Diversity and Biomineralization Potential of the Epilithic Bacterial Communities Inhabiting the Oldest Public Stone Monument of Cluj-Napoca (Transylvania, Romania)
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
28326074
PubMed Central
PMC5339310
DOI
10.3389/fmicb.2017.00372
Knihovny.cz E-zdroje
- Klíčová slova
- bacterial cultivation, calcite, carbonatogenesis, epilithic microbiota, limestone statue, vaterite,
- Publikační typ
- časopisecké články MeSH
In this study, we investigated the biomineralization potential and diversity of the epilithic bacterial communities dwelling on the limestone statue of Saint Donatus, the oldest public monument of Cluj-Napoca city (Transylvania region, NW Romania). Their spatial distribution together with phylogenetic and metabolic diversity, as well as their capacity to precipitate calcium carbonate was evaluated by combining molecular and phenotypic fingerprinting methods with X-ray diffraction, Fourier transform infrared spectroscopy, and scanning electron-microscopy analyses. The results of real-time quantitative PCR, molecular fingerprinting and community-level physiological profiling showed that diverse and abundant bacterial assemblages that differ in relation to their collection site colonized the statue. The cultivation and molecular identification procedures allowed the characterization of 79 bacterial isolates belonging to Proteobacteria (73.4%), Firmicutes (19%), and Actinobacteria (7.6%). Amongst them, the 22 strains identified as being capable of calcium carbonate precipitation were found to belong mostly to Bacillus and Pseudomonas genera. We found that bacteria acted as nucleation sites, inducing the formation of nanoscale aggregates that were shown to be principally composed of vaterite. Furthermore, we expanded the current knowledge on culturable diversity of carbonatogenic bacteria by providing evidence for biogenic vaterite/calcite formation mediated by: Pseudomonas synxantha, P. graminis, Brevibacterium iodinum, Streptomyces albidoflavus, and Stenotrophomonas chelatiphaga. Overall, this study highlights the need to evaluate the carbonatogenetic potential of all the bacterial communities present on stone artwork prior to designing an efficient conservation treatment based on biomineralization.
Department of Geology Babeş Bolyai University Cluj Napoca Romania
Faculty of Physics Babeş Bolyai University Cluj Napoca Romania
Zobrazit více v PubMed
Asnicar F., Weingart G., Tickle T. L., Huttenhower C., Segata N. (2015). Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PubMed DOI PMC
Balog A.-A., Cobîrzan N., Mosonyi E. (2014). Microstructural analysis for investigation of limestone damages - a case study of the Fortress Wall of Cluj-Napoca, Romania.
Banciu H. L. (2013). Diversity of endolithic prokaryotes living in stone monuments.
Banks E. D., Taylor N. M., Gulley J., Lubbers B. R., Giarrizzo J. G., Bullen H. A., et al. (2010). Bacterial calcium carbonate precipitation in cave environments: a function of calcium homeostasis. DOI
Baskar S., Baskar R., Lee N., Theophilus P. K. (2008). Speleothems from Mawsmai and Krem Phyllut caves, Meghalaya, India: some evidences on biogenic activities. DOI
Baskar S., Baskar R., Mauclaire L., McKenzie J. A. (2006). Microbially induced calcite precipitation in culture experiments: possible origin for stalactites in Sahastradhara caves, Dehradun, India.
Ben Chekroun K., Rodriguez-Navarro C., Gonzalez-Munoz M. T., Arias J. M., Cultrone G., Rodriguez-Gallego M. (2004). Precipitation and growth morphology of calcium carbonate induced by DOI
Boquet E., Boronat A., Ramos-Cormenzana A. (1973). Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. DOI
Brânzilă M., Ştefan P. (2009). Golia monastery from Iasi (Romania) - alteration and deterioration of the building limestones. DOI
Braun B., Böckelmann U., Grohmann E., Szewzyk U. (2006). Polyphasic characterization of the bacterial community in an urban soil profile with in situ and culture-dependent methods. DOI
Buck J. D. (1982). Nonstaining (KOH) method for determination of gram reactions of marine bacteria. PubMed PMC
Cameotra S., Dakal T. (2012). Carbonatogenesis: microbial contribution to the conservation of monuments and artwork of stone. DOI
Cañveras J. C., Sanchez-Moral S., Sloer V., Saiz-Jimenez C. (2001). Microorganisms and microbially induced fabrics in cave walls. DOI
Chou C.-W., Seagren E. A., Aydilek A. H., Lai M. (2011). Biocalcification of sand through ureolysis. DOI
Cole J. R., Wang Q., Cardenas E., Fish J., Chai B., Farris R. J., et al. (2009). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. PubMed DOI PMC
Cole J. R., Wang Q., Fish J. A., Chai B., McGarrell D. M., Sun Y., et al. (2014). Ribosomal Database Project: data and tools for high throughput rRNA analysis. PubMed DOI PMC
Daskalakis M. I., Rigas F., Bakolas A., Magoulas A., Kotoulas G., Katsikis I., et al. (2015). Vaterite bio-precipitation induced by DOI
Dhami N. K., Reddy M. S., Mukherjee A. (2013). Biomineralization of calcium carbonate polymorphs by the bacterial strains isolated from calcareous sites. PubMed DOI
Dhami N. K., Reddy M. S., Mukherjee A. (2014a). Synergistic role of bacterial urease and carbonic anhydrase in carbonate mineralization. PubMed DOI
Dhami N. K., Sudhakara Reddy M., Mukherjee A. (2014b). Application of calcifying bacteria for remediation of stones and cultural heritages. PubMed DOI PMC
Ettenauer J., Piñar G., Sterflinger K., Gonzalez-Muñoz M. T., Jroundi F. (2011). Molecular monitoring of the microbial dynamics occurring on historical limestone buildings during and after the in situ application of different bio-consolidation treatments. PubMed DOI PMC
Ferrer M. R., Quevedo-Sarmiento J., Rivadeneyra M. A., Bejar V., Delgado R., Ramos-Cormenzana A. (1988). Calcium carbonate precipitation by two groups of moderately halophilic microorganisms at different temperatures and salt concentrations. DOI
Gebauer D., Gunawidjaja P. N., Ko J. Y. P., Bacsik Z., Aziz B., Liu L., et al. (2010). Proto-calcite and proto-vaterite in amorphous calcium carbonates. PubMed DOI
Gil E., Mas Á., Lerma C., Vercher J. (2015). Exposure factors influence stone deterioration by crystallization of soluble salts. DOI
González-Muñoz M. T., Rodriguez-Navarro C., Martínez-Ruiz F., Arias J. M., Merroun M. L., Rodriguez-Gallego M. (2010). Bacterial biomineralization: new insights from DOI
Gorbushina A. A. (2007). Life on the rocks. PubMed DOI
Jagadeesha Kumar B. G., Prabhakara R., Pushpa H. (2013). Biomineralization of calcium carbonate by different bacterial strains and their application in concrete crack remediation.
Jimenez-Lopez C., Jroundi F., Pascolini C., Rodriguez-Navarro C., Piñar-Larrubia G., Rodriguez-Gallego M., et al. (2008). Consolidation of quarry calcarenite by calcium carbonate precipitation induced by bacteria activated among the microbiota inhabiting the stone. DOI
Jroundi F., Gómez-Suaga P., Jimenez-Lopez C., González-Muñoz M. T., Fernandez-Vivas M. A. (2012). Stone-isolated carbonatogenic bacteria as inoculants in bioconsolidation treatments for historical limestone. PubMed DOI
Jroundi F., Gonzalez-Muñoz M. T., Garcia-Bueno A., Rodriguez-Navarro C. (2014). Consolidation of archaeological gypsum plaster by bacterial biomineralization of calcium carbonate. PubMed DOI
Kiel G., Gaylarde C. C. (2006). Bacterial diversity in biofilms on external surfaces of historic buildings in Porto Alegre. DOI
Koch R., Racataianu P. C., Bucur I. (2008). Examples of weathering and deterioration of Tertiary building stones at St. Michaels Cathedral in Cluj-Napoca (Romania). DOI
Laiz L., Groth I., Gonzalez I., Saiz-Jimenez C. (1999). Microbiological study of the dripping waters in Altamira cave (Santillana del Mar, Spain). PubMed DOI
Lan W., Li H., Wang W. D., Katayama Y., Gu J. D. (2010). Microbial community analysis of fresh and old microbial biofilms on Bayon Temple sandstone of Angkor Thom, Cambodia. PubMed DOI PMC
Le Métayer-Levrel G., Castanier S., Orial G., Loubière J.-F.,, Perthuisot J.-P. (1999). Applications of bacterial carbonatogenesis to the protection and regeneration of limestones in buildings and historic patrimony. DOI
Lisci M., Monte M., Pacini E. (2003). Lichens and higher plants on stone: a review. DOI
López-Moreno A., Sepúlveda-Sánchez J. D., Alonso Guzmán E. M., Le Borgne S. (2014). Calcium carbonate precipitation by heterotrophic bacteria isolated from biofilms formed on deteriorated ignimbrite stones: influence of calcium on EPS production and biofilm formation by these isolates. PubMed DOI
Mann S. (2001).
McNamara C. J., Perry T. D., Bearce K. A., Hernandez-Duque G., Mitchell R. (2006). Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. PubMed DOI
Miller A. Z., Sanmartín P., Pereira-Pardo L., Dionísio A., Saiz-Jimenez C., Macedo M. F., et al. (2012). Bioreceptivity of building stones: a review. PubMed DOI
Okwadha G. D. O., Li J. (2010). Optimum conditions for microbial carbonate precipitation. PubMed DOI
Ortega-Morales B. O., Narváez-Zapata J. A., Schmalenberger A., Sosa-López A., Tebbe C. C. (2004). Biofilms fouling ancient limestone Mayan monuments in Uxmal, Mexico: a cultivation-independent analysis. DOI
Pentecost A., Whitton B. A. (eds) (2000). “Limestones,” in DOI
Rodriguez-Navarro C., Jimenez-Lopez C., Rodriguez-Navarro A., Gonzalez-Muñoz M. T., Rodriguez-Gallego M. (2007). Bacterially mediated mineralization of vaterite. DOI
Rodriguez-Navarro C., Rodriguez-Gallego M., Ben Chekroun K., Gonzalez-Muñoz M. T. (2003). Conservation of ornamental stone by PubMed DOI PMC
Ruijter J. M., Ramakers C., Hoogaars W. M. H., Karlen Y., Bakker O., van den Hoff M. J. B., et al. (2009). Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. PubMed DOI PMC
Rusznyák A., Akob D. M., Nietzsche S., Eusterhues K., Totsche K. U., Neu T. R., et al. (2012). Calcite biomineralization by bacterial isolates from the recently discovered pristine karstic herrenberg cave. PubMed DOI PMC
Sabãu I. (2002).
Saiz-Jimenez C. (1997). Biodeterioration vs biodegradation: the role of microorganisms in the removal of pollutants deposited on historic buildings. DOI
Sato M., Matsuda S. (1969). Structure of vaterite and infrared spectra. DOI
Scheerer S., Ortega-Morales O., Gaylarde C. (2009). Microbial deterioration of stone monuments–an updated overview. PubMed DOI
Seifan M., Samani A. K., Berenjian A. (2016). Induced calcium carbonate precipitation using PubMed DOI
Shirakawa M. A., Cincotto M. A., Atencio D., Gaylarde C. C., John V. M. (2011). Effect of culture medium on biocalcification by PubMed DOI PMC
Silva-Castro G. A., Uad I., Rivadeneyra A., Vilchez J. I., Martin-Ramos D., González-López J., et al. (2013). Carbonate precipitation of bacterial strains isolated from sediments and seawater: formation mechanisms. DOI
Smalla K., Oros-Sichler M., Milling A., Heuer H., Baumgarte S., Becker R., et al. (2007). Bacterial diversity of soils assessed by DGGE, T-RFLP and SSCP fingerprints of PCR-amplified 16S rRNA gene fragments: Do the different methods provide similar results? PubMed DOI
Sondi I., Juraěić M. (2010). Whiting events and the formation of aragonite in Mediterranean karstic marine lakes: new evidence on its biologically induced inorganic origin. DOI
Steiger M., Charola A. E., Sterflinger K. (2014). “Weathering and deterioration,” in DOI
Stocks-Fischer S., Galinat J. K., Bang S. S. (1999). Microbiological precipitation of CaCO3. DOI
Suihko M. L., Alakomi H. L., Gorbushina A., Fortune I., Marquardt J., Saarela M. (2007). Characterization of aerobic bacterial and fungal microbiota on surfaces of historic Scottish monuments. PubMed DOI
Tourney J., Ngwenya B. T. (2014). The role of bacterial extracellular polymeric substances in geomicrobiology. DOI
Vagenas N. V., Gatsouli A., Kontoyannis C. G. (2003). Quantitative analysis of synthetic calcium carbonate polymorphs using FT-IR spectroscopy. PubMed DOI
Walsh J. H. (2001). Ecological considerations of biodeterioration. DOI
Warscheid T., Braams J. (2000). Biodeterioration of stone: a review. DOI
Wei H., Shen Q., Zhao Y., Wang D.-J., Xu D.-F. (2003). Influence of polyvinylpyrrolidone on the precipitation of calcium carbonate and on the transformation of vaterite to calcite. DOI
Zhu T., Dittrich M. (2016). Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: a review. PubMed DOI PMC
Succession, Replacement, and Modification of Chicken Litter Microbiota