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Evaluation of potential of molecular and physical techniques in studying biodeterioration

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Abstract

Recently, researcher’s abilities to elucidate the biogeophysical and biogeochemical mechanisms of complex biodeterioration processes occurring at monumental sites has been greatly revolutionized by use of molecular, physical and highly sophisticated so called high throughput next generation sequencing techniques. Such achievements are obvious in several areas of biotechnology and environmental science including geomicrobiological studies related to biodeterioration and bioconservation of ancient historic architectural monuments and artworks. Application of these techniques in studying architectural monuments and artworks is not just limited to predict the prevalence microbial diversity and identifying the mechanism of biodeterioration caused by inhabiting microorganisms, but also to provide in-depth molecular, biogeophysical and biogeochemical basis of how microorganisms respond to different environmental conditions to accelerate the process of biodeterioration, which in turn will offer tremendous opportunities to environmental scientists and researchers to formulate or device preventive and remedial safeguard techniques to control undesirable growth and survival of microorganisms on monuments and work of arts. Further evaluation studies and investigations are currently in progress to upgrade these molecular and physical strategies and to develop reliable approaches to better explain the various processes of biodeterioration and related phenomenon. A comprehensive description of techniques being successfully incorporated and applied in this regard is described in this review. Taken together, it can be anticipated that these techniques possess an astounding potential to turn around research related to geomicrobiological studies related to biodeterioration and bioconservation of monuments.

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References

  • Adorni E, Venturelli G (2010) Mortars and stones of the Damascus Citadel (Syria). Int J Archit Herit Conserv Anal Restor 4:337–350

    Google Scholar 

  • Alakomi HL, Saarela M, Gorbushina AA, Krumbein WE, McCullagh C, Robertson P, Rodenacker K (2006a) Control of biofilm growth through photodynamic treatments combined with chemical inhibitors: in vitro evaluation methods. In: Fort R, De Buergo MA, Gomez-Heras M, Vazquez-Calvo C (eds) Heritage, Weathering and Conservation (HWC-2006). Taylor and Francis, London, pp 713–717

    Google Scholar 

  • Alakomi HL, Paananen A, Suihko ML, Helander IM, Saarela M (2006b) Weakening effect of cell permeabilizers on Gram-negative bacteria causing biodeterioration. Appl Environ Microbiol 72:4695–4703

    Article  CAS  Google Scholar 

  • Albertano P, Urzì C (1999) Structural interactions among epilithic cyanobacteria and heterotrophic microorganisms in Roman hypogeal. Microb Ecol 38:244–252

    Article  Google Scholar 

  • Amaan RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Mol Biol Rev 59:143–169

    Google Scholar 

  • Anastasiou M, Hasapis T, Zorba T, Pavliduo E, Chrissafis K, Paraskevopoulos KM (2006) TG/DTA and FTIR analyses of plasters from Byzantine monuments in Balkan region—comparative study. J Therm Anal Calorim 84:27–32

    Article  CAS  Google Scholar 

  • 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. Appl Environ Microbiol 5:36–47

    CAS  Google Scholar 

  • Ascaso C, Wierzchos J (1995) Study of the bioeterioration zone between the lichen thallus and the substrate. Cryptogam Bot 5:270–281

    Google Scholar 

  • Ascaso C, Sancho LG, Rodriguez-Pascual C (1990) The weathering action of saxicolous lichens in maritime Antarctica. Polar Biol 11:33–39

    Article  Google Scholar 

  • Ascaso C, Wierzchos J, Souza-Egipsy V, De los Ríos A, 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 Biodeterior Biodegrad 49:1–12

    Article  Google Scholar 

  • Avşar EO, Duran Z, Akyol O, Toz G (2008) Modelling of the temple of Apollo Smintheus using photogrammetry and virtual realty. The international archives of the photogrammetry, remote sensing and spatial information sciences, vol XXXVII, Part B5. Beijing

  • Barberousse H, Lombardo RJ, Tell G, Couté A (2006) Factors involved in the colonization of building façades by algae and cyanobacteria in France. Biofouling 22:69–77

    Google Scholar 

  • Barcina LM, Espina A, Suárez M, García JR, Rodríguez J (1997) Characterization of monumental carbonate stones by thermal analysis (TG, DTG and DSC). Thermochim Acta 290:181–189

    Article  CAS  Google Scholar 

  • 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 Methods 52:75–84

    Article  CAS  Google Scholar 

  • Baskar S, Baskar R, Mauclaire L, McKenzie JA (2006) Microbially induced calcite precipitation in culture experiments: possible origin for stalactites in Sahastradhara caves, Dehradun, India. Curr Sci 90:58–64

    CAS  Google Scholar 

  • Benavente D, García del Cura MA, García-Guinea J, Sánchez-Moral S, Ordóñez S (2004) Role of pore structure in salt crystallization in unsaturated porous stone. J Cryst Growth 260:532–544

    Article  CAS  Google Scholar 

  • Benzzi K, Tanouti B, Bouabdelli M, Alvarez A, Brianso JL, Cherradi F (2008) Determination of the composition and the origin of the ochre brown patina on the monumental Bab Agnaou gate (Marrakech, Morocco). Environ Geol 53:1283–1288

    Article  CAS  Google Scholar 

  • Berdoulay M, Salvado JC (2009) Genetic characterization of microbial communities living at the surface of building stones. Lett Appl Microbiol 49:311–316

    Article  CAS  Google Scholar 

  • Billi D, Caiola MG, Paolozzi L, Ghelardini P (1998) A method for DNA extraction from the desert cyanobacterium Chroococcidiopsis and its application to identification of ftsZ. Appl Environ Microbiol 64:4053–4056

    CAS  Google Scholar 

  • Boon J, Asahina S (2006) Surface preparation of cross sections to traditional and modern paint using the argon ion milling polishing CP system. Microsc Microanal 12:1322–1323

    Article  Google Scholar 

  • Brimblecombe P, Grossi CM (2005) Aesthetic thresholds and blackening of stone buildings. Sci Total Environ 349:175–189

    Article  CAS  Google Scholar 

  • Cámara B, De loa Ríos A, Urizal M, De Buergo MA, Varas MJ, Fort R, Ascaso C (2011) Characterizing the microbial colonization of a dolostone quarry: implications for stone biodeterioration and response to biocide treatments. Microb Ecol. doi:10.1007/s00248-011-9815-x

    Google Scholar 

  • Campos-Suñol MJ, Domínguez-Vidal A, Ayora-Cañada MJ, De la Torre-López MJ (2008) Renaissance patinas in Úbeda (Spain): mineralogic, petrographic and spectroscopic study. Anal Bioanal Chem 391:1039–1048

    Article  CAS  Google Scholar 

  • Caneva G, Salvadori O, Ricci S, Ceschina S (2005) Ecological analysis and biodeterioration processes over time at the Hieroglyphic Stairway in the Copàn (Honduras) archaeological site. Plant Biosyst 139:295–310

    Google Scholar 

  • Cappitelli F, Zanardini E, Ranalli G, Mello E, Daffonchio D, 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

    Google Scholar 

  • Cappitelli F, Toniolo L, Sansonetti A, Gulotta D, Ranalli G, Zanardini E, Sorlini C (2007) Advantages of using microbial technology over traditional chemical technology in removal of black crusts from stone surfaces of historical monuments. Appl Environ Microbiol 73:5671–5675

    Article  CAS  Google Scholar 

  • Cappitelli F, Abbruscato P, Foladori P, Zanardini E, Ranalli G, Principi P, Villa F, Polo A, Sorlini C (2009) Detection and elimination of cyanobacteria from frescoes: the case of the St. Brizio Chapel (Orvieto Cathedral, Italy). Microb Ecol 57:633–639

    Article  CAS  Google Scholar 

  • Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, Zanardini E, Sorlini C, Corselli C, Daffonchio D (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70:6147–6156

    Article  CAS  Google Scholar 

  • Carmona N, Laiz L, Gonzalez JM, Garcia-Herasa M, Villegasa MA, Saiz-Jimenez C (2006) Biodeterioration of historic stained glasses from the Cartuja de Miraflores (Spain). Int Biodeterior Biodegrad 58:155–161

    Article  CAS  Google Scholar 

  • Cecchi G, Pantani L, Raimondi V, Tomaselli L, Lamenti G, Tiano P, Chiari R (2000) Fluorescence lidar technique for the remote sensing of stone monuments. J Cult Herit 1:29–36

    Article  Google Scholar 

  • Chiavari C, Rahmouni K, Takenouti H, Joiret S, Vermaut P, Robbiola L (2007) Composition and electrochemical properties of natural patinas of outdoor bronze monuments. Electrochim Acta 52:7760–7769

    Article  CAS  Google Scholar 

  • Ciupiński L, Fortuna-Zaleśna E, Garbacz H, Koss A, Kurzydłowski KJ, Marczak J, Mróz J, Onyszczuk T, Rycyk A, Sarzyński A, Skrzeczanowski W, Strzelec M, Zatorska A, Śukowska GZ (2010) Comparative laser spectroscopy diagnostics for ancient metallic artefacts exposed to environmental pollution. Sensors 10:4926–4949

    Article  CAS  Google Scholar 

  • Colao F, Fantoni R, Fiorani L, Palucci A, Gomoiua I (2005) Compact scanning LIDAR for fluorosensor for investigation of biodegradation of ancient painted surfaces. J Optoelectron Adv Mater 7:3197–3208

    CAS  Google Scholar 

  • Comelli D, D’Andrea C, Valentini G, Cubeddu R, Colombo C, Toniolo L (2004) Fluorescence lifetime imaging and spectroscopy as tools for nondestructive analysis of works of art. Appl Opt 43:2175–2183

    Article  Google Scholar 

  • Crispim CA, Gaylarde CC (2005) Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1–9

    Article  CAS  Google Scholar 

  • Crispim CA, Gaylarde CC, Gaylarde PM, Copp J, Neilan BA (2003) Molecular biology for investigation of cyanobacterial populations on historic buildings in Brazil. In: Saiz-Jimenez C (ed) Molecular biology and cultural heritage. Zwets & Zeitlinger, Lisse, pp 141–143

    Google Scholar 

  • Cuzman OA (2009) Biofilms on exposed monumental stones: mechanism of formation and development of new control methods (PhD thesis). University of Bologna, Italy

  • Cuzman OA, Ventura S, Sili C, Mascalchi C, Turchetti T, D’Acqui LP, Tiano P (2010) Biodiversity of phototrophic biofilms dwelling on monumental fountains. Microb Ecol 60:81–95

    Article  CAS  Google Scholar 

  • Dakal T, Cameotra SS (2012) Geomicrobiology of heritage monuments and artworks: mechanisms of biodeterioration, bioconservation strategies and applied molecular approaches. In: Mason AC (ed) Bioremediation: biotechnology, engineering and environmental management. Nova, New York

  • 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 89:253–257

    Article  Google Scholar 

  • De los Ríos A, Ascaso C (2005) Contributions of in situ microscopy to the current understanding of stone biodeterioration. Int Microbiol 8:181–188

    Google Scholar 

  • De los Ríos A, Wierzchos J, Ascaso C (2002) Microhabitats and chemical microenvironments under saxicolous lichens growing on granite. Microb Ecol 43:181–188

    Article  CAS  Google Scholar 

  • De los Ríos A, Galvan V, Ascaso C (2004) In situ microscopical diagnosis of biodeterioration processes at the convent of Santa Cruz la Real, Segovia, Spain. Int Biodeterior Biodegrad 54:113–120

    Article  Google Scholar 

  • De Muynck W, Debrouwer D, De Belie N (2008) Bacterial carbonate precipitation improves the durability of cementitious materials. Cem Concr Res 38:1005–1014

    Article  CAS  Google Scholar 

  • Del Barrio SV, Garcia-Vallès M, Pradell T, Vendrell-Saz M (2002) The red-orange patina developed on a monumental dolostone. Eng Geol 63:31–38

    Article  Google Scholar 

  • Delgado Rodrigues J, Valero Congil J, Wakefield R, Brechet E, Larranaga I (2004) Monitoraggio della biocolonizzazione e valutazione dell’efficacia di un biocida. Arkos, Scienza e Restauro nell’Architettura 7:52–58

    Google Scholar 

  • Diamond S (2000) Mercury porosimetry. An inappropriate method for the measurement of pore size distributions in cement-based materials. Cem Concr Res 30:1517–1525

    Article  CAS  Google Scholar 

  • Dick J, De Windt W, De Graef B, Saveyn H, De Belie N, Verstraete W (2006) Biodeposition of a calcium carbonate layer on degraded limestone by Bacillus sphaericus. Biodegradation 17:357–367

    Article  CAS  Google Scholar 

  • Diez B, Pedros-Alio C, Marsh TL, Massana R (2001) Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl Environ Microbiol 67:2942–2951

    Article  CAS  Google Scholar 

  • Dupont J, Claire Jacquet C, Dennetière B, Lacoste S, Bousta F, Orial G, Cruaud C, Couloux A, Roquebert MF (2007) Invasion of the French Paleolithic painted cave of Lascaux by members of the Fusarium solani species complex. Mycologia 99:526–533

    Article  CAS  Google Scholar 

  • Echigo A, Hino M, Fukushima T, Mizuki T, Kameruka M, Usami R (2005) Endospores of halophilic bacteria of the family Bacillaceae isolated from non-saline Japanese soil may be transported by Kosa event (Asian dust storm). Saline Syst 1:8–20

    Article  CAS  Google Scholar 

  • Edwards HGM, Seaward MRD, Attwood SJ, Little SJ, De Oliveira LFC, Tretiach M (2003) FT-Raman spectroscopy of lichens on dolomitic rocks: an assessment of metal oxalate formation. Analyst 128:1218–1221

    Article  CAS  Google Scholar 

  • Edwards RA, Rodriguez-Brito B, Wegley L, Haynes M, Breitbart M, Peterson DM, Saar MO, Alexander S, Alexander EC Jr, Rohwer F (2006) Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 7:57–69

    Article  CAS  Google Scholar 

  • Ferris MJ, Ruff-Roberts AL, Kopczynski ED, Bateson MM, Ward DM (1996) Enrichment culture and microscopy conceal diverse thermophilic Synechococcus populations in a single hot spring microbial mat habitat. Appl Environ Microbiol 62:1045–1050

    CAS  Google Scholar 

  • Fonseca AJ, Pina F, Macedo MF, Leal N, Romanowska-Deskins A, Laiz L, Gómez-Bolea A, Saiz-Jimenez C (2010) Anatase as an alternative application for preventing biodeterioration of mortars: evaluation and comparison with other biocides. Int Biodeterior Biodegrad 64:388–396

    Article  CAS  Google Scholar 

  • Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643

    Article  CAS  Google Scholar 

  • Gaylarde C, Silva MR, Warscheid T (2003) Microbial impact on building materials: an overview. Mater Struct 36:342–352

    Article  CAS  Google Scholar 

  • Gaylarde CC, Gaylarde PM, Janine Copp J, Neilan B (2004) Polyphasic detection of cyanobacteria in terrestrial biofilms. Biofouling 20:71–79

    Article  CAS  Google Scholar 

  • Giacomucci L, Bertoncello R, Salvadori O, Martini I, Favaro M, Villa F, Sorlini C,Cappitelli F (2011) Microbial deterioration of artistic tiles from the façade of the Grande Albergo Ausonia & Hungaria (Venice, Italy). Microb Ecol. doi:10.1007/s00248-011-9812-0

  • Goldstein JI, Newbury DE, Joy DC, Lyman CE, Echlin P, Lifshin E, Sawyer LC, Michael JR (2003) Scanning electron microscopy and X-ray microanalysis. Kluwer/Plenum, New York, p 297

    Book  Google Scholar 

  • Gómez-Alarcón, Munoz ML, Flores M (1994) Excretion of organic acids by fungal strains isolated from decayed sandstone. Internat Biodet Biodeg 34:169–180

  • Gonzalez JM, Saiz-Jimenez C (2004) Microbial diversity in biodeteriorated monuments as studied by denaturing gradient gel electrophoresis. J Sep Sci 27:174–180

    Google Scholar 

  • Gonzalez JM, Saiz-Jimenez C (2005) Application of molecular nucleic acid-based techniques for the study of microbial communities in monuments and artworks. Int Microbiol 8:189–194

    Google Scholar 

  • Gorbushina AA, Lialikova NN, Vlasov DIu, Khizhniak TV (2002) Microbial communities on the monuments of Moscow and St. Petersburg: biodiversity and trophic relations. Mikrobiologiia 71:409–417

  • Grbić MVL, Vukojeviã JB (2009) Role of fungi in biodeterioration process of stones in historic buildings. Proc Natl Acad Sci 116:245–251

    Google Scholar 

  • Grbić ML, Subakov-Simić G, Krizmanić J, Ladić V (2009) Cyanobacterial, algal and fungal biofilm on sandstone substrata of Eiffel’s Lock in Bečej (Serbia). Bot Ser 33:101–105

    Google Scholar 

  • Grondona I, Hermosa MR, Tejada M, Gomis MD, Mateos PF, Bridge PD, Monte E, Garcia-Acha I (1997) Physiological and biochemical characterization of Trichoderma harzianum, a biological control agent against soil borne fungal plant pathogens. Appl Environ Microbiol 63:3189–3198

    Google Scholar 

  • Gurtner C, Heyrman J, Piñar G, Lubitz W, Swings J, Rölleke S (2000) Comparative analyses of the bacterial diversity on two different biodeteriorated wall paintings by DGGE and 16S rDNA sequence analysis. Int Biodeterior Biodeg 46:229–239

    Google Scholar 

  • Hällström J, Barup K, Gronlund R, Johansson A, Svanberg S, Palombi L, Lognoli D, Raimondi V, Cecchi G, Conti C (2009) Documentation of soiled and biodeteriorated facades: a case study on the Coliseum, Rome, using hyperspectral imaging fluorescence lidars. J Cult Heri 10:106–115

    Google Scholar 

  • Häubner N, Schumann R, Karsten U (2006) Aeroterrestrial microalgae growing in biofilms on facades: response to temperature and water stress. Microb Ecol 51:285–293

    Article  Google Scholar 

  • Hernández-Mariné M, Clavero E, Roldán M (2004) Microscopy methods applied to research on cyanobacteria. Limnetica 23:179–186

    Google Scholar 

  • Herrera LK, Videla HA (2009) Surface analysis and materials characterization for the study of biodeterioration and weathering effects on cultural property. Int Biodeterior Biodegrad 63:813–822

    Article  CAS  Google Scholar 

  • Herrera LK, Arroyave C, Videla HA (2003) Atmospheric and biological deterioration of two churches from the cultural heritage of the city of Medellin, Colombia. In: Saiz-Jimenez C (ed) Molecular biology and cultural heritage. A.A. Balkema, Lisse, pp 271–276

    Google Scholar 

  • Herrera LK, Arroyave C, Guiamet P, Gómez de Saravia S, Videla H (2004) Biodeterioration of peridotite and other constructional materials in a building of the Colombian cultural heritage. Int Biodeterior Biodegrad 54:135–141

    Article  CAS  Google Scholar 

  • Herrera LK, Cotte M, Jimenez De Haro MC, Duran A, Justo A, Perez-Rodriguez JL (2008) Characterization of iron-oxide based pigments by synchrotron-based micro X-ray diffraction. Appl Clay Sci 42:57–62

    Article  CAS  Google Scholar 

  • Heyrman J, Mergaert J, Denys R, Swings J (1999) The use of fatty acid methyl ester analysis (FAME) for the identification of heterotrophic bacteria present on three mural paintings showing severe damage by microorganisms. FEMS Microbiol Lett 181:55–62

    Article  CAS  Google Scholar 

  • Hutchens E, Gleeson D, McDermott F, Miranda-Caso Luengo R, Clipson N (2010) Meter-scale diversity of microbial communities on a weathered pegmatite granite outcrop in the Wicklow Mountains, Ireland: evidence for mineral induced selection. Geomicrobiol J 27:1–14

    Article  CAS  Google Scholar 

  • Jimenez-Lopez C, Rodriguez-Navarro C, Piñar G, Carrillo-Rosuá FJ, Rodriguez-Gallego M, Gonzalez-Muñoz MT (2007) Consolidation of degraded ornamental porous limestone stone by calcium carbonate precipitation induced by the microbiota inhabiting the stone. Chemosphere 68:1929–1936

    Article  CAS  Google Scholar 

  • Jones SE, Shade AL, McMahon KD, Kent AD (2007) Comparison of primer sets for use in automated ribosomal intergenic spacer analysis of aquatic bacterial communities: an ecological perspective. Appl Environ Microbiol 73:659–662

    Article  CAS  Google Scholar 

  • Jroundi F, Fernández-Vivas A, Rodriguez-Navarro C, Bedmar EJ, González-Muñoz MT (2010) Bioconservation of deteriorated monumental calcarenite stone and identification of bacteria with carbonatogenic activity. Microb Ecol 60:39–54

    Article  CAS  Google Scholar 

  • Kiel G, Gaylarde CC (2007) Diversity of salt-tolerant culturable aerobic microorganisms on historic buildings in Southern Brazil. World J Microbiol Biotechnol 23:363–366

    Article  CAS  Google Scholar 

  • Kolo K, Keppens E, Préat A, Claeys P (2007) Experimental observations on fungal diagenesis of carbonate substrates. J Geophys Res 112:G01700

    Google Scholar 

  • Kramar S, Mirtič B (2008) Characterization of black crusts of Robba’s fountain statues Ljubljana (Slovenia). RMZ Mater Geoenviron 55:490–504

    Google Scholar 

  • Kuhlman KR, Fusco WG, La Duc MT, Allenbach LB, Ball CL, Kuhlman GM, Anderson RC, Erickson IK, Stuecker T, Benardini J, Strap JL, Crawford RL (2006) Diversity of microorganisms within rock varnish in the Whipple Mountains, California. Appl Environ Microbiol 72:1708–1715

    Article  CAS  Google Scholar 

  • Kumar R, Kumar AV (1999) Biodeterioration of stones in tropical environments. J. Paul Getty Trust, Los Angeles, p 7

    Google Scholar 

  • Kyi CP (2003) The significance of appropriate sampling and cultivation techniques in the effective assessment of biodeterioration. AICCM Bull 28:89–92

    Google Scholar 

  • 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 BV, Lisse, pp 23–28

    Google Scholar 

  • Laiz L, Miller AZ, Jurado V, Akatova E, Sanchez-Moral S, Gonzalez JM, Dionísio A, Macedo MF, Saiz-Jimenez C (2009) Isolation of five Rubrobacter strains from biodeteriorated monuments. Naturwissenschaften 96:71–79

    Article  CAS  Google Scholar 

  • Lan W, Hui 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 60:105–115

    Article  Google Scholar 

  • Lazic V, Colao F, Fantoni R, Palucci A, Spizzichino V, Borgia I, Brunetti BG, Sgamellotti A (2003) Characterization of lustre and pigment composition in ancient pottery by laser induced fluorescence and breakdown spectroscopy. J Cult Herit 4:303–308

    Article  Google Scholar 

  • Lèpere C, Wilmotte A, Meyer B (2000) Molecular diversity of microcystis strains (Cyanophyceae, Chroococcales) based on 16S rDNA sequences. Syst Geogr Plants 70:275–283

    Article  Google Scholar 

  • Levsky JM, Singer RH (2003) Fluorescence in situ hybridization: past, present and future. J Cell Sci 166:2833–2838

    Article  CAS  Google Scholar 

  • Lognoli D, Cecchi G, Mochi I, Pantani L, Raimondi V, Chiari R, Johansson T, Weibring P, Edner H, Svanberg S (2003) Fluorescence lidar imaging of the cathedral and baptistery of Parma. Appl Phys B 76:457–465

    Article  CAS  Google Scholar 

  • Maidak BL, Cole JR, Parker CT Jr, Garrity GM, Larsen N, Li B, Lilburn TG, McCaughey MJ, Olsen GJ, Overbeek R, Pramanik S, Schmidt TM, Tiedje JM, Woese CR (1999) A new version of the RDP (ribosomal database project). Nucleic Acids Res 27:171–173

    Article  CAS  Google Scholar 

  • May E, Jones M, Mitschell J (2008a) Fluorescent in situ hybridization (FISH) as a molecular tool to study bacteria causing biodeterioration. In: May E, Jones M, Mitschell J (eds) Heritage microbiology and science: microbes, monuments, and maritime materials. RCS Publication, London, pp 143–150

    Google Scholar 

  • May E, Jones M, Mitschell J (2008b) Novel combined approach based on phospholipid fatty acids and 16S-rDNA PCR-SSCP analyses to characterize fouling biofilms on historic monuments. In: May E, Jones M, Mitschell J (eds) Heritage microbiology and science: microbes, monuments, and maritime materials. RCS Publication, London, pp 156–165

    Google Scholar 

  • Miller A, Laiz L, Dionísio A, Macedo MF, Saiz-Jimenez C (2009) Growth of phototrophic biofilms from limestone monuments under laboratory conditions. Int Biodeterior Biodegrad 63:860–867

    Article  CAS  Google Scholar 

  • Mohammadi P, Krumbein WE (2008) Biodeterioration of ancient stone materials from the Persepolis monuments (Iran). Aerobiologia 24:27–33

    Article  Google Scholar 

  • Monte M (2003) Biogenesis of oxalate patinas on marble specimens in fungal culture. Aerobiologia 19:271–275

    Article  Google Scholar 

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  Google Scholar 

  • Ortega-Morales BO (2006) Cyanobacterial diversity and ecology on historic monuments in Latin America. Microbiologia 48:188–195

    Google Scholar 

  • Ortega-Morales BO, Guenennec J, Hernández-Duque G, Gaylarde CC, Gaylarde PM (2000) Phototrophic biofilms on ancient Mayan buildings in Yucatan, Mexico. Current Microbiology 40:81–85

    Article  CAS  Google Scholar 

  • Ortega-Morales BO, Lopez-Cortes A, Hernandez-Duque G, Crassous P, Guezennec J (2001) Extracellular polymers of microbial communities colonizing ancient limestone monuments. In: Doyle RJ (ed) Methods in enzymology. Academic Press, San Diego, pp 331–339

    Google Scholar 

  • Ortega-Morales BO, Narváez-Zapata JA, Schmalenberger A, Sosa-López A, Tebbe CC (2004) Biofilms fouling ancient limestone Mayan monuments in Uxmal, Mexico: a cultivation independent analysis. Biofilms 1:79–90

    Article  Google Scholar 

  • Osborn AM, Moore ERB, Timmis KN (2000) An evaluation of terminal restriction fragment length polymorphism (t-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2:39–50

    Article  CAS  Google Scholar 

  • Ostrooumov M, Taran YA, Arellano-Jimenez M, Ponce A, Reyes-Gasga J (2008) La colimaíta, K3VS4, un nuevo mineral del volcán Colima (México): Boletín de la Sociedad Mexicana de. Mineralogía 18:7–8

    Google Scholar 

  • Palla F, Anello L, Pecorella S, Russo R, Damian F (2003) Characterization of bacterial communities on stone monuments by molecular biology tools. In: Saiz-Jimenez C (ed) Molecular biology and cultural heritage. Swets & Zeitlinger BV, Lisse, pp 115–118

    Google Scholar 

  • Pangallo D, Chovanová K, Drahovska H, De Leo F, Urzì C (2009) Application of fluorescence internal transcribed spacer-PCR (f-ITS) for the cluster analysis of bacteria isolated from air and deteriorated fresco surface. Int Biodeterior Biodegrad 63:868–872

    Article  CAS  Google Scholar 

  • Pasanen AL, Pietila KY, Pasanen P, Kaliokoski P, Tarhanen J (1999) Ergosterol content in various fungal species and biocontaminated building materials. Appl Environ Microbiol 65:138–142

    CAS  Google Scholar 

  • Perez-Rodriguez JL, Duran A, Centeno MA, Martinez-Blanes JM, Robador MD (2011) Thermal analysis of monument patina containing hydrated calcium oxalates. Thermochim Acta 512:5–12

    Article  CAS  Google Scholar 

  • Piñar G, Gurtner C, Lubitz W, Rölleke S (2001a) Identification of archaea in objects of art by denaturing gradient gel electrophoresis analysis and shotgun cloning. Methods Enzymol 336:356–366

    Article  Google Scholar 

  • Piñar G, Gurtner C, Ramos C, Lubitz W, Rölleke S (2001b) Identification of archaea in deteriorated ancient wall paintings by DGGE and FISH analysis. In: Galan E, Zezza E (eds) Protection and conservation of the cultural heritage of the Mediterranean cities. Balkema/Swets and Zeitlinger, pp 209–214

  • Piñar G, Ramos C, Rölleke S, Schabereiter-Gurtner C, Vybiral D, Lubitz W, Denner EBM (2001c) Detection of indigenous Halobacillus populations in damaged ancient wall paintings and building materials: molecular monitoring and cultivation. Appl Environ Microbiol 67:4891–4895

    Article  Google Scholar 

  • Piñar G, Saiz-Jimenez C, Schabereiter-Gurtner C, Blanco-Varela MT, Lubitz W, Rölleke S (2001d) Archaeal communities in two disparate deteriorated ancient wall paintings: detection, identification and temporal monitoring by denaturing gradient gel electrophoresis. FEMS Microbiol Ecol 37:45–54

    Article  Google Scholar 

  • 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 60:1–14

    Article  CAS  Google Scholar 

  • Popescu CM, Sakata Y, Popescu MC, Okasa A, Vasile C (2005) Degradation of lime wood painting supports. E-Preserv Sci 2:19–29

    CAS  Google Scholar 

  • Prieto B, Seaward MRD, Edwards HGM, Rivas T, Silva B (1999) Biodeterioration of granite monuments by Ochrolechia parella (L.) mass: an FT Raman spectroscopic study. Biospectroscopy 5:53–59

    Article  CAS  Google Scholar 

  • Prieto B, Aira N, Silva B (2007) Comparative study of dark patinas on granitic outcrops and buildings. Sci Total Environ 381:280–289

    Article  CAS  Google Scholar 

  • Ramírez M, Hernández-Mariné M, Novelo E, Roldán M (2010) Cyanobacteria-containing biofilms from a Mayan monument in Palenque, Mexico. Biofouling 26:399–409

    Article  Google Scholar 

  • Raskin I, Nanda-Kumar PBA, Dushenkov V, Salt DE (1994) Bioconcentration of heavy metals by plants. Curr Opin Biotechnol 5:285–290

    Google Scholar 

  • Robbiola L, Rahmouni K, Chiavari C, Martini C, Prandstraller D, Texier A, Takenouti H, Vermaut P (2008) New insight into the nature and properties of pale green surfaces of outdoor bronze monuments. Appl Phys A 92:161–169

    Article  CAS  Google Scholar 

  • Roldán M, Clavero E, Hernández-Marine M (2002) Biofilm structure of cyanobacteria in catacombs. Coalition 5:6–8

    Google Scholar 

  • Roldán M, Clavero E, Castel S, Hernández-Mariné M (2004) Biofilms fluorescence and image analysis in hypogean monuments research. Algol Stud 111:127–143

    Article  Google Scholar 

  • Rölleke S, Muyzer G, Wawer C, Wanner G, Lubitz W (1996) Identification of bacteria in the biodegraded wall painting by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 62:2059–2065

    Google Scholar 

  • Rölleke S, Witte A, Wanner G, Lubitz W (1998) Medieval wall painting-a habitat for archaea: identification of archaea by denaturing gradient gel electrophoresis (DGGE) of PCR-amplified gene fragments coding 16S rRNA in a medieval wall painting. Int Biodeterior Biodegrad 41:85–92

    Article  Google Scholar 

  • Rölleke S, Gurtner C, Drewello U, Drewello R, Lubitz W, Weissmann R (1999) Analysis of bacterial communities on historical glass by denaturing gradient gel electrophoresis of PCRamplified gene fragments coding for 16S rRNA. J Microbiol Methods 36:107–114

    Article  Google Scholar 

  • Rölleke S, Gurtner C, Piñar G, Lubitz W (2000) Molecular approaches for the assessment of microbial deterioration of objects of art. In: Ciferri O, Tiano P, Mastromei G (eds) Proceedings of International Conference on Microbiology and Conservation (ICMC). Kluwer/Plenum, New York, pp 39–47

    Google Scholar 

  • Ronaghi M (2001) Pyrosequencing sheds light on DNA sequencing. Genome Res 11:3–11

    Article  CAS  Google Scholar 

  • Ronaghi M, Uhlén M, Nyrén P (1998) A sequencing method based on real-time pyrophosphate. Science 281:363–365

    Article  CAS  Google Scholar 

  • Ruiz-Agudo E, Mees F, Jacobs P, Rodriguez-Navarro C (2007) The role of saline solution properties on porous limestone salt weathering by magnesium and sodium sulfates. Environ Geol 52:269–281

    Article  CAS  Google Scholar 

  • Saad DS, Saad DS, Kinsey GC, Paterson R, Gaylarde C (2003) Ergosterol analysis for the quantification of fungal growth on paint films. Proposal for a standard method. Surf Coat Int Part B Coat Trans 86:131–134

    Google Scholar 

  • Saarela M, Alakomi HL, Suihko ML, Maunuksela L, Raaska L, Mattila-Sandholm T (2004) Heterotrophic microorganisms in air and biofilm from Roman catacombs, with special emphasis on actinobacteria and fungi. Int Biodeterior Biodegrad 54:27–37

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sanchez-Moral S, Luque L, Cuezva S, Soler V, Benavente D, Laiz L, Gonzalez JM, Saiz-Jimenez C (2005) Deterioration of building materials in Roman catacombs: the influence of visitors. Sci Total Environ 349:260–276

    Article  CAS  Google Scholar 

  • Sarkar SL, Bhadra AK, Mandal PK (1994) Investigation of mortar and stone deterioration in the Victoria Memorial, Calcutta. Mater Struct 27:548–556

    Article  CAS  Google Scholar 

  • Schabereiter-Gurtner C, Piñar G, Lubitz W, Rölleke S (2001a) An advanced molecular strategy to identify bacterial communities on art objects. J Microbiol Methods 45:77–87

    Article  CAS  Google Scholar 

  • Schabereiter-Gurtner C, Piñar G, Lubitz W, Rölleke S (2001b) Analysis of fungal communities on historical church window glass by denaturing gradient gel electrophoresis and phylogenetic 18S rDNA sequence analysis. J Microbiol Methods 47:345–354

    Article  CAS  Google Scholar 

  • Schabereiter-Gurtner C, Piñar G, Vybiral D, Lubitz W, Rölleke S (2001c) Rubrobacter related bacteria associated with rosy discoloration of masonry and lime wall paintings. Arch Microbiol 176:347–354

    Article  CAS  Google Scholar 

  • Schabereiter-Gurtner C, Saiz-Jimenez C, Piñar G, Lubitz W, Rölleke S (2003) Molecular biology and cultural heritage. In: Saiz-Jimenez C (ed) Balkema, Lisse, pp 15–21

  • Scheerer S, Ortega-Morales O, Gaylarde C (2009) Microbial deterioration of stone monuments: an updated overview. Adv Appl Microbiol 66:97–139

    Article  CAS  Google Scholar 

  • Schumann R, Eixler S, Görs S, Karsten U (2003) Moderne Methoden der angewandten Ö kologie: II. Visualisierung von Mikroorganismen und ihren Lebensäußerungen. Altbauinstandsetzung 5/6:171–180

    Google Scholar 

  • Schumann R, Häubner N, Klausch S, Karsten U (2005) Chlorophyll extraction methods for the quantification of green microalgae colonizing building facades. Int Biodeterior Biodegrad 55:213–222

    Article  CAS  Google Scholar 

  • Sebastián E, Cultrone G, Benavente D, Fernandez LL, Elert K, Rodriguez-Navarro C (2008) Swelling damage in clay-rich sandstones used in the church of San Mateo in Tarifa (Spain). J Cult Herit 9:66–76

    Article  Google Scholar 

  • Sert HB, Sümbül H, Sterflinger K (2007) A new species of Capnobotryella from monument surfaces. Mycol Res III 111:1235–1241

    Article  CAS  Google Scholar 

  • Severiano LC, Lahr FAR, Bardi MAG, Santos AC, Machado LDB (2010) Influence of gamma radiation on properties of common Brazilian wood species used in artwork. Prog Nucl Energy 52:730–734

    Article  CAS  Google Scholar 

  • Suzuki MT, Giovannoni SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62:625–630

    CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • Tayler S, May E (1995) A comparison of methods for the measurement of microbial activity on stone. Stud Conserv 40:163–170

    Article  Google Scholar 

  • Tayler S, May E (2000) Investigations of the localisation of bacterial activity on sandstone from ancient monument. Int Biodeterior Biodeg 46:327–333

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Tomaselli L, Lamenti G, Bosco M, Tiano P (2000) Biodiversity of photosynthetic microorganisms dwelling on stone monuments. Int Biodeterior Biodegrad 46:251–258

    Article  Google Scholar 

  • Tomaselli L, Lamenti G, Tiano P (2002) Chlorophyll fluorescence for evaluating biocide treatments against phototrophic biodeteriogens. Ann Microbiol 52:197–206

    CAS  Google Scholar 

  • Toniolo L, Zerbi CM, Bugini R (2009) Black layers on historical architecture. Environ Sci Pollut Res 16:218–226

    Article  CAS  Google Scholar 

  • Tretiach M, Bertuzzi S, Salvadori O (2008) In situ vitality monitoring of photosynthetic organisms by chlorophyll a fluorescence techniques. In: Tiano P, Pardini C (eds) In situ monitoring of monumental surfaces. Edifir, Firenze, pp 279–286

    Google Scholar 

  • 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 Biodeterior Biodegrad 64:452–460

    Article  CAS  Google Scholar 

  • Urzì C, Albertano P (2001) Studying phototrophic and heterotrophic microbial communities on stone monuments. In: Doyle RJ (ed) Methods in enzymology. Academic Press, San Diego, pp 340–355

    Google Scholar 

  • Urzì C, De Leo F, Donato P, La Cono V (2003) Multiple approaches to study the structure and diversity of microbial communities colonizing artistic surfaces. In: Saiz-Jimenez C (ed) Molecular biology and cultural heritage. Swets & Zeitlinger, Lisse, pp 187–194

    Google Scholar 

  • Videla HA, Herrera LK (2003) A comparative study on biodeterioration and weathering effects in three sites of the Latin American cultural heritage. In: Saiz-Jimenez C (ed) Molecular biology and cultural heritage. A.A. Balkema, Lisse, pp 253–258

    Google Scholar 

  • Videla HA, Guiamet PS, De Saravia SG (2000) Biodeterioration of Mayan archaeological sites in the Yucatan Peninsula, Mexico. Int Biodeterior Biodegrad 46:335–341

    Article  CAS  Google Scholar 

  • Villar SEJ, Edwards HGM, Seaward MRD (2004) Lichen biodeterioration of ecclesiastical monuments in northern Spain. Spectrochim Acta Part A 60:1229–1237

    Article  CAS  Google Scholar 

  • Von Wintzingerode F, Goebel UB, Stackerbrandt E (1997) Determination of microbial diversity in environmental samples-pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Article  Google Scholar 

  • Ward DM, Weller R, Bateson MM (1990) 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345:63–65

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Warscheid T, Petersen K, Krumbein WE (1990) A rapid method to demonstrate and evaluate microbial activity on decaying sandstone. Stud Conserv 35:137–147

    Article  Google Scholar 

  • Weibring P, Johansson T, Edner H, Svanberg S, Sundnér B, Raimondi V, Cecchi G, Pantani L (2001) Fluorescence lidar imaging of historical monuments. Appl Opt 40:6111–6120

    Article  CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  Google Scholar 

  • Welton RG, Cuthbert SJ, Mclean R, Hursthouse A, Hughes J (2003) A preliminary study of the phycological degradation of natural stone masonry. Environ Geochem Health 25:139–145

    Article  CAS  Google Scholar 

  • Welton M, Silva MR, Gaylarde C, Herrera LK, Anleo X, De Belie N, Modry S (2005) Techniques applied to the study of microbial impact on building materials. Mater Struct 38:883–893

    Article  CAS  Google Scholar 

  • White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62

    Article  Google Scholar 

  • White DC, Pinkart HC, Ringelberg DB (1997) Biomass measurements: biochemical approaches. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD, Walter MV (eds) Manual of environmental microbiology. American Society for Microbiology Press, Washington, DC, pp 91–101

    Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JH, White TJ (eds) PCR protocols—a guide to methods and applications. Academic, New York, pp 315–332

  • 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 63:1062–1065

    Article  CAS  Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    CAS  Google Scholar 

  • Zhang H, Parameswaran P, Badalamenti J, Rittmann BE, Krajmalnik-Brown R (2011) Integrating high-throughput pyrosequencing and quantitative real-time PCR to analyze complex microbial communities. In: Clifton NJ (ed) Methods molecular biology. Springer, Germany, pp 107–128

    Google Scholar 

  • Zimmermann J, Gonzalez JM, Saiz-Jimenez C (2005) Epilithic biofilms in Saint Callixtus Catacombs (Rome) harbour a broad spectrum of Acidobacteria. Antonie van Leeuwenhoek 89:203–208

    Article  Google Scholar 

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Dakal, T.C., Arora, P.K. Evaluation of potential of molecular and physical techniques in studying biodeterioration. Rev Environ Sci Biotechnol 11, 71–104 (2012). https://doi.org/10.1007/s11157-012-9264-0

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