Advertisement

Biodeterioration of Roman hypogea: the case study of the Catacombs of SS. Marcellino and Pietro (Rome, Italy)

  • Laura BrunoEmail author
  • Lorenza Rugnini
  • Valeria Spizzichino
  • Luisa Caneve
  • Antonella Canini
  • Neil Thomas William Ellwood
Original Article
  • 21 Downloads

Abstract

No information exists on phototrophs growing on the stone surfaces of the Catacombs of SS. Marcellino and Pietro (the site was only recently opened to the public in 2014). Therefore, it was decided to characterise the microbial communities and to compare them with those of the other previously studied catacombs. Moreover, a new non-invasive strategy to reduce the phototrophic growth was tested. Phototrophic microorganisms were investigated under light and confocal laser scanning microscopes from samples collected non-invasively in situ. Tests were carried out to determine the effect of the application of two essential oils (from L. angustifolia and T. vulgaris) on biofilm photosynthetic activity. Laser-induced fluorescence (LIF) and reflectance measurements in the visible range have been used to evaluate respectively, any chemical modification and discolouration on a frescoed stone that may occur after the application of the essential oils. At all the concentrations of essential oils, there was a quasi-immediate, large reduction in photosynthetic activity of the biofilms. At 10% essential oil concentration, there was no detectable photosynthetic activity after 15 min. At 1%, there was a need for two applications and after 5-day activity was undetectable. No effect of the essential oils on the substrate surface properties or colour modification of the fresco has been observed with the LIF prototype. Cyanobacterial typical of Roman catacombs were present in the sites investigated. Innovative and non-destructive strategies, involving the application of a combination of two essential oils, have been successfully tested and developed to prevent biodeterioration of these sites.

Keywords

Biodeterioration Phototrophic biofilms Cyanobacteria Essential oils Laser-induced fluorescence 

Notes

Acknowledgments

The authors thank the ‘Pontificia Commissione of Archeologia Sacra’ for the permission to investigate the Catacombs of SS. Marcellino and Pietro and the centre ‘CMA-P Albertano’ for the use of the CLSM.

Funding

The work was partially funded by the project ADAMO in the frame of DTC (Technological District for Cultural Heritage) Lazio Det.reg. G08622.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

No humans or animals were used in this work.

Informed consent

N/A

References

  1. Albertano P (2012) Cyanobacterial biofilms in monuments and caves. In: Whitton (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Netherlands, pp 317–343CrossRefGoogle Scholar
  2. Albertano P, Bruno L (2003) The importance of light in the conservation of hypogean monuments. In: Saiz-Jimenez (ed) Molecular biology and cultural heritage. Swets & Zeitlinger, Lisse, pp 171–177 ISBN 90 5809 555XGoogle Scholar
  3. Albertano P, Pacchiani D, Capucci E (2004) The public response to innovative strategies for the control of biodeterioration in archaeological hypogea. J Cult Herit 5(4:399–407CrossRefGoogle Scholar
  4. Albertano P, Bruno L, Bellezza S (2005) New strategy for the monitoring and control of cyanobacterial films on valuable lithic faces. Plant Biosyst 139:311–322CrossRefGoogle Scholar
  5. Barresi G, Cammarata M, Palla F (2017) Biocide. In: Palla F, Barresi G (eds) Biotechnology and conservation of cultural heritage.  https://doi.org/10.1007/978-3-319-46168-7_3 Google Scholar
  6. Bilger W, Schreiber U, Bock M (1995) Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 102:425–432CrossRefGoogle Scholar
  7. Bruno L, Billi D, Bellezza S, Albertano P (2009) Cytomorphological and genetic characterization of troglophilic Leptolyngbya strains isolated from Roman hypogea. Appl Environ Microbiol 75:608–617CrossRefGoogle Scholar
  8. Bruno L, Bellezza S, De Leo F, Urzi C (2014a) A study for monitoring and conservation in the Roman catacombs of St. Callistus and Domitilla, Rome (Italy). In: Saiz-Jimenez (ed) The conservation of subterranean cultural heritage. CRC Press, pp 37–44 Chapter 5, ISBN 978-1-138-02694-0Google Scholar
  9. Bruno L, Ficorella I, Valentini F, Quici L, Keshari N, Adhikary SP (2014b) Characterization of phototrophic biofilms deteriorating Indian stone monuments, their response to heat stress and development of a non-invasive remediation strategy. In: Rogerio-Candelera MA (ed) Science, technology and cultural heritage. CRC Press/Balkema, The Netherlands, pp 205–210 ISBN 978-1-138-02744-2Google Scholar
  10. Bruno L, Quici L, Ficorella I, Valentini F (2014c) NanoGraphene oxide: a new material for a non-invasive and non-destructive strategy to remove biofilms from rock surfaces. In: Saiz-Jimenez C (ed) The conservation of subterranean cultural heritage. CRC Press, Taylor & Francis Group, London, pp 125–130, ISBN 978–1–138-02694-0.  https://doi.org/10.1201/b17570-17s2.0-84958762820 CrossRefGoogle Scholar
  11. Bruno L, Valle V (2017) Effect of white and monochromatic lights on cyanobacteria and biofilms from Roman Catacombs. Int Biodeter Biodegr 123:286-295CrossRefGoogle Scholar
  12. Bruno L, Valle V, Gismondi A, Di Marco G, Canini A (2018) Applicazione di oli essenziali come metodo non­-invasivo per il controllo del biodeterioramento di beni culturali in pietra. Notiz Soc Bot Ital 2:6–7Google Scholar
  13. Castenholz RW (2001) Phylum BX. Cyanobacteria. Oxygenic photosynthetic bacteria. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. Springer, New York, pp 473–487CrossRefGoogle Scholar
  14. Chelius MK, Beresford G, Horton H, Quirk M, Selby G, Simpson RT, Horrocks R, Moore JC (2009) Impacts of alterations of organic inputs on the bacterial community within the sediments of wind cave, South Dakota, USA. Int J Speleol 38:1–10CrossRefGoogle Scholar
  15. Fernandes C, Barros S, Galhano V, Geraldes AM (2014) Searching for algaecide or algaestatic effects of several plant extracts on phytoplankton: preliminary results. Br Biotechnol J 4(10):1077–1087CrossRefGoogle Scholar
  16. Giovannini D, Gismondi A, Basso L, Canuti L, Braglia R, Canini A, Mariani F, Cappelli G (2016) Lavandula angustifolia Mill. Essential oil exerts antibacterial and anti-inflammatory effect in macrophage mediated immune response to Staphylococcus aureus. Immunol Investig 45(1):11–28CrossRefGoogle Scholar
  17. Guiamet PS, de la Paz NJ, Arenas PM, Gómez de Saravia SG (2008) Differential sensitivity of Bacillus sp. isolated from archive materials to plant extracts. Pharmacologyonline 3:649–658Google Scholar
  18. Hernández-Máriné M, Clavero E, Roldán M (2003) Why there is such luxurious growth in the hypogean environments. Algol Stud 109(1):229–239CrossRefGoogle Scholar
  19. Hsieh P, Pedersen JZ, Bruno L (2014) Photoinhibition of cyanobacteria and its application in cultural heritage conservation. Photochem Photobiol 90:533–543CrossRefGoogle Scholar
  20. Kim AR, Kim HS, Park SO (2011) Measuring of the perceptibility and acceptability in various color quality measures. J Opt Soc Korea 15(3):310–317CrossRefGoogle Scholar
  21. Krakova L, De Leo F, Bruno L, Pangallo D, Urzì C (2015) Complex bacterial diversity in the white biofilms of St. Callistus catacombs in Rome evidenced by different investigation strategies. Environ Microbiol 17(5):1738–1752CrossRefGoogle Scholar
  22. Mann CM, Markham JL (1998) A new method for determining the minimum inhibitory concentration of essential oils. J Appl Microbiol 84:538–544CrossRefGoogle Scholar
  23. Marshall WA, Chalmers MO (1997) Airborne dispersal of Antarctic terrestrial algae and cyanobacteria. Ecography 20(6):585–594CrossRefGoogle Scholar
  24. Martinez JR, Nieto-Villena A, de la Cruz-Mendoza JA, Ortega-Zarzosa G, Guerrero AL (2017) Monitoring the natural aging degradation of paper by fluorescence. J Cult Herit 26:22–27.  https://doi.org/10.1016/j.culher.2017.01.011 CrossRefGoogle Scholar
  25. Moghimi R, Aliahmadi A, Rafati H (2017) Antibacterial hydroxypropyl methyl cellulose edible films containing nanoemulsions of Thymus daenensis essential oil for food packaging. Carbohydr Polym 175:241–248CrossRefGoogle Scholar
  26. Nevin A, Spoto G, Anglos D (2012) Laser spectroscopies for elemental and molecular analysis in art and archeology. Appl Phys A Mater Sci Process 106(2):339–361CrossRefGoogle Scholar
  27. Palombi L, Alderighi D, Cecchi G, Raimondi V, Toci G, Lognoli D (2013) A fluorescence LIDAR sensor for hyper-spectral time-resolved remote sensing and mapping. Opt Express 21:14737–14746CrossRefGoogle Scholar
  28. Pozo-Antonio JS, Montojo C, Lopez de Silanes ME, de Rosario I, Rivas T (2017) In situ evaluation by colour spectrophotometry of cleaning and protective treatments in granitic cultural heritage. Int Biodeterior Biodegrad 123:251–261CrossRefGoogle Scholar
  29. Puškárová A, Bučková M, Kraková, Pangallo D, Kozics K (2017) The antibacterial and antifungal activity of six essential oils and their cyto/genotoxicity to human HEL 12469 cells. Sci Rep 7(8211):1–11Google Scholar
  30. Rippka R, Deruelles J, Waterbury B, Herdman M, Stanier R (1979) Generic assignments, strains histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  31. Ruffolo SA, De Leo F, Ricca M, Arcudi A, Silvestri C, Bruno L, Urzì C, La Russa MF (2017) Medium-term in situ experiment by using organic biocides and titanium dioxide for the mitigation of microbial colonization on stone surfaces. Int Biodeterior Biodegrad 123:17–26CrossRefGoogle Scholar
  32. Saiz-Jimenez C, Cuezva S, Jurado V, Fernandez-Cortes A, Porca E, Benevante D, Cañaveras JC, Sanchez-Moral S (2011) Paleolithic art in peril: policy and science collide at Altamira Cave. Science 334:42–43CrossRefGoogle Scholar
  33. Sanchez-Moral S, Luque S, Cuezva S, Soler V, Benavente D, Laiz L, Gonzàlez JM, Saiz-Jimenez C (2005) Deterioration of building materials in Roman catacombs: the influence of visitors. Sci Total Environ 349:260–276CrossRefGoogle Scholar
  34. Sanchez-Moral S, Cañaveras JC, Benavente D, Fernandez-Cortes A, Cuezva S, Elez J, Jurado V, Rogerio-Candelera MA, Saiz-Jimenez C (2018) A study in the state of conservation of the Roman Necropolis of Carmona (Sevilla, Spain). J Cult Herit 34:185–197CrossRefGoogle Scholar
  35. Sanmartín P, Villa F, Polo A, Silva B, Prieto B, Cappitelli F (2015) Rapid evaluation of three biocide treatments against the cyanobacterium Nostoc sp. PCC 9104 by color changes. Ann Microbiol 2–65Google Scholar
  36. Sanmartín P, De Araujo A, Vasanthakumar A (2018) Melding the old with the new: trends in methods used to identify, monitor and control microorganisms on cultural heritage materials. Microb Ecol 76:64–80CrossRefGoogle Scholar
  37. Sasso S, Miller AZ, Rogerio-Candelera MA, Cubero B, Coutinho ML, Scrano L, Bufo SA (2016) Potential of natural biocides for biocontrolling phototrophic colonization on limestone. Int Biodeterior Biodegrad 107:102–110CrossRefGoogle Scholar
  38. Schreiber U, Bilger W (1993) Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. Prog Bot 54:151–173Google Scholar
  39. Spizzichino V, Angelini F, Caneve L, Colao F, Corrias R, Ruggiero L (2015) In situ study of modern synthetic materials and pigments in contemporary paintings by laser-induced fluorescence scanning. Stud Conserv 60(1):178–184CrossRefGoogle Scholar
  40. Stupar M, Grbić MLJ, Džamić A, Unković N, Ristić M, Jelikić A, Vukojević J (2014) Antifungal activity of selected essential oils and biocide benzalkonium chloride against the fungi isolated from cultural heritage objects. S Afr J Bot 93:118–124CrossRefGoogle Scholar
  41. Targowski P, Walczak M, Pouli P (2017) Lasers in the Conservation of Artworks XI. In: Targowski P, Walczak M, Pouli P (eds) Proceedings of the International Conference LACONA XI, Kraków, Poland, 20–23 September 2016, NCU Press, Toruń.  https://doi.org/10.12775/3875-4
  42. Toreno G, Isola D, Meloni P, Carcangiu G, Selbmann L, Onofri S, Caneva G, Zucconi L (2018) Biological colonization on stone monuments: a new low impact cleaning method. J Cult Herit 30:100–109CrossRefGoogle Scholar
  43. UNI EN 15886 (2010) Conservation of cultural property—test methods—colour measurement of surfaces. UNI Ente Nazionale Italiano di UnificazioneGoogle Scholar
  44. Urzì C, De Leo F (2001) Sampling with adhesive tape strips: an easy and rapid method to monitor microbial colonization on monument surfaces. J Microbiol Methods (44):1–11Google Scholar
  45. Urzì C, De Leo F, Bruno L, Albertano P (2010) Microbial diversity in Paleolithic Caves: a study case on the phototrophic biofilms of the cave of bats (Zuheros, Spain). Microb Ecol 60:116–129CrossRefGoogle Scholar
  46. Urzì C, De Leo F, Bruno L, Pangallo D, Krakova L (2014) New species description, biomineralization processes and biocleaning applications of Roman catacombs-living bacteria. In: Saiz-Jimenez C (ed) The conservation of subterranean cultural heritage. CRC Press, Taylor & Francis Group, London, pp 65–72, ISBN 978-1-138-02694-0.  https://doi.org/10.1201/b17570-10 CrossRefGoogle Scholar
  47. Urzì C, De Leo F, Krakova L, Pangallo D, Bruno L (2016) Effects of biocide treatments on the biofilm community in Domitilla’s catacombs in Rome. Sci Total Environ 572(1):252–262CrossRefGoogle Scholar
  48. Zammit G, Billi D, Albertano P (2012) The subaerophytic cyanobacterium Oculatella subterranea (Oscillatoriales, Cyanophyceae) gen. et sp. nov.: a cytomorphological and molecular description. Eur J Phycol 47(4):341–354CrossRefGoogle Scholar

Copyright information

© Università degli studi di Milano 2019

Authors and Affiliations

  1. 1.Laboratory of Biology of Algae, Department of BiologyUniversity of Rome ‘Tor Vergata’RomeItaly
  2. 2.ENEA—Italian National Agency for New Technologies, Energy and Sustainable Economic Development, FSN-TECFIS-DIM Diagnostic and Metrology Laboratory, Research Centre of FrascatiFrascatiItaly
  3. 3.Laboratory of Botany, Department of BiologyUniversity of Rome ‘Tor Vergata’RomeItaly
  4. 4.Department of ScienceUniversity of Roma TreRomeItaly

Personalised recommendations