Advertisement

Annals of Microbiology

, Volume 65, Issue 3, pp 1243–1255 | Cite as

An overview of techniques for the characterization and quantification of microbial colonization on stone monuments

  • Agnes Mihajlovski
  • Damien Seyer
  • Hayette Benamara
  • Faisl Bousta
  • Patrick Di Martino
Review Article

Abstract

Biodeterioration can be defined as any undesired change of the properties of a material caused by biological activity of living organisms. The biodeterioration of stone materials is related to the production of pigments (aesthetic action), to cell metabolism (biochemical action) and to the mechanical action of the biomass colonizing the material during its growth (physical action). Quantification of the sessile biomass and characterization of microbial communities colonizing stone are essential first steps to ensure the diagnosis of biodeterioration processes and to implement control strategies and appropriate treatment. Different destructive and non-destructive approaches can be used to sample stone specimens from monuments: scraping, swab using, and cutting. Different analytical methods can be used depending on the type of microorganism sought: determination of chlorophyll content and color analysis for pigmented microorganisms; measurement of in situ physiological activity of surface microcolonies by applying fluorogenic substrate analogues or confocal laser scanning microscopy observations after CTC staining for active biomass; scanning or transmission electron microscopy observation for biofilm visualization; enzyme-linked immunosorbent assay for the investigation of both microorganisms that can and cannot be cultured; classical microbiological methods, which consist in cultivation of microorganisms on synthetic media; and molecular methods for the study of microbial biodiversity based on the polymorphism of molecular markers using PCR, hybridization, classical or high throughput sequencing. The aim of this review is to present basics of the different biodeterioration mechanisms and to focus on the main techniques that can be used to characterize and quantify the biodeterioration biomass.

Keywords

Biodeterioration Stone Monument Microorganisms Biofilm 

Notes

Acknowledgment

This work has been funded in part by a grant from the Labex PATRIMA.

References

  1. Adamson C, McCabe S, Warke PA, McAllister D, Smith BJ (2013) The influence of aspect on the biological colonization of stone in Northern Ireland. Int Biodeterior Biodegrad 84:357–366Google Scholar
  2. Allen GC, El-Turki A, Hallam KR, McLaughlin D, Stacey M (2000) Role of NO2 and SO2 in degradation of limestone. Brit Corros J 35(1):35–38Google Scholar
  3. Allsopp D (2011) Worldwide wastage: the economics of biodeterioration. Microbiol Tod 38:150–153Google Scholar
  4. Anderson IC, Campbell CD, Prosser JI (2003) Potential bias of fungal 18S rDNA and internal transcribed spacer polymerase chain reaction primers for estimating fungal biodiversity in soil. Environ Microbiol 5(1):36–47PubMedGoogle Scholar
  5. Ariño X, Gomez-Bolea A, Saiz-Jimenez C (1997) Lichens on ancient mortars. Int Biodeter Biodegrad 40:217–224Google Scholar
  6. Ascaso C, Ollacarizqueta MA (1991) Structural relationship between lichen and carved stonework of silos monastery, Burgos, Spain. Int Biodeter 27:337–349Google Scholar
  7. Ascaso C, Wierzchos J, Souza-Egipsy V, de los Rios V, Rodrigues JD (2002) In situ evaluation of the biodeteriorating action of microorganisms and the effects of biocides on carbonate rock of the jeronimos monastery (Lisbon). Int Biodeter Biodegrad 49(1):1–12Google Scholar
  8. Barberousse H, Lombardo RJ, Tell G, Couté A (2006) Factors involved in the colonisation of building façades by algae and cyanobacteria in France. Biofouling 22:69–77PubMedGoogle Scholar
  9. Barreto M, Jedlicki E, Holmes DS (2005) Identification of a gene cluster for the formation of extracellular polysaccharide precursors in the chemolithoautotroph Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:2902–2909PubMedCentralPubMedGoogle Scholar
  10. Bartosch S, Mansch R, Knötzsch K, Bock E (2003) CTC staining and counting of actively respiring bacteria in natural stone using confocal laser scanning microscopy. J Microbiol Meth 52(1):75–84Google Scholar
  11. Baumgärtner M, Remde A, Bock E, Conrad R (1990) Release of nitric oxide from building stones into the atmosphere. Atmos Environ Part B-Urb 24(1):87–92Google Scholar
  12. Beech IB, Sunner J (2004) Biocorrosion: towards understanding interactions between biofilms and metals. Curr Opin Biotechnol 15(3):181–186PubMedGoogle Scholar
  13. Berdoulay M, Salvado JC (2009) Genetic characterization of microbial communities living at the surface of building stones. Lett Appl Microbiol 49(3):311–316PubMedGoogle Scholar
  14. Bityukova L (2006) Air pollution effect on the decay of carbonate building stones in old town of Tallinn. Water Air Soil Poll 172(1–4):239–271Google Scholar
  15. Camuffo D (1992) Acid rain and the deterioration of monuments: how old is the phenomenon? Atmos Environ 26(2):241–247Google Scholar
  16. Caneva G, Gori E, Montefinale T (1995) Biodeterioration of monuments in relation to climatic changes in Rome between 19–20th centuries. Sci Total Environ 167(1–3):205–214Google Scholar
  17. Cappitelli F, Principi P, Pedrazzani R, Toniolo L, Sorlini C (2007) Bacterial and fungal deterioration of the Milan cathedral marble treated with protective synthetic resins. Sci Total Environ 385(1–3):172–81PubMedGoogle Scholar
  18. Carter NEA, Viles HA (2005) Bioprotection explored: the story of a little known earth surface process. Geomorphology 67(3–4):273–281Google Scholar
  19. Concha-Lozano N, Gaudon P, Pages J, de Billerbeck G, Lafon D, Eterradossi O (2012) Protective effect of endolithic fungal hyphae on oolitic limestone buildings. J Cult Herit 13(2):120–127Google Scholar
  20. Crispim CA, Gaylarde CC (2005) Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1–9PubMedGoogle Scholar
  21. Cutler N, Viles H (2010) Eukaryotic microorganisms and stone biodeterioration. Geomicrobiol J 27(6–7):630–646. doi: 10.1080/01490451003702933 Google Scholar
  22. Cutler NA, Oliver AE, Viles HA, Whiteley AS (2012) Non-destructive sampling of rock-dwelling microbial communities using sterile adhesive tape. J Microbiol Meth 91(3):391–398Google Scholar
  23. Cutler NA, Oliver AE, Viles HA, Ahmad S, Whiteley AS (2013a) The characterisation of eukaryotic microbial communities on sandstone buildings in Belfast, UK, using TRFLP and 454 pyrosequencing. Int Biodeter Biodegrad 82:124–133Google Scholar
  24. Cutler NA, Viles HA, Ahmad S, McCabe S, Smith BJ (2013b) Algal ‘greening’ and the conservation of stone heritage structures. Sci Total Environ 442:152–164PubMedGoogle Scholar
  25. Dakal TC, Arora PK (2012) Evaluation of potential of molecular and physical techniques in studying biodeterioration. Rev Environ Sci Biotechnol 11:71–104Google Scholar
  26. Danin A, Caneva G (1990) Deterioration of limestone walls in Jerusalem and marbles monuments in Rome caused by cyanobacteria and cyanophilous lichens. Int Biodeterior 26:397–417Google Scholar
  27. De Felice B, Pasquale V, Tancredi N, Scherillo S, Guida M (2010) Genetic fingerprint of microorganisms associated with the deterioration of an historical tuff monument in Italy. J Genet 89(2):253–257PubMedGoogle Scholar
  28. de la Torre MA, Gómez-Alarcón G, Melgarejo P, Saiz-Jimenez C (1991) Fungi in weathered sandstone from Salamanca cathedral, Spain. Sci Tot Environ 107:159–168Google Scholar
  29. de los Ríos A, Ascaso C (2005) Contributions of in situ microscopy to the current understanding of stone biodeterioration. Int Microbiol 8(3):181–188Google Scholar
  30. de los Ríos A, Cámara B, del Cura MA G, Rico VJ, Galván V, Ascaso C (2009) Deteriorating effects of lichen and microbial colonization of carbonate building rocks in the Romanesque churches of Segovia (Spain). Sci Tot Environ 407(3):1123–1134Google Scholar
  31. de los Rios A, Galván V, Ascaso C (2004) In situ microscopical diagnosis of biodeterioration processes at the convent of Santa Cruz la Real, Segovia, Spain. Int Biodeter Biodegrad 54:113–120Google Scholar
  32. Dere S, Günes T, Sivaci R (1998) Spectrophotometric determination of chlorophyll – a, b and total carotenoid contents of some species using different solvents. Turk J Bot 22:13–17Google Scholar
  33. Diakumaku E, Gorbushina AA, Krumbein WE, Panina L, Soukharjevski S (1995) Black fungi in marble and limestones — an aesthetical, chemical and physical problem for the conservation of monuments. Sci Tot Environ 167(1–3):295–304Google Scholar
  34. Dilling W, Cypionka H (1990) Aerobic respiration in sulfate-reducing bacteria. FEMS Microbiol Lett 71:123–128Google Scholar
  35. Dornieden T, Gorbushina AA (2000) New methods to study the detrimental effects of poikilotroph microcolonial micromycetes (PMM) on building materials. Proceedings of the 9th International Congress on Deterioration and Conservation of Stone — Venice June 19–24, 461–468Google Scholar
  36. EN 15898 (2011) Conservation of cultural property - Main general terms and definitionsGoogle Scholar
  37. Ettenauer JD, Piñar G, Lopandic K, Spangl B, Ellersdorfer G, Voitl C, Sterflinger K (2012) Microbes on building materials — evaluation of DNA extraction protocols as common basis for molecular analysis. Sci Tot Environ 439:44–53Google Scholar
  38. Favero-Longo SE, Borghi A, Tretiach M, Piervittori R (2009) In vitro receptivity of carbonate rocks to endolithic lichen-forming aposymbionts. Mycol Res 113(10):1216–1227PubMedGoogle Scholar
  39. Garcia-Vallès M, Vendrell-Saz M, Krumbein WE, Urzì C (1997) Coloured mineral coatings on monument surfaces as a result of biomineralization: the case of the Tarragona cathedral (Catalonia). Appl Geochem 12(3):255–266Google Scholar
  40. Garty J (1990) Influence of epilithic microorganisms on the surface temperature of building walls. Can J Bot 68:1349–1353Google Scholar
  41. Gaylarde CC, Gaylarde PM (2005) A comparative study of the major microbial biomass of biofilms on exteriors of buildings in Europe and Latin America. Int Biodeterior Biodegrad 55:131–139Google Scholar
  42. Gaylarde CC, Rodríguez CH, Navarro-Noya YE, Ortega-Morales BO (2012) Microbial biofilms on the sandstone monuments of the angkor wat complex, Cambodia. Curr Microbiol 64(2):85–92PubMedGoogle Scholar
  43. Gazzano C, Favero-Longo SE, Matteucci E, Roccardi A, Piervittori R (2009) Index of Lichen Potential Biodeteriogenic Activity (LPBA): a tentative tool to evaluate the lichen impact on stonework. Int Biodeter Biodegrad 63(7):836–843Google Scholar
  44. George RP, Ramya S, Ramachandran D, Kamachi Mudali U (2013) Studies on biodegradation of normal concrete surfaces by fungus Fusarium sp. Cement Concret Res 47:8–13Google Scholar
  45. Giovannacci D, Leclaire C, Horgnies M, Ellmer M, Mertz JD, Orial G, Chen J, Bousta F (2013) Algal colonization kinetics on roofing and façade tiles: influence of physical parameters. Constr Build Mater 48:670–676Google Scholar
  46. Golubic S, Perkins RD, Lukas KJ (1975) Boring microorganisms and microborings in carbonate substrates. In: Frey RW (ed) The Study of Trace Fossils. Springer Verl, New York, pp 229–259Google Scholar
  47. Golubic S, Friedmann EI, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sedimentol Petrol 51:475–478Google Scholar
  48. Gómez-Alarcón G, de la Torre MA (1994) The effect of filamentous fungi on stone monuments: the Spanish experience. In: Singh J (ed) Building Mycology. Management of decay and health in buildings. Chapman and Hall, UK, pp 295–309Google Scholar
  49. Gómez-Alarcón G, Cirellos B, Flores M, Lorenzo J (1995a) Microbial communities and alteration processes in monuments at Alcala de Henares. Spain. Sci Tot Environ 167:231–239Google Scholar
  50. Gómez-Alarcón G, Muñoz M, Ariño X, Ortega-Calvo JJ (1995b) Microbial communities in weathered sandstones: the case of Carrascosa del Campo church, Spain. Sci Total Environ 167:249–254Google Scholar
  51. Gómez-Bolea A, Llop E, Ariño X, Saiz-Jimenez C, Bonazza Z, Messina P, Sabbioni C (2012) Mapping the impact of climate change on biomass accumulation on stone. J Cult Herit 13(3):254–258Google Scholar
  52. Gómez-Cornelio S, Mendoza-Vega J, Gaylarde CC, Reyes-Estebanez M, Morón-Ríos A, del Carmen De la Rosa-García S, Ortega-Morales BO (2012) Succession of fungi colonizing porous and compact limestone exposed to subtropical environments. Fungal Biol 116(10):1064–1072PubMedGoogle Scholar
  53. Gorbushina AA (2007) Life on the Rocks. Environ Microbiol 9(7):1613–1631PubMedGoogle Scholar
  54. Gorbushina AA, Broughton WJ (2009) Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol 63:431–450PubMedGoogle Scholar
  55. Gorbushina AA, Krumbein WE, Hamann CH, Panina L, Soukharjevski S, Wollenzien U (1993) On the role of black fungi in colour change and biodeterioration of antique marbles. Geomicrobiol J 11:205–221Google Scholar
  56. Guiamet P, Crespo M, Lavin P, Ponce B, Gaylarde C, de Saravia Gómez S (2013) Biodeterioration of funeral sculptures in La recoleta cemetery, Buenos Aires, Argentina: Pre- and post-intervention studies. Colloid Surf B 101:337–342Google Scholar
  57. Guillitte O (1995) Bioreceptivity: a new concept for building ecology studies. Sci Tot Environ 167:215–220Google Scholar
  58. Herrera LK, Videla HA (2004) The importance of atmospheric effects on biodeterioration of cultural heritage constructional materials. Int Biodeterior Biodegrad 54:125–134Google Scholar
  59. Herrera LK, Arroyave C, Guiamet P, de Saravia Gomez S, Videla H (2004) Biodeterioration of peridotite and other constructional materials in a building of the Colombian cultural heritage. Int Biodeterior Biodegrad 54:135–141Google Scholar
  60. Herrera LK, Le Borgne S, Videla HA (2009) Modern methods for materials characterization and surface analysis to study the effects of biodeterioration and weathering on buildings of cultural heritage. Int J Architect Herit 3:74–91Google Scholar
  61. Hirsch P, Eckhardt FEW, Palmer RJ Jr (1995) Methods for the study of rock-inhabiting microorganisms—a mini review. J Microbiol Meth 23(2):143–167Google Scholar
  62. Hu H, Ding S, Katayama Y, Kusumi A, Li SX, de Vries RP, Wang J, Yu XZ, Gu JD (2013) Occurrence of Aspergillus allahabadii on sandstone at Bayon temple, Angkor Thom, Cambodia. Int Biodeterior Biodegrad 76:112–117Google Scholar
  63. Hueck HJ (2001) The biodeterioration of materials—an appraisal. Int Biodeter Biodegrad 48:5–11Google Scholar
  64. Jenneman GE, McInerney MJ, Knapp RM (1985) Microbial penetration through nutrient saturated Berea sandstone. Appl Environ Microbiol 50:383–391PubMedCentralPubMedGoogle Scholar
  65. Jerez CA (2008) The use of genomics, proteomics and other OMICS technologies for the global understanding of biomining microorganisms. Hydrometallurgy 94(1–4):162–169Google Scholar
  66. Kaplan D, Christiaen D, Arad SM (1987) Chelating properties of extracellular polysaccharides from Chlorella spp. Appl Environ Microbial 53:2953–2956Google Scholar
  67. Kinzler K, Gehrke T, Telegdi J, Sand W (2003) Bioleaching—a result of interfacial processes caused by extracellular polymeric substances (EPS). Hydrometallurgy 71(1–2):83–88Google Scholar
  68. Konkol N, McNamara CJ, Mitchell R (2010) Fluorometric detection and estimation of fungal biomass on cultural heritage materials. J Microbiol Meth 80(2):178–182Google Scholar
  69. Krumbein WE, Gorbushina A (1995) Organic pollution and rock decay. In: Morton LHG (ed) Biodeterioration of constructional materials, p 277–284Google Scholar
  70. La Cono V, Urzì C (2003) Fluorescent in situ hybridization applied on samples taken with adhesive tape strips. J Microbiol Methods 55(1):65–71PubMedGoogle Scholar
  71. Laiz L, Piñar G, Lubitz W, Saiz-Jimenez C (2003) The colonization of building materials by microorganisms as revealed by culturing and molecular methods. In: Saiz-Jimenez C (ed) Molecular biology and cultural heritage. Swets & Zeitlinger, Lisse, pp 23–28Google Scholar
  72. Laiz L, Romanowska-Deskins A, Saiz-Jimenez C (2011) Survival of a bacterial/archael consortium on building materials as revealed by molecular methods. Int Biodeterior Biodegrad 65(7):1100–1103Google Scholar
  73. Lan W, Li H, Wang WD, Katayama Y, Gu JD (2010) Microbial community analysis of fresh and old microbial biofilms on Bayon temple sandstone of Angkor Thom, Cambodia. Microb Ecol 60:105–115PubMedCentralPubMedGoogle Scholar
  74. Li XS, Sato T, Ooiwa Y, Kusumi A, Gu JG, Katayama Y (2010) Oxidation of Elemental Sulfur by Fusarium solani StrainTHIF01 Harboring Endobacterium Bradyrhizobium sp. Microb Ecol 60:96–104PubMedGoogle Scholar
  75. Little B, Wagner P, Ray R, Pope R, Scheetz R (1991) Biofilms: an ESEM evaluation of artifacts introduced during SEM preparation. J Ind Microbiol 8(4):213–221Google Scholar
  76. Lueders T, Friedrich MW (2003) Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl Environ Microbiol 69:320–326PubMedCentralPubMedGoogle Scholar
  77. Marques J, Hespanhol H, Paz-Bermúdez G, Almeida R (2014) Choosing between sides in the battle for pioneer colonization of schist in the Côa Valley Archaeological Park: a community ecology perspective. J Archaeol Sci 45:196–206Google Scholar
  78. McNamara CC, Perry TD, Bearce KA, Hernandez-Duque G, Mitchell R (2006) Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. Microb Ecol 51:51–64PubMedGoogle Scholar
  79. Miller AZ, Sanmartín P, Pereira-Pardo L, Dionísio A, Saiz-Jimenez C, Macedo MF, Prieto B (2012) Bioreceptivity of building stones: a review. Sci Tot Environ 426:1–12Google Scholar
  80. Müller E, Drewello U, Drewello R, Weißmann R, Wuertz S (2001) In situ analysis of biofilms on historic window glass using confocal laser scanning microscopy. J Cult Herit 2(1):31–42Google Scholar
  81. Nuhoglu Y, Oguz E, Uslu H, Ozbek A, Ipekoglu B, Ocak I, Hasenekoglu I (2006) The accelarating effects of the microorganisms on biodeterioration of stone monuments under air pollution and continental-cold climatic conditions in Erzurum, Turkey. Sci Tot Environ 364:272–283Google Scholar
  82. Ortega-Morales BO, Narvaez-Zapata JA, Schmalenberger A, Dousa-Lopez A, Tebbe CC (2004) Biofilms fouling ancient limestone Mayan monuments in Uxmal, Mexico: a cultivation-independent analysis. Biofilms 1:79–90Google Scholar
  83. Ortega-Morales BO, Gaylarde CC, Englert GE, Gaylarde PM (2005) Analysis of salt-containing biofilms on limestone buildings of the Mayan culture at Edzna, Mexico. Geomicrobiol J 22:261–268Google Scholar
  84. Ortega-Morales BO, Gaylarde C, Anaya-Hernandez A, Chan-Bacab MJ, De la Rosa-García SC, Arano-Recio D, Montero-M J (2013) Orientation affects Trentepohlia-dominated biofilms on Mayan monuments of the Rio Bec style. Int Biodeterior Biodegrad 84:351–356Google Scholar
  85. Palmer SR, Gaines AF, Jarvie AWP (1987) Analysis of the structures of the organic materials in Kimmeridge and Oxford clays. Fuel 66(4):499–504Google Scholar
  86. Papida S, Murphy W, May E (2000) Enhancement of physical weathering of building stones by microbial populations. Int Biodeterior Biodegrad 46(4):305–317Google Scholar
  87. Piñar G, Ripka K, Weber J, Sterflinger K (2009) The micro-biota of a sub-surface monument the medieval chapel of St. Virgil (Vienna, Austria). Int Biodeterior Biodegrad 63(7):851–859Google Scholar
  88. Polo A, Cappitelli F, Brusetti L, Principi P, Villa F, Giacomucci L, Ranalli G, Sorlini C (2010) Feasibility of removing surface deposits on stone using biological and chemical remediation methods. Microb Ecol 60(1):1–14PubMedGoogle Scholar
  89. Priester JH, Horst AM, Van De Werfhorst LC, Saleta JL, Mertes LAK, Holden PA (2007) Enhanced visualization of microbial biofilms by staining and environmental scanning electron microscopy. J Microbiol Meth 68(3):577–587Google Scholar
  90. Prieto B, Silva B, Lantes O (2004) Biofilm quantification on stone surfaces: comparison of various methods. Sci Tot Environ 333(1–3):1–7Google Scholar
  91. Qi-Wang MGY, He LY, Sheng XF (2011) Characterization of bacterial community inhabiting the surfaces of weathered bricks of Nanjing Ming city walls. Sci Tot Environ 409(4):756–762Google Scholar
  92. Ratogi G, Sani RK (2011) Molecular techniques to assess Microbial community structure, function and dynamics in the environment. In: Ahmad I, Ahmad F, Pichtel J (eds) Microbes and Microbial Technology: Agricultural and Environmental Applications, p 29–57Google Scholar
  93. Roh W, Abell G, Kim KH, Nam YD, Bae JW (2010) Comparing microarrays and next-generation sequencing technologies for microbial ecology research Seong. Trends Biotechnol 28:291–299PubMedGoogle Scholar
  94. Sand W (1997) Microbial mechanisms of deterioration of inorganic substrates—a general mechanistic overview. Int Biodeterior Biodegrad 40(2–4):183–190Google Scholar
  95. Sand W, Bock E (1991) Biodeterioration of ceramic materials by biogenic acids. Int Biodeterior 27(2):175–183Google Scholar
  96. Sand W, Gehrke T (2006) Extracellular polymeric substances mediate bioleaching/biocorrosion via interfacial processes involving iron (III) ions and acidophilic bacteria. Res Microbiol 157(1):49–56PubMedGoogle Scholar
  97. Sand W, Jozsa PG, Mansch R (2002) Weathering, Microbiology. In: Britton G (ed) Environmental Microbiology, Vol 6. Wiley, New York, pp 3364–3375Google Scholar
  98. Scheerer S, Ortega-Morales O, Gaylarde C (2009) Microbial deterioration of stone-monuments-an updated overview. Adv Appl Microbiol 66:97–139PubMedGoogle Scholar
  99. Schiavon N (2002) Biodeterioration of calcareous and granitic building stones in urban environments. Geological Society, vol 205. Special Publications, London, pp 195–205Google Scholar
  100. Schumann R, Haubner N, Klausch S, Karsten U (2005) Chlorophyll extraction methods for the quantification of green microalgae colonizing building facades. Int Biodeterior Biodegrad 55(3):213–222Google Scholar
  101. Seaward MRD (1982) Lichen ecology of changing urban environments. In: Bornkamm R, Lee JA, Seaward MRD (eds) Urban Ecology. Blackwell Scientific Publications, Oxford, pp 181–189Google Scholar
  102. Seaward MRD, Giacobini C, Giuliani MR, Roccardi A (1989) The role of lichens in the biodeterioration of ancient monuments with particular reference to central Italy. Int Biodeter 25(1–3):49–55Google Scholar
  103. Shively JM, Benson AA (1967) Phospholipids of Thiobacillus thiooxidans. J Bacteriol 94:1679–1683PubMedCentralPubMedGoogle Scholar
  104. Speranza M, Wierzchos J, De Los RA, Perez-Ortega S, Souza-Egipsy V, Ascaso C (2012) Towards a more realistic picture of in situ biocide actions: combining physiological and microscopy techniques. Sci Total Environ 439:114–122PubMedGoogle Scholar
  105. Starosvetsky J, Zukerman U, Armon RH (2013) A simple medium modification for isolation, growth and enumeration of Acidithiobacillus thiooxidans (syn. Thiobacillus thiooxidans) from water samples. J Microbiol Meth 92:178–182Google Scholar
  106. Steiger M (2005) Crystal growth in porous materials—I: the crystallization pressure of large crystals. J Crystal Growth 282(3–4):455–469Google Scholar
  107. Steiger M, Wolf F, Dannecker W (1993) Deposition and enrichment of atmospheric pollutants on building stones as determined by field exposure experiments. In: Thiel MJ (ed) Conservation of stone and other Materials, vol 1. E & FN Spon, London, pp 35–42Google Scholar
  108. Sterflinger K (2010) Fungi: their role in deterioration of cultural heritage. Fungal Biol Rev 24:47–55Google Scholar
  109. Sterflinger K, Piñar G (2013) Microbial deterioration of cultural heritage and works of art — tilting at windmills? Appl Microbiol Biotechnol 97:9637–9646PubMedCentralPubMedGoogle Scholar
  110. Suihko ML, Alakomi HL, Gorbushina A, Fortune I, Marquardt J, Saarela M (2007) Characterization of aerobic bacterial and fungal microbiota on surfaces of historic Scottish monuments. Syst Appl Microbiol 30(6):494–508PubMedGoogle Scholar
  111. Taber S (1929) Frost heaving. J Geol 37(5):428–461Google Scholar
  112. Taber S (1930) The mechanics of frost heaving. J Geol 38(4):303–317Google Scholar
  113. Tanner RS, Udegbunam EO, MMcInnerey MJ, Knapp RM (1991) Microbially enhanced oil recovery from carbonate reservoirs. Geomicrobiol J 9:169–195Google Scholar
  114. Tayler S, May E (1991) The seasonality of heterotrophic bacteria on sandstones on ancient monuments. Int Biodeterior 28:49–64Google Scholar
  115. Tayler S, May E (1994) Detection of specific bacteria on stone using an enzyme-linked immunosorbent assay. Int Biodeterior Biodegrad 34(2):155–167Google Scholar
  116. Tecer L, Cerit O (2002) The effects of air pollution on carbonate stone monuments in urban areas (Sivas, Turkey). Fresenius Environ Bull 11:505–509Google Scholar
  117. Tomaselli L, Lamenti G, Bosco M, Tiano P (2000) Biodiversity of photosynthetic microorganisms dwelling on stone monuments. Int Biodeterior Biodegrad 46:251–258Google Scholar
  118. Tretiach M, Bertuzzi S, Salvadori O (2010) Chlorophyll a fluorescence as a practical tool for checking the effects of biocide treatments on endolithic lichens. Int Biodeter Biodegrad 64(6):452–460Google Scholar
  119. Urzi C (2004) Microbial deterioration of rocks and marble monuments in Mediterranean Basin: A review. Corros Rev 22:441–457Google Scholar
  120. Urzi C, Albertano P (2001) Studying phototrophic and heterotrophic microbial communities on stone monuments. In: Doyle RJ (ed) Methods in Enzymology, vol 336. Academic, San Diego, pp 340–355Google Scholar
  121. Urzi C, Realini M (1998) Colour changes of Notos calcareous sandstone as related to its colonisation by microorganisms. Int Biodeterior Biodegrad 42:45–54Google Scholar
  122. Vázquez-Nion D, Sanmartín P, Silva B, Prieto B (2013) Reliability of color measurements for monitoring pigment content in a biofilm-forming cyanobacterium. Int Biodeterior Biodegrad 84:220–226Google Scholar
  123. Ward DM, Weller R, Bateson MM (1990) 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345:63–65PubMedGoogle Scholar
  124. Warscheid T (2003) The evaluation of biodeterioration processes on cultural objects and approaches for their effective control. In: Koestler RJ, Charola AE, Nieto-Fernandez FE (eds) Art, biology and conservation. Biodeterioration of works of art, the metropolitan museum of art, New York, pp 14–27Google Scholar
  125. Warscheid T, Braams J (2000) Biodeterioration of stone: a review. Int Biodeterior Biodegrad 46(4):343–368Google Scholar
  126. Warscheid T, Petersen K, Krumbein WE (1990) A rapid method to demonstrate and evaluate microbial activity on decaying sandstone. Stud Conserv 35:137–147Google Scholar
  127. Warscheid T, Becker TW, Resende MA (1996) Biodeterioration of stone: a comparison between (sub-) tropical and moderate climate zones. Int Biodeterior Biodegrad 37(1–2):124Google Scholar
  128. Wierzchos J, Ascaso C (1994) Application of back-scattered electron imaging to the study of the lichen-rock interface. J Microsc 175(1):54–59Google Scholar
  129. Wiktor V, De Leo F, Urzì C, Guyonnet R, Grosseau P, Garcia-Diaz E (2009) Accelerated laboratory test to study fungal biodeterioration of cementitious matrix. Int Biodeterior Biodegrad 63(8):1061–1065Google Scholar
  130. Wilmes P, Bond PL (2006) Metaproteomics: studying functional gene expression in microbial ecosystems. Trends Microbiol 14:92–97PubMedGoogle Scholar
  131. Witteburg C (1994) Trickene Schadgas und Partikeldeposition auf verschidene Sandsteinvarietäten unter besonderer Beücksichtigung atlosphärischer EinfluBgröben. PhD thesis, HamburgGoogle Scholar
  132. Zanardini E, Abbruscato P, Ghedini N, Realini M, Sorlini C (2000) Influence of atmospheric pollutants on biodeterioration of stone. Int Biodeterior Biodegrad 45:35–42Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and the University of Milan 2014

Authors and Affiliations

  • Agnes Mihajlovski
    • 1
  • Damien Seyer
    • 1
  • Hayette Benamara
    • 1
  • Faisl Bousta
    • 2
  • Patrick Di Martino
    • 1
  1. 1.Laboratoire ERRMECe-EA1391Université de Cergy-PontoiseCergy-Pontoise, cedexFrance
  2. 2.USR3224 LRMH, CNRS, CRCCChamps-sur-MarneFrance

Personalised recommendations