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Laboratory-Induced Endolithic Growth in Calcarenites: Biodeteriorating Potential Assessment

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Abstract

This study is aimed to assess the formation of photosynthetic biofilms on and within different natural stone materials, and to analyse their biogeophysical and biogeochemical deterioration potential. This was performed by means of artificial colonisation under laboratory conditions during 3 months. Monitoring of microbial development was performed by image analysis and biofilm biomass estimation by chlorophyll extraction technique. Microscopy investigations were carried out to study relationships between microorganisms and the mineral substrata. The model applied in this work corroborated a successful survival strategy inside endolithic microhabitat, using natural phototrophic biofilm cultivation, composed by cyanobacteria and algae, which increased intrinsic porosity by active mineral dissolution. We observed the presence of mineral-like iron derivatives (e.g. maghemite) around the cells and intracellularly and the precipitation of hausmannite, suggesting manganese transformations related to the biomineralisation.

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References

  1. Alakomi HL, Arrien N, Gorbushina AA, Krumbein WE, Maxwell I, McCullagh C, Robertson P, Ross N, Saarela M, Valero J, Vendrell M, Young ME (2004) Inhibitors of biofilm damage on mineral materials (Biodam). In: Kwiatkowski D, Löfvendahl R (eds) Proceedings of the 10th International Congress on Deterioration and Conservation of Stone. ICOMOS, Stockholm, pp 399–406

    Google Scholar 

  2. Ariño X, Hernandez-Marine M, Saiz-Jimenez C (1997) Colonization of Roman tombs by calcifying cyanobacteria. Phycologia 36:366–373

    Article  Google Scholar 

  3. Ascaso C, Wierzchos J, Castello R (1998) Study of the biogenic weathering of calcareous litharenite stones caused by lichen and endolithic microorganisms. Int Biodeterior Biodegrad 42:29–38

    Article  CAS  Google Scholar 

  4. Ascaso C, Wierzchos J, Souza-Egipsy V, De los Ríos A, Delgado Rodrigues J (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 

  5. Bargar JR, Tebo BM, Pecher KH, Chiu V, Villinski JE, Tonner BP (2000) Kinetics and products on Mn oxide biomineralization by spores of the marine Bacillus sp. strain-1. Symposia papers presented before the division of Environment Chemistry American Chemical Society 40(2):491–493

    Google Scholar 

  6. Bartolini M, Ricci S, Del Signore G (2004) Release of photosynthetic pigments from epilithic biocenosis alter biocida treatments. In: Kwiatkowski D, Löfvendahl R (eds) Proceedings of the 10th International Congress on Deterioration and Conservation of Stone. ICOMOS, Stockholm, pp 519–526

    Google Scholar 

  7. Bell RA (1993) Cryptoendolithic algae of hot semiarid lands and deserts. J Phycol 29:133–139

    Article  Google Scholar 

  8. Bellinzoni AM, Caneva G, Ricci S (2003) Ecological trends in travertine colonisation by pioneer algae and plant communities. Int Biodeterior Biodegrad 51:203–210

    Article  Google Scholar 

  9. Brown G (1980) Associated minerals. In: Brindley GW, Brown G (eds) Crystal structures of clay minerals and their X-ray identification, vol 5. Mineralogical Society, London, pp 361–410

    Google Scholar 

  10. Büdel B, Weber B, Kühl M, Pfanz H, Sültemeyer D, Wessels D (2004) Reshaping of sandstone surfaces by cryptoendolithic cyanobacteria: bioalkalization causes chemical weathering in arid landscapes. Geobiology 3:261–268

    Article  Google Scholar 

  11. Caneva G, Nugari MP, Salvadori O (1991) Biology in the conservation of work of art. ICCROM, Rome, p 182

    Google Scholar 

  12. De Los Ríos A, Galván 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 

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

    PubMed  Google Scholar 

  14. Dixon J (1977) Minerals in soil environments. Soil Science Society of America, Wisconsin

    Google Scholar 

  15. Dorn R (1998) Rock coatings. Developments in Earth Surface Processes 6. Elsevier, Amsterdam

    Google Scholar 

  16. Fischer TB, Heaney PJ, Jang JH, Ross DE, Brantley SL, Post JE, Tien M (2008) Continuous time-resolved X-ray diffraction of the biocatalysed reduction of Mn oxide. American Mineralogist 93(11-12):1929–1932

    Article  CAS  Google Scholar 

  17. Friedmann EI (1982) Endolithic microorganisms in the Antarctic Cold Desert. Science 215:1045–1053

    Article  CAS  PubMed  Google Scholar 

  18. Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Petrol 51:475–478

    Google Scholar 

  19. Gonzalez I, Laiz L, Hermosin B, Caballero B, Incerti C, Saiz-Jimenez C (1999) Bacteria isolated from rock art paintings: the case of Atlanterra shelter (south Spain). J Microbiol Methods 36:123–127

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Guillitte O, Dreesen R (1995) Laboratory chamber studies and petrographical analysis as bioreceptivity assessment tools of building materials. Sci Total Environ 167:365–374

    Article  CAS  Google Scholar 

  22. Kaplan D, Christiaen D, Arad S (1987) Chelating properties of extracellular polysaccharides from Chlorella spp. Appl Environ Microbiol 53:2953–2956

    CAS  PubMed  Google Scholar 

  23. Krumbein WE (1983) Microbial geochemistry. Blackwell Scientific, Oxford

    Google Scholar 

  24. Krumbein WE (1992) Colour changes of building stones and their direct and indirect biological causes. Proceedings of 7th International congress on Deterioration and Conservation of Stone, Lisboa, pp 443–452

  25. Leite Magalhães S, Sequeira Braga MA, Ascaso C (1998) Pátinas biogénicas numa fachada granítica do edifício do Largo do Paço (Braga). Actas do V Congresso Nacional de Geologia, Tomo 84, Fas. 2, Lisboa, pp F-194-F-197

  26. Leite Magalhães S (2000) Biodeterioração de um monumento da cidade de Braga. Estudo microbiológico da pedra granítica. MScE thesis, Universidade do Minho, Braga, Portugal

  27. Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    Article  CAS  Google Scholar 

  28. McNamara CJ, Perry TD IV, Bearce KA, Hernandez-Duque G, Mitchell R (2006) Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. Microb Ecol 51:51–64

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. Miller AZ, Laiz L, Gonzalez JM, Dionisio A, Macedo MF, Saiz-Jimenez C (2008) Reproducing stone monument photosynthetic-based colonization under laboratory conditions. Sci Total Environ 405:278–285

    Article  CAS  PubMed  Google Scholar 

  31. Miller AZ, Leal N, Laiz L, Rogerio-Candelera MA, Gonzalez JM, Silva RJC, Dionísio A, Macedo MF, Saiz-Jimenez C (2010) Primary bioreceptivity of limestones used in Southern Europe monuments. In: Smith BJ, Gomez-Heras M, Viles HA, Cassar J (eds) Limestone in the built environment: Present day challenges for the preservation of the past. Geological Society of London, London, Special Publications 331:79–92

  32. Miller AZ, 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 

  33. Ortega-Calvo JJ, Hernandez-Marine M, Saiz-Jimenez C (1991) Biodeterioration of building materials by cyanobacteria and algae. Int Biodeterior 28:165–185

    Article  Google Scholar 

  34. Pohl W, Schneider J (2002) Impact of endolithic biofilms on carbonate rock surfaces. Geological Society, London, Special Publication, pp 177–194

  35. Robert M (1993) Rôle du facteur biologique dans la dégradation des roches et des monuments. In: Vincente Hernández MA, Molina Ballesteros E, Rives Arnau V (eds) Actas del workshop: Alteración de granitos y rocas afines, empleados como materiales de contrucción. CSIC, Madrid, pp 103–115

    Google Scholar 

  36. Rogerio-Candelera MA (2008) Una propuesta no invasiva para la documentación integral del arte rupestre. MScE thesis, Universidad de Sevilla, Spain

  37. Rogerio-Candelera MA, Laiz L, Saiz-Jimenez C (2008) Una experiencia de laboratorio para la separación de cubiertas en la documentación de pinturas rupestres y murales afectadas por biodeterioro. In: Saiz-Jimenez C, Rogerio-Candelera MA (eds) Novena Reunión de la Red Temática del CSIC de Patrimonio Histórico y Cultural “Avances recientes en la investigación sobre Patrimonio”. CSIC, Sevilla, pp 71–72

    Google Scholar 

  38. Rogerio-Candelera MA, Laiz L, González JM, Saiz-Jimenez C (2008) Monitorización del crecimiento microbiano en una tumba romana mediante técnicas de teledetección. In: Rovira S, Garcia-Heras M, Gener M, Montero I (eds) Actas del VII Congreso Ibérico de Arqueometría, CSIC, Madrid, pp 593–600

  39. Saiz-Jimenez C, Garcia-Rowe J, Garcia del Cura MA, Ortega-Calvo JJ, Roekens E, Van Grieten R (1990) Endolithic cyanobacteria in Maastricht limestone. Sci Total Environ 94:209–220

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  41. Salvadori O (2000) Characterization of endolithic communities of stone monuments and natural outcrops. In: Ciferri O, Tiano P, Mastromei G (eds) Of microbes and art—the role of microbial communities in the degradation and protection of cultural heritage. Kluwer Academic, New York, pp 89–101

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  44. Vollenweider RA, Talling JF, Westlake DF (1974) A manual on methods for measuring primary production in aquatic environments, 2nd edn. Blackwell, Oxford

    Google Scholar 

  45. Walker JJ, Spear JR, Pace NR (2005) Geobiology of a microbial endolithic community in the Yellowstone geothermal environment. Nature 434:1011–1014

    Article  CAS  PubMed  Google Scholar 

  46. Wierzchos J, Ascaso C (1994) Application of backscattered electron imaging to the study of the lichen-rock interface. Journal of Microsc-Oxford 175:54–59

    Google Scholar 

  47. Wilderer PA, Characklis WG (1989) Structure and function of biofilms. In: Characklis WG, Wildener PA (eds) Structure and function of biofilms. Wiley, Chichester, pp 5–17

    Google Scholar 

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Acknowledgements

This work was supported by the Ministério da Ciência, Tecnologia e Ensino Superior, Portugal, with a doctoral grant (SFRH/BD/21481/2005) and partially financed by the CEPGIST FCT subproject DECASTONE. The projects TCP CSD2007-00058 and 2007PT0041 are acknowledged. We also thank F. Pinto (CCMA, CSIC) for technical assistance and CA and JW thanks for support by grant CGL2007-62875/BOS from the Ministry of Science and Innovation of Spain and by PIE-631A from CSIC, Spain.

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Miller, A.Z., Rogerio-Candelera, M.A., Laiz, L. et al. Laboratory-Induced Endolithic Growth in Calcarenites: Biodeteriorating Potential Assessment. Microb Ecol 60, 55–68 (2010). https://doi.org/10.1007/s00248-010-9666-x

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