y. & Gu, J.-D. More wide occurrence and dominance of ammonia-oxidizing archaea than bacteria at three Angkor sandstone temples of Bayon, Phnom Krom and Wat Athvea in Cambodia. Int. Biodeterior. Biodegrad. 117, 78–88 (2017).

    CAS  Google Scholar 

  25. Zammit, G., Sánchez-Moral, S. & Albertano, P. Bacterially mediated mineralisation processes lead to biodeterioration of artworks in Maltese catacombs. Sci. Total Environ. 409, 2773–2782 (2011).

    CAS  Google Scholar 

  26. McNamara, C. J., Perry, T. D., Bearce, K. A., Hernandez-Duque, G. & Mitchell, R. Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. Microb. Ecol. 51, 51–64 (2006).

    Google Scholar 

  27. Ortega-Morales, B. O. et al. Bioweathering potential of cultivable fungi associated with semi-arid surface microhabitats of Mayan buildings. Front. Microbiol. 7, 201 (2016).

    Google Scholar 

  28. Cappitelli, F., Principi, P., Pedrazzani, R., Toniolo, L. & Sorlini, C. Bacterial and fungal deterioration of the Milan Cathedral marble treated with protective synthetic resins. Sci. Total Environ. 385, 172–181 (2007).

    CAS  Google Scholar 

  29. Rosado, T. et al. Pink! Why not? On the unusual colour of Évora Cathedral. Int. Biodeterior. Biodegrad. 94, 121–127 (2014).

    CAS  Google Scholar 

  30. Schiavon, N. et al. A multianalytical approach to investigate stone biodeterioration at a UNESCO world heritage site: the volcanic rock-hewn churches of Lalibela, Northern Ethiopia. Appl. Phys. A 113, 843–854 (2013).

    CAS  Google Scholar 

  31. Guillitte, O. Bioreceptivity: a new concept for building ecology studies. Sci. Total Environ. 167, 215–220 (1995).

    CAS  Google Scholar 

  32. Warscheid, T. & Leisen, H. in Biocolonization of Stone: Control and Preventive Methods: Proceedings from the MCI Workshop Series (eds Charola, A. E. et al.) 1–18 (Smithsonian Institution Scholarly Press, 2011).

  33. Warscheid, T., Oelting, M. & Krumbein, W. E. Physico-chemical aspects of biodeterioration processes on rocks with special regard to organic pollutants. Int. Biodeterior. Biodegrad. 28, 37–48 (1991).

    CAS  Google Scholar 

  34. Haack, T. K. & McFeters, G. A. Nutritional relationships among microorganisms in an epilithic biofilm community. Microb. Ecol. 8, 115–126 (1982).

    CAS  Google Scholar 

  35. Liu, X., Meng, H., Wang, Y., Katayama, Y. & Gu, J.-D. Water is a critical factor in evaluating and assessing microbial colonization and destruction of Angkor sandstone monuments. Int. Biodeterior. Biodegrad. 133, 9–16 (2018).

    CAS  Google Scholar 

  36. Prieto, B. & Silva, B. Estimation of the potential bioreceptivity of granitic rocks from their intrinsic properties. Int. Biodeterior. Biodegrad. 56, 206–215 (2005).

    CAS  Google Scholar 

  37. Miller, A. Z. et al. Bioreceptivity of building stones: a review. Sci. Total Environ. 426, 1–12 (2012).

    CAS  Google Scholar 

  38. Warscheid, T. et al. Biodeterioration studies on soapstone, quartzite & sandstones of historical monuments in Brazil and Germany. Preliminary results and evaluation for restoration practices. In Proc. of the 7th International Congress on Deterioration and Conservation of Stone 491–500 (Laboratório Nacional de Engenharia Civil, 1992).

  39. Beck, K., Al-Mukhtar, M., Rozenbaum, O. & Rautureau, M. Characterization, water transfer properties and deterioration in tuffeau: building material in the Loire valley—France. Build. Environ. 38, 1151–1162 (2003).

    Google Scholar 

  40. Sousa, L. M. O., Suárez del Río, L. M., Calleja, L., Ruiz de Argandoña, V. G. & Rey, A. R. Influence of microfractures and porosity on the physico-mechanical properties and weathering of ornamental granites. Eng. Geol. 77, 153–168 (2005).

    Google Scholar 

  41. Koestler, R., Warscheid, T. & Nieto, F. in Saving our Architectural Heritage: The Conservation of Historic Stone Structures (eds Baer, N. S. & Snethlage, R.) 25–36 (Wiley, 1997).

  42. Miller, A. Z., Dionísio, A., Laiz, L., Macedo, M. F. & Saiz-Jimenez, C. The influence of inherent properties of building limestones on their bioreceptivity to phototrophic microorganisms. Ann. Microbiol. 59, 705–713 (2009).

    CAS  Google Scholar 

  43. Tiano, P., Accolla, P. & Tomaselli, L. Phototrophic biodeteriogens on lithoid surfaces: an ecological study. Microb. Ecol. 29, 299–309 (1995).

    CAS  Google Scholar 

  44. Vázquez-Nion, D., Silva, B. & Prieto, B. Influence of the properties of granitic rocks on their bioreceptivity to subaerial phototrophic biofilms. Sci. Total Environ. 610–611, 44–54 (2018).

    Google Scholar 

  45. Miller, A., Dionísio, A. & Macedo, M. F. Primary bioreceptivity: a comparative study of different Portuguese lithotypes. Int. Biodeterior. Biodegrad. 57, 136–142 (2006).

    CAS  Google Scholar 

  46. Hunt, J. M. Distribution of hydrocarbons in sedimentary rocks. Geochim. Cosmochim. Acta 22, 37–49 (1961).

    CAS  Google Scholar 

  47. Carter, N. & Viles, H. Lichen hotspots: raised rock temperatures beneath Verrucaria nigrescens on limestone. Geomorphology 62, 1–16 (2004).

    Google Scholar 

  48. Castanier, S., Le Métayer-Levrel, G. & Perthuisot, J.-P. Ca-carbonates precipitation and limestone genesis—the microbiogeologist point of view. Sediment. Geol. 126, 9–23 (1999).

    CAS  Google Scholar 

  49. Leavengood, P., Twilley, J. & Asmus, J. F. Lichen removal from Chinese Spirit Path figures of marble. J. Cult. Herit. 1, S71–S74 (2000).

    Google Scholar 

  50. Gu, J.-D., Ford, T. E. & Mitchell, R. in Uhlig’s Corrosion Handbook 3rd edn (ed. Revie, R. W.) 451–460 (Wiley, 2011).

  51. Roig, P. B., Regidor Ros, J. L. & Estellés, R. M. Biocleaning of nitrate alterations on wall paintings by Pseudomonas stutzeri. Int. Biodeterior. Biodegrad. 84, 266–274 (2013).

    CAS  Google Scholar 

  52. Šimonovičová, A., Gódyová, M. & Ševc, J. Airborne and soil microfungi as contaminants of stone in a hypogean cemetery. Int. Biodeterior. Biodegrad. 54, 7–11 (2004).

    Google Scholar 

  53. Lan, W., Li, H., Wang, W.-D., Katayama, Y. & Gu, J.-D. Microbial community analysis of fresh and old microbial biofilms on Bayon Temple Sandstone of Angkor Thom, Cambodia. Microb. Ecol. 60, 105–115 (2010).

    Google Scholar 

  54. Bartoli, F. et al. Biological colonization patterns on the ruins of Angkor temples (Cambodia) in the biodeterioration vs bioprotection debate. Int. Biodeterior. Biodegrad. 96, 157–165 (2014).

    Google Scholar 

  55. Xu, H.-B. et al. Lithoautotrophical oxidation of elemental sulfur by fungi including Fusarium solani isolated from sandstone Angkor temples. Int. Biodeterior. Biodegrad. 126, 95–102 (2018).

    CAS  Google Scholar 

  56. Kusumi, A., Li, X. S. & Katayama, Y. Mycobacteria isolated from Angkor monument sandstones grow chemolithoautotrophically by oxidizing elemental sulfur. Front. Microbiol. 2, 104 (2011).

    CAS  Google Scholar 

  57. Caneva, G. et al. Exploring ecological relationships in the biodeterioration patterns of Angkor temples (Cambodia) along a forest canopy gradient. J. Cult. Herit. 16, 728–735 (2015).

    Google Scholar 

  58. Kemmling, A., Kämper, M., Flies, C., Schieweck, O. & Hoppert, M. Biofilms and extracellular matrices on geomaterials. Environ. Geol. 46, 429–435 (2004).

    CAS  Google Scholar 

  59. Gaylarde, C. C., Rodríguez, C. H., Navarro-Noya, Y. E. & Ortega-Morales, B. O. Microbial biofilms on the sandstone monuments of the Angkor Wat complex, Cambodia. Curr. Microbiol. 64, 85–92 (2012).

    CAS  Google Scholar 

  60. Nuhoglu, Y. et al. The accelerating effects of the microorganisms on biodeterioration of stone monuments under air pollution and continental-cold climatic conditions in Erzurum, Turkey. Sci. Total Environ. 364, 272–283 (2006).

    CAS  Google Scholar 

  61. Gaylarde, C. et al. Epilithic and endolithic microorganisms and deterioration on stone church facades subject to urban pollution in a sub-tropical climate. Biofouling 33, 113–127 (2017).

    Google Scholar 

  62. Mansch, R. & Bock, E. Biodeterioration of natural stone with special reference to nitrifying bacteria. Biodegradation 9, 47–64 (1998).

    CAS  Google Scholar 

  63. Viles, H. A. Implications of future climate change for stone deterioration. Geol. Soc. Lond. Spec. Publ. 205, 407–418 (2002).

    Google Scholar 

  64. Moroni, B. & Pitzurra, L. Biodegradation of atmospheric pollutants by fungi: a crucial point in the corrosion of carbonate building stone. Int. Biodeterior. Biodegrad. 62, 391–396 (2008).

    CAS  Google Scholar 

  65. Saiz-Jimenez, C. Biodeterioration vs biodegradation: the role of microorganisms in the removal of pollutants deposited on historic buidlings. Int. Biodeterior. Biodegrad. 40, 225–232 (1997).

    CAS  Google Scholar 

  66. Mitchell, R. & Gu, J.-D. Changes in the biofilm microflora of limestone caused by atmospheric pollutants. Int. Biodeterior. Biodegrad. 46, 299–303 (2000).

    CAS  Google Scholar 

  67. Stefanis, N.-A., Theoulakis, P. & Pilinis, C. Dry deposition effect of marine aerosol to the building stone of the medieval city of Rhodes, Greece. Build. Environ. 44, 260–270 (2009).

    Google Scholar 

  68. Leysen, L., Roekens, E. & Van Grieken, R. Air-pollution-induced chemical decay of a sandy-limestone Cathedral in Belgium. Sci. Total Environ. 78, 263–287 (1989).

    CAS  Google Scholar 

  69. Duan, Y. et al. The microbial community characteristics of ancient painted sculptures in Maijishan Grottoes, China. PLoS ONE 12, e0179718 (2017).

    Google Scholar 

  70. Bakr, A. & El Hafez, M. A. Role assessment of bat excretions in degradation of painted surface from Mohamed Ali’s palace, Suez, Egypt. Egypt. J. Archaeol. Restor. Stud. 3, 47–56 (2012).

    Google Scholar 

  71. Wierzchos, J. et al. Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the Atacama Desert. Front. Microbiol. 6, 934 (2015).

    Google Scholar 

  72. Aviam, O., Bar-Nes, G., Zeiri, Y. & Sivan, A. Accelerated biodegradation of cement by sulfur-oxidizing bacteria as a bioassay for evaluating immobilization of low-level radioactive waste. Appl. Environ. Microbiol. 70, 6031–6036 (2004).

    CAS  Google Scholar 

  73. Vupputuri, S. et al. Isolation of a sulfur-oxidizing Streptomyces sp. from deteriorating bridge structures and its role in concrete deterioration. Int. Biodeterior. Biodegrad. 97, 128–134 (2015).

    CAS  Google Scholar 

  74. Sand, W. & Bock, E. Biodeterioration of mineral materials by microorganisms—biogenic sulfuric and nitric acid corrosion of concrete and natural stone. Geomicrobiol. J. 9, 129–138 (1991).

    CAS  Google Scholar 

  75. Salvadori, O. & Municchia, A. C. The role of fungi and lichens in the biodeterioration of stone monuments. Open Conf. Proc. J. 7, 39–54 (2016).

    CAS  Google Scholar 

  76. Meng, H., Luo, L., Chan, H. W., Katayama, Y. & Gu, J.-D. Higher diversity and abundance of ammonia-oxidizing archaea than bacteria detected at the Bayon Temple of Angkor Thom in Cambodia. Int. Biodeterior. Biodegrad. 115, 234–243 (2016).

    CAS  Google Scholar 

  77. Daims, H. et al. Complete nitrification by Nitrospira bacteria. Nature 528, 504–509 (2015).

    CAS  Google Scholar 

  78. Gu, J.-D. & Katayama, Y. A microbiological challenge in protection of the sandstone Angkor monuments in Cambodia. IIC Newsletter (15 December 2017).

  79. Gu, J.-D., Ford, T. E., Berke, N. S. & Mitchell, R. Biodeterioration of concrete by the fungus Fusarium. Int. Biodeterior. Biodegrad. 41, 101–109 (1998).

    Google Scholar 

  80. Li, X. S. et al. Oxidation of elemental sulfur by Fusarium solani strain THIF01 harboring endobacterium Bradyrhizobium sp. Microb. Ecol. 60, 96–104 (2010).

    CAS  Google Scholar 

  81. Li, X., Arai, H., Shimoda, I., Kuraishi, H. & Katayama, Y. Enumeration of sulfur-oxidizing microorganisms on deteriorating stone of the Angkor monuments, Cambodia. Microbes Environ. 23, 293–298 (2008).

    Google Scholar 

  82. Bourcart, J., Noetzlin, J., Pochon, J. & Berthelier, S. Etude des détériorations des pierres des monuments historiques. In Annales de l’Institut Technique de Bâtiment et des Travaux Publics 1–16 (1949).

  83. Lepidi, A. & Schippa, G. Some aspects of the growth of chemotrophic and heterotrophic microorganisms on calcareous surfaces. In Colloque international sur la deterioration des pierres en oeuvre. 1er. International symposium on the deterioration of building stones 143–148 (Les Imprimerie Reunites de Chambery, 1973).

  84. Barcellona Vero, L. & Monte Sila, M. Isolation of various sulphur-oxidizing bacteria from stone monuments. In The conservation of stone i. Proceedings of the international symposium (ed. Rossi-Manaresi, R.) 233–244 (Centro per la conservazione delle sculture all’aperto, 1976).

  85. Tarantino, M. M. S.-G. The metabolic state of microorganisms of the genus Thiobacillus on stone monuments. In The Conservation of stone II: preprints of the contributions to the international symposium 117–138 (Centro per la conservazione delle sculture all’aperto, 1981).

  86. Milde, K., Sand, W., Wolff, W. & Bock, E. Thiobacilli of the corroded concrete walls of the Hamburg sewer system. Microbiology 129, 1327–1333 (1983).

    Google Scholar 

  87. Krumbein, W. E. Photolithotropic and chemoorganotrophic activity of bacteria and algae as related to beachrock formation and degradation (gulf of Aqaba, Sinai). Geomicrobiol. J. 1, 139–203 (1979).

    CAS  Google Scholar 

  88. Suzuki, D., Li, Z., Cui, X., Zhang, C. & Katayama, A. Reclassification of Desulfobacterium anilini as Desulfatiglans anilini comb. nov. within Desulfatiglans gen. nov., and description of a 4-chlorophenol-degrading sulfate-reducing bacterium, Desulfatiglans parachlorophenolica sp. nov. Int. J. Syst. Evol. Microbiol. 64, 3081–3086 (2014).

    CAS  Google Scholar 

  89. Kleindienst, S. et al. Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. ISME J. 8, 2029–2044 (2014).

    CAS  Google Scholar 

  90. Griffin, P., Indictor, N. & Koestler, R. The biodeterioration of stone: a review of deterioration mechanisms, conservation case histories, and treatment. Int. Biodeterior. Biodegrad. 28, 187–207 (1991).

    Google Scholar 

  91. Gaylarde, P., Englert, G., Ortega-Morales, O. & Gaylarde, C. Lichen-like colonies of pure Trentepohlia on limestone monuments. Int. Biodeterior. Biodegrad. 58, 119–123 (2006).

    CAS  Google Scholar 

  92. Isola, D. et al. Extremotolerant rock inhabiting black fungi from Italian monumental sites. Fungal Divers. 76, 75–96 (2016).

    Google Scholar 

  93. Suihko, M.-L. et al. Characterization of aerobic bacterial and fungal microbiota on surfaces of historic Scottish monuments. Syst. Appl. Microbiol. 30, 494–508 (2007).

    CAS  Google Scholar 

  94. Morillas, H. et al. Characterization of the main colonizer and biogenic pigments present in the red biofilm from La Galea Fortress sandstone by means of microscopic observations and Raman imaging. Microchem. J. 121, 48–55 (2015).

    CAS  Google Scholar 

  95. Hu, H. et al. Occurrence of Aspergillus allahabadii on sandstone at Bayon temple, Angkor Thom, Cambodia. Int. Biodeterior. Biodegrad. 76, 112–117 (2013).

    CAS  Google Scholar 

  96. ElBaghdady, K. Z., Tolba, S. T. & Houssien, S. S. Biogenic deterioration of Egyptian limestone monuments: treatment and conservation. J. Cult. Herit. 38, 118–125 (2019).

    Google Scholar 

  97. Gonzalez-Pimentel, J. L. et al. Yellow coloured mats from lava tubes of La Palma (Canary Islands, Spain) are dominated by metabolically active Actinobacteria. Sci. Rep. 8, 1944 (2018).

    Google Scholar 

  98. Garty, J. Influence of epilithic microorganisms on the surface temperature of building walls. Can. J. Bot. 68, 1349–1353 (1990).

    Google Scholar 

  99. Sterflinger, K. Fungi: their role in deterioration of cultural heritage. Fungal Biol. Rev. 24, 47–55 (2010).

    Google Scholar 

  100. Ortega-Morales, B. O., Gaylarde, C. C., Englert, G. E. & Gaylarde, P. M. Analysis of salt-containing biofilms on limestone buildings of the Mayan culture at Edzna, Mexico. Geomicrobiol. J. 22, 261–268 (2005).

    CAS  Google Scholar 

  101. Cappitelli, F. et al. Improved methodology for bioremoval of black crusts on historical stone artworks by use of sulfate-reducing bacteria. Appl. Environ. Microbiol. 72, 3733–3737 (2006).

    CAS  Google Scholar 

  102. Vincke, E. et al. Influence of polymer addition on biogenic sulfuric acid attack of concrete. Int. Biodeterior. Biodegrad. 49, 283–292 (2002).

    CAS  Google Scholar 

  103. De Windt, L. & Devillers, P. Modeling the degradation of Portland cement pastes by biogenic organic acids. Cem. Concr. Res. 40, 1165–1174 (2010).

    Google Scholar 

  104. Turkington, A. V. & Paradise, T. R. Sandstone weathering: a century of research and innovation. Geomorphology 67, 229–253 (2005).

    Google Scholar 

  105. Rossi, F. et al. Characteristics and role of the exocellular polysaccharides produced by five cyanobacteria isolated from phototrophic biofilms growing on stone monuments. Biofouling 28, 215–224 (2012).

    CAS  Google Scholar 

  106. Li, W.-W. & Yu, H.-Q. Insight into the roles of microbial extracellular polymer substances in metal biosorption. Bioresour. Technol. 160, 15–23 (2014).

    CAS  Google Scholar 

  107. Stone, A. T. Microbial metabolites and the reductive dissolution of manganese oxides: oxalate and pyruvate. Geochim. Cosmochim. Acta 51, 919–925 (1987).

    CAS  Google Scholar 

  108. Monte, M. Oxalate film formation on marble specimens caused by fungus. J. Cult. Herit. 4, 255–258 (2003).

    Google Scholar 

  109. Cariati, F., Rampazzi, L., Toniolo, L. & Pozzi, A. Calcium oxalate films on stone surfaces: experimental assessment of the chemical formation. Stud. Conserv. 45, 180–188 (2000).

    CAS  Google Scholar 

  110. Scherer, G. W. Stress from crystallization of salt. Cem. Concr. Res. 34, 1613–1624 (2004).

    CAS  Google Scholar 

  111. Saiz-Jimenez, C. & Laiz, L. Occurrence of halotolerant/halophilic bacterial communities in deteriorated monuments. Int. Biodeterior. Biodegrad. 46, 319–326 (2000).

    CAS  Google Scholar 

  112. Favero-Longo, S. E., Borghi, A., Tretiach, M. & Piervittori, R. In vitro receptivity of carbonate rocks to endolithic lichen-forming aposymbionts. Mycol. Res. 113, 1216–1227 (2009).

    Google Scholar 

  113. Lisci, M., Monte, M. & Pacini, E. Lichens and higher plants on stone: a review. Int. Biodeterior. Biodegrad. 51, 1–17 (2003).

    Google Scholar 

  114. Caneva, G., Danin, A., Ricci, S. & Conti, C. The pitting of Trajan’s column, Rome: an ecological model of its origin. In Conservazione del Patrimonio culturale II, Contributi Centro Linceo Interdisciplinare Beniamino Segre 78–102 (Accademia Nazionale dei Lincei, 1994).

  115. Danin, A. Pitting of calcareous rocks by organisms under terrestrial conditions. Isr. J. Earth Sci. 41, 201–207 (1992).

    Google Scholar 

  116. Danin, A. & Caneva, G. Deterioration of limestone walls in Jerusalem and marble monuments in Rome caused by cyanobacteria and cyanophilous lichens. Int. Biodeterior. Biodegrad. 26, 397–417 (1990).

    Google Scholar 

  117. Lombardozzi, V., Castrignanò, T., D’Antonio, M., Casanova Municchia, A. & Caneva, G. An interactive database for an ecological analysis of stone biopitting. Int. Biodeterior. Biodegrad. 73, 8–15 (2012).

    Google Scholar 

  118. Gehrmann, C., Krumbein, W. & Petersen, K. Endolithic lichens and the corrosion of carbonate rocks. A study of biopitting. Int. J. Mycol. Lichenol. 5, 37–48 (1992).

    Google Scholar 

  119. McIlroy de la Rosa, J. P., Warke, P. A. & Smith, B. J. Microscale biopitting by the endolithic lichen Verrucaria baldensis and its proposed role in mesoscale solution basin development on limestone. Earth Surf. Process. Landf. 37, 374–384 (2012).

    Google Scholar 

  120. Pomar, F., Gómez-Pujol, L., Fornós, J. J., Del Valle, L. & Nogales, B. Limestone biopitting in coastal settings: A spatial, morphometric, SEM and molecular microbiology sequencing study in the Mallorca rocky coast (Balearic Islands, Western Mediterranean). Geomorphology 276, 104–115 (2017).

    Google Scholar 

  121. Caneva, G. Ecological approach to the genesis of calcium oxalate patinas on stone monuments. Aerobiologia 9, 149–156 (1993).

    Google Scholar 

  122. Bruno, L. & Valle, V. Effect of white and monochromatic lights on cyanobacteria and biofilms from Roman Catacombs. Int. Biodeterior. Biodegrad. 123, 286–295 (2017).

    Google Scholar 

  123. Danin, A. Patterns of biogenic weathering as indicators of palaeoclimates in Israel. Proc. R. Soc. Edinb. B 89, 243–253 (1986).

    Google Scholar 

  124. de Ferri, L., Lottici, P. P., Lorenzi, A., Montenero, A. & Salvioli-Mariani, E. Study of silica nanoparticles – polysiloxane hydrophobic treatments for stone-based monument protection. J. Cult. Herit. 12, 356–363 (2011).

    Google Scholar 

  125. Son, S. et al. Organic−inorganic hybrid compounds containing polyhedral oligomeric silsesquioxane for conservation of stone heritage. ACS Appl. Mater. Inter. 1, 393–401 (2009).

    CAS  Google Scholar 

  126. Erkal, A., D’Ayala, D. & Sequeira, L. Assessment of wind-driven rain impact, related surface erosion and surface strength reduction of historic building materials. Build. Environ. 57, 336–348 (2012).

    Google Scholar 

  127. Traversetti, L., Bartoli, F. & Caneva, G. Wind-driven rain as a bioclimatic factor affecting the biological colonization at the archaeological site of Pompeii, Italy. Int. Biodeterior. Biodegrad. 134, 31–38 (2018).

    Google Scholar 

  128. Ortega-Morales, O., Guezennec, J., Hernández-Duque, G., Gaylarde, C. C. & Gaylarde, P. M. Phototrophic biofilms on ancient Mayan buildings in Yucatan, Mexico. Curr. Microbiol. 40, 81–85 (2000).

    CAS  Google Scholar 

  129. Li, Q., Zhang, B., He, Z. & Yang, X. Distribution and diversity of bacteria and fungi colonization in stone monuments analyzed by high-throughput sequencing. PLoS ONE 11, e0163287 (2016).

    Google Scholar 

  130. Wu, F., Wang, W., Feng, H. & Gu, J.-D. Realization of biodeterioration to cultural heritage protection in China. Int. Biodeterior. Biodegrad. 117, 128–130 (2017).

    CAS  Google Scholar 

  131. Wang, W. et al. Seasonal dynamics of airborne fungi in different caves of the Mogao Grottoes, Dunhuang, China. Int. Biodeterior. Biodegrad. 64, 461–466 (2010).

    Google Scholar 

  132. Zamarreño, D. V., Inkpen, R. & May, E. Carbonate crystals precipitated by freshwater bacteria and their use as a limestone consolidant. Appl. Environ. Microbiol. 75, 5981–5990 (2009).

    Google Scholar 

  133. Jroundi, F. et al. Protection and consolidation of stone heritage by self-inoculation with indigenous carbonatogenic bacterial communities. Nat. Commun. 8, 279 (2017).

    Google Scholar 

  134. Ascaso, C. et al. In situ evaluation of the biodeteriorating action of microorganisms and the effects of biocides on carbonate rock of the Jeronimos Monastery (Lisbon). Int. Biodeterior. Biodegrad. 49, 1–12 (2002).

    Google Scholar 

  135. Koestler, R. J., Parreira, E., Santoro, E. D. & Noble, P. Visual effects of selected biocides on easel painting materials. Stud. Conserv. 38, 265–273 (1993).

    Google Scholar 

  136. Fidanza, M. R. & Caneva, G. Natural biocides for the conservation of stone cultural heritage: a review. J. Cult. Herit. 38, 271–286 (2019).

    Google Scholar 

  137. Silva, M., Rosado, T., Teixeira, D., Candeias, A. & Caldeira, A. T. Production of green biocides for cultural heritage. Novel biotechnological solutions. Int. J. Conserv. Sci. 6, 519–530 (2015).

    CAS  Google Scholar 

  138. Silva, M., Rosado, T., Teixeira, D., Candeias, A. & Caldeira, A. T. Green mitigation strategy for cultural heritage: bacterial potential for biocide production. Environ. Sci. Pollut. Res. 24, 4871–4881 (2017).

    CAS  Google Scholar 

  139. Marin, E., Vaccaro, C. & Leis, M. Biotechnology applied to historic stoneworks conservation: testing the potential harmfulness of two biological biocides. Int. J. Conserv. Sci. 7, 227–238 (2016).

    Google Scholar 

  140. Caneva, G., Fidanza, M. R., Tonon, C. & Favero-Longo, S. E. Biodeterioration patterns and their interpretation for potential applications to stone conservation: a hypothesis from allelopathic inhibitory effects of lichens on the Caestia Pyramid (Rome). Sustainability 12, 1132 (2020).

    CAS  Google Scholar 

  141. Alfano, G. et al. The bioremoval of nitrate and sulfate alterations on artistic stonework: the case-study of Matera Cathedral after six years from the treatment. Int. Biodeterior. Biodegrad. 65, 1004–1011 (2011).

    CAS  Google Scholar 

  142. Soffritti, I. et al. The potential use of microorganisms as restorative agents: an update. Sustainability 11, 3853 (2019).

    CAS  Google Scholar 

  143. Scherer, G. W., Flatt, R. & Wheeler, G. Materials science research for the conservation of sculpture and monuments. MRS Bull. 26, 44–50 (2001).

    CAS  Google Scholar 

  144. Gu, J.-D. Microbiological deterioration and degradation of synthetic polymeric materials: recent research advances. Int. Biodeterior. Biodegrad. 52, 69–91 (2003).

    CAS  Google Scholar 

  145. Charola, A. E., McNamara, C. & Koestler, R. J. (eds) Biocolonization of Stone: Control and Preventive Methods: Proceedings from the MCI Workshop Series Smithsonian Contributions to Museum Conservation no. 2 (Smithsonian Institution Scholarly Press, 2011).

  146. Yang, F. et al. Conservation of weathered historic sandstone with biomimetic apatite. Chin. Sci. Bull. 57, 2171–2176 (2012).

    CAS  Google Scholar 

  147. Gherardi, F., Roveri, M., Goidanich, S. & Toniolo, L. Photocatalytic nanocomposites for the protection of European architectural heritage. Materials 11, 65 (2018).

    Google Scholar 

  148. Sierra-Fernandez, A., Gomez-Villalba, L., Rabanal, M. & Fort, R. New nanomaterials for applications in conservation and restoration of stony materials: a review. Mater. Construcc. 67, e107 (2017).

    Google Scholar 

  149. Grossi, C. M., Bonazza, A., Brimblecombe, P., Harris, I. & Sabbioni, C. Predicting twenty-first century recession of architectural limestone in European cities. Environ. Geol. 56, 455–461 (2008).

    CAS  Google Scholar 

  150. de la Rosa, J. P. M., Warke, P. A. & Smith, B. J. Lichen-induced biomodification of calcareous surfaces: bioprotection versus biodeterioration. Prog. Phys. Geog. 37, 325–351 (2013).

    Google Scholar 

  151. Gadd, G. M. & Dyer, T. D. Bioprotection of the built environment and cultural heritage. Microb. Biotechnol. 10, 1152–1156 (2017).

    Google Scholar 

  152. Pinna, D. Biofilms and lichens on stone monuments: do they damage or protect? Front. Microbiol. 5, 133 (2014).

    Google Scholar 

  153. Gadd, G. M. et al. Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol. Rev. 28, 36–55 (2014).

    Google Scholar 

  154. Bosch-Roig, P. & Ranalli, G. The safety of biocleaning technologies for cultural heritage. Front. Microbiol. 5, 155 (2014).

    Google Scholar 

  155. Zhang, G. et al. Biochemical reactions and mechanisms involved in the biodeterioration of stone world cultural heritage under the tropical climate conditions. Int. Biodeterior. Biodegrad. 143, 104723 (2019).

    CAS  Google Scholar 

  156. Zhang, X., Ge, Q., Zhu, Z., Deng, Y. & Gu, J.-D. Microbiological community of the Royal Palace in Angkor Thom and Beng Mealea of Cambodia by Illumina sequencing based on 16S rRNA gene. Int. Biodeterior. Biodegrad. 134, 127–135 (2018).

    CAS  Google Scholar 

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Acknowledgements

This research is supported in part by Hong Kong RGC GRF (grant no. 17302119). X.L. acknowledges support from the International Biodeterioration & Biodegradation Society.

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Authors and Affiliations

  1. Laboratory of Environmental Microbiology and Toxicology, School of Biological Sciences, The University of Hong Kong, Hong Kong, PR China

    Xiaobo Liu

  2. Museum Conservation Institute, Smithsonian Institution, Museum Support Center, Suitland, MD, USA

    Robert J. Koestler

  3. LBW Bioconsult, Wiefelstede, Germany

    Thomas Warscheid

  4. Tokyo National Research Institute for Cultural Properties, Tokyo, Japan

    Yoko Katayama

  5. Environmental Engineering, Guangdong Technion Israel Institute of Technology, Guangdong, PR China

    Ji-Dong Gu

  6. Southern Laboratory of Ocean Science and Engineering (Guangdong, Zhuhai), Zhuhai, PR China

    Ji-Dong Gu

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  1. Xiaobo Liu
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  2. Robert J. Koestler
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  3. Thomas Warscheid
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  4. Yoko Katayama
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  5. Ji-Dong Gu
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J.-D.G. and X.L. conceived the framework and led the writing of the manuscript. J.-D.G. and X.L. analysed the data and made all figures. All authors wrote and revised the manuscript.

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Correspondence to Ji-Dong Gu.

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Liu, X., Koestler, R.J., Warscheid, T. et al. Microbial deterioration and sustainable conservation of stone monuments and buildings. Nat Sustain 3, 991–1004 (2020). https://doi.org/10.1038/s41893-020-00602-5

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