Journal of Wood Science

, Volume 64, Issue 4, pp 417–426 | Cite as

Heterotrophic components of biofilms on wood artefacts

  • Paola CennamoEmail author
  • Maria Rosaria Barone Lumaga
  • Claudia Ciniglia
  • Ottavio Soppelsa
  • Aldo Moretti
Original Article


Heterotrophic components of biofilms on wood artefacts were studied at the Conservation Laboratory for Wood Artefacts of the University Suor Orsola Benincasa of Naples, Italy. The aim of the study was to add new information on the micro-habitats represented by biofilms formed by wood-dwelling organisms. Light and electron microscopy of histological features of woods used to make the artefacts showed that the woods belonged to species of lime (Tilia sp.), poplar (Populus sp.) and pear (Pyrus sp.). A Denaturing Gradient Gel Electrophoresis analysis performed on heterotrophic microorganisms colonizing the artefacts led to identify four species of bacteria, namely Bacillus cereus, B. mycoides, B. subtilis and Microbacterium oleivorans, and seven species of fungi, namely Alternaria alternata, Aspergillus fumigans, A. versicolor, Cladosporium cladosporioides, C. oxysporum, Fusarium oxysporum and Penicillium chrysogenum. Based on its morphological features, an insect found on some artefacts was identified as the xylophagous beetle Nicobium castaneum (Anobiidae). The influence of wood type and environmental conditions on the diversity of microorganisms was discussed.


Bacteria Biofilm Fungi Insects Wood 



The authors thank the personnel at the Conservation Laboratory for Wood Artefacts of the University Suor Orsola Benincasa of Naples, Italy. In particular, authors are grateful to its director, Professor Giancarlo Fatigati, for the collaboration provided and for making all facilities available in the course of this study. The authors also thank Professor Paolo Caputo for his valuable suggestions. Finally, the authors thank the anonymous reviewers for their constructive comments.


  1. 1.
    Caneva G, Nugari MP, Salvadori O (2009) Plant biology for cultural heritage: biodeterioration and conservation. The Getty Conservation Institute, Los AngelesGoogle Scholar
  2. 2.
    Ciferri O (1999) Microbial degradation of paintings. Appl Environ Microbiol 65:879–885PubMedPubMedCentralGoogle Scholar
  3. 3.
    Cennamo P, Marzano C, Ciniglia C, Pinto G, Cappelletti P, Caputo P, Pollio A (2012) A survey of the algal flora of anthropogenic caves of Campi Flegrei (Naples, Italy) archeological district. J Caves Karst Stud 74:243–250CrossRefGoogle Scholar
  4. 4.
    Cennamo P, Caputo P, Giorgio A, Moretti A, Pasquino N (2013) Biofilms on tuff stones at historical sites: identification and removal by nonthermal effects of radiofrequencies. Microb Ecol 66:659–668CrossRefGoogle Scholar
  5. 5.
    Cennamo P, Caputo P, Marzano C, Miller AZ, Saiz-Jimenez C, Moretti A (2016) Diversity of phototrophic components in biofilms from piperno historical stoneworks. Plant Biosyst 150:720–729CrossRefGoogle Scholar
  6. 6.
    Cennamo P, Montuori N, Trojsi G, Fatigati G, Moretti A (2016) Biofilms in churches built in grottoes. Sci Total Environ 543:727–738CrossRefGoogle Scholar
  7. 7.
    Capodicasa S, Fedi S, Porcelli AM, Zannoni D (2010) The microbial community dwelling on a biodeteriorated 16th century painting. Int Biodeterior Biodegrad 64:727–733CrossRefGoogle Scholar
  8. 8.
    Seves AM, Sora S, Ciferri O (1996) The microbial colonization of oil paintings. A laboratory investigation. Int Biodeterior Biodegrad 37:215–224CrossRefGoogle Scholar
  9. 9.
    Sterflinger K, Piñar G (2013) Microbial deterioration of cultural heritage and works of art—tilting at windmills? Appl Microbiol Biotechnol 97:9637–9646CrossRefGoogle Scholar
  10. 10.
    Indrayani Y, Yoshimura T, Imamura Y (2008) A novel control strategy for dry-wood termite Incisitermes minor infestation using a bait system. J Wood Sci 54:220–224CrossRefGoogle Scholar
  11. 11.
    Horisawa S, Sakuma Y, Chen K, Doi S (2002) Effects of wood species on degradation rates and bacterial communities in a small-scale biodegradation system for garbage using wood matrices. J Wood Sci 48:232–236CrossRefGoogle Scholar
  12. 12.
    Clausen CA (1996) Bacterial associations with decaying wood: a review. Int Biodeterior Biodegrad 37:101–107CrossRefGoogle Scholar
  13. 13.
    Dicus DH (2000) One response to a collection-wide mold outbreak: how bad can it be, how good can it get? J Am Inst Conserv 39:85–105Google Scholar
  14. 14.
    Florian ML (1993) Conidial fungi (mould) activity on artifact materials: a new look at prevention, control and eradication, pp 868–874. In: ICOM, committee for conservation, tenth triennial meeting, Washington DC Accessed 28 Feb 2017
  15. 15.
    Schmidt O (2007) Indoor wood-decay basidiomycetes: damage, causal fungi, physiology, identification and characterization, prevention and control. Mycol Prog 6:261–279CrossRefGoogle Scholar
  16. 16.
    Kaarakainen P, Rintala H, Vepsäläinen A, Hyvärinen A, Nevalainen A, Meklin T (2009) Microbial content of house dust samples determined with qPCR. Sci Total Environ 407:4673–4680CrossRefGoogle Scholar
  17. 17.
    Griffin DH (1996) Fungal physiology. Wiley, New YorkGoogle Scholar
  18. 18.
    Štafura A, Nagy Š, Bučková M, Puškárová A, Kraková L, Čulík M, Nagy Š, Beronská N, Pangallo D (2017) The influence of microfilamentous fungi on wooden organ pipes: one year investigation. Int Biodeterior Biodegrad 121:139–147CrossRefGoogle Scholar
  19. 19.
    Cotter DA (1981) Spore activation. In: Turian G, Hohl HR (eds) The fungal spore. Academic Press, New York, pp 385–411Google Scholar
  20. 20.
    Lupan I, Ianc MB, Kelemen BS, Carpa R, Rosca-Casian O, Chiriac MT, Popescu O (2014) New and old microbial communities colonizing a seventeenth-century wooden church. Folia Microbiol 59:45–51CrossRefGoogle Scholar
  21. 21.
    Pangallo D, Chovanová K, Šimonovičová A, Ferianc P (2009) Investigation of microbial community isolated from indoor artworks and air environment: identification, biodegradative abilities, and DNA typing. Can J Microbiol 55:277–287CrossRefGoogle Scholar
  22. 22.
    Pangallo D, Šimonovičová A, Chovanová K, Ferianc P (2007) Wooden art objects and the museum environment: identification and biodegradative characteristics of isolated microflora. Lett Appl Microbiol 45:87–94CrossRefGoogle Scholar
  23. 23.
    Pangallo D, Bučková M, Kraková L, Puškárová A, Šaková N, Grivalský T, Chovanová K, Zemánková M (2015) Biodeterioration of epoxy resin: a microbial survey through culture-independent and culture-dependent approaches. Environ Microbiol 17:462–479CrossRefGoogle Scholar
  24. 24.
    Liotta G, Leto Barone G (1989) Methods for the preservation of wooden handworks of artistic and historical interest from the attacks of xylophagous insects (in Italian). In: Tampone G (ed) Restauro del legno. Nardini, Firenze, pp 215–233Google Scholar
  25. 25.
    Brues CT (1936) Evidences of insect activity preserved in fossil wood. J Paleontol 10:637–643Google Scholar
  26. 26.
    Chiappini E, Liotta G, Raguzzini MC, Battisti A (2001) Insects and restoration. Wood, paper, canvas, leather and other materials (in Italian). Calderini, BolognaGoogle Scholar
  27. 27.
    Schabereiter-Gurtner C, Piñar G, Lubitz W, Rölleke S (2001) An advanced molecular strategy to identify bacterial communities on art objects. J Microbiol Methods 45:77–87CrossRefGoogle Scholar
  28. 28.
    Schettini A, Fatigati G, Cennamo P, Moretti A (2010–2011) (Published in 2016) Identification and removal of biodeteriogens on a polychrome wood sculpture, Delpinoa 52–53:47–56. Accessed 28 Feb 2017
  29. 29.
    Borrelli G (2004) The Neapolitan nativity (in Italian). Edizioni Banco di Roma, RomaGoogle Scholar
  30. 30.
    Fittipaldi T (1980) Neapolitan sculpture of the eighteenth century (in Italian). Liguori, NapoliGoogle Scholar
  31. 31.
    Leone De Castris P, Middione R (1986) The painting of the Girolamini (in Italian). Guida, NapoliGoogle Scholar
  32. 32.
    Fatigati G (2010) The arts of wood: nature, property and problems of materials in the preservation of art works (in Italian). Quaderni della ricerca scientifica, Serie Beni Culturali, 17. Published by Università degli Studi Suor Orsola Benincasa di Napoli, Naples, ItalyGoogle Scholar
  33. 33.
    Berti S, Lazzeri S, Macchioni N, Sozzi L (2002) Xylotheca Project. Wood database and software for identification of species by dichotomous keys. Version for MS-Windows operating systems (in Italian). I.Va.L.S.A. G. L. Vottero, Ecodata, Italy Accessed February 2017
  34. 34.
    Schweingruber FH (1990) Anatomie Europäischer Hölzer. Ein Atlas zur Bestimmung europäischer Baum-, Strauch- und Zwergstrauchhölzer (in Germany). Paul Haupt, BernGoogle Scholar
  35. 35.
    Milanesi C, Baldi F, Vignani R, Ciampolini F, Faleri C, Cresti M (2006) Fungal deterioration of medieval wall fresco determined by analysing small fragments copper. Int Biodeterior Biodegrad 57:7–13CrossRefGoogle Scholar
  36. 36.
    Norris JR, Ribbons DW (1969) Methods in microbiology, vol 1. Academic Press, LondonGoogle Scholar
  37. 37.
    Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62:293–300PubMedPubMedCentralGoogle Scholar
  38. 38.
    Doyle JJ (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  39. 39.
    Neefs JM, Van de Peer Y, Hendriks L, De Wachter R (1990) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 18:2237–2317CrossRefGoogle Scholar
  40. 40.
    White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, Orlando, pp 315–322Google Scholar
  41. 41.
    Muyzer G, de Waal EAC, 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 59:695–700PubMedPubMedCentralGoogle Scholar
  42. 42.
    Teske A, Wawer C, Muyzer G, Ramsing NB (1996) Distribution of sulfate-reducing bacteria in a stratified fjord (Mariager Fjord, Denmark) as evaluated by most-probable-number counts and denaturing gradient gel electrophoresis of PCR-amplified ribosomal DNA fragments. Appl Environ Microbiol 62:1405–1415PubMedPubMedCentralGoogle Scholar
  43. 43.
    Buchan A, Newell SY, Moreta JIL, Moran MA (2002) Analysis of internal transcribed spacer (ITS) regions of rRNA genes in fungal communities in a south-easternU.S. salt marsh. Microb Ecol 43:329–340CrossRefGoogle Scholar
  44. 44.
    Michaelsen A, Pinzari F, Ripka K, Lubitz K, Piñar G (2006) Application of molecular techniques for the identification of fungal communities colonising paper material. Int Biodeterior Biodegrad 58:133–141CrossRefGoogle Scholar
  45. 45.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, 41. Nucleic Acids Symposium Series, Oxford University Press, pp 95–98Google Scholar
  46. 46.
    Ministero per i Beni e le Attività Culturali (2001) Scientific technical criteria and standards of operation and management of museums (in Italian). Photometric controls, recommended lighting, pp. 129–130. Microclimatic conditions for the prevention of microbiological attacks on organic materials. pp 148–150. Accessed February 2017
  47. 47.
    Perusini G (2004) The restoration of paintings and wooden sculptures. History, theories and techniques (in Italian). Del Bianco Editore,, ItalyGoogle Scholar
  48. 48.
    Gambetta A (2010) Fungi and insects in the wood. Diagnosis, prevention, control (in Italian). Nardini Editore, FirenzeGoogle Scholar
  49. 49.
    Fromin N, Hamelin J, Tarnawski S, Roesti D, Jourdain-Miserez K, Forestier N, Teyssier-Cuvelle S, Gillet F, Aragno M, Rossi P (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4:634–643CrossRefPubMedGoogle Scholar
  50. 50.
    Schippers A, Bosecker K, Spröer C, Schumann P (2005) Microbacterium oleivorans sp. nov. and Microbacterium hydrocarbonoxydans sp. nov., novel crude-oil-degrading Gram-positive bacteria. Int J Syst Evol Microbiol 55:655–660CrossRefGoogle Scholar
  51. 51.
    Kim YK, Lee SC, Cho YY, Oh HJ, Ko YH (2012) Isolation of cellulolytic Bacillus subtilis strains from agricultural environments. ISRN Microbiol 2012:650563CrossRefGoogle Scholar
  52. 52.
    Vimal J, Venu A, Jini J (2016) Isolation and identification of cellulose degrading bacteria and optimization of the cellulose production. Int J Res Biosciences 5(3):58–67Google Scholar
  53. 53.
    Khalid A, Kausar F, Arshad M, Mahmood T, Ahmed I (2012) Accelerated decolorization of reactive azo dyes under saline conditions by bacteria isolated from Arabian seawater sediment. Appl Microbiol Biotechnol 96:1599–1606CrossRefGoogle Scholar
  54. 54.
    Qian J, Hospodsky D, Yamamoto N, Nazaroff WW, Peccia J (2012) Size-resolved emission rates of airborne bacteria and fungi in an occupied classroom. Indoor Air 22:339–351CrossRefGoogle Scholar
  55. 55.
    Fajardo-Cavazos P, Nicholson W (2006) Bacillus endospores isolated from granite: close molecular relationships to globally distributed Bacillus spp. from endolithic and extreme environments. Appl Environ Microbiol 72:2856–2863CrossRefGoogle Scholar
  56. 56.
    Osman S, Peeters Z, La Duc MT, Mancinelli R, Ehrenfreund P, Venkateswaran K (2008) Effect of shadowing on survival of bacteria under conditions simulating the Martian atmosphere and UV radiation. Appl Environ Microbiol 74:959–970CrossRefGoogle Scholar
  57. 57.
    Rivas R, Mateos PF, Martínez-Molina E, Velázquez E (2005) Paenibacillus xylanilyticus sp. nov., an airborne xylanolytic bacterium. Int J Syst Evol Microbiol 55:405–408CrossRefGoogle Scholar
  58. 58.
    Rayner ADM, Boddy L (1988) Fungal decomposition of wood: its biology and ecology. Wiley, New YorkGoogle Scholar
  59. 59.
    Sterflinger K (2010) Fungi: their role in deterioration of cultural heritage. Fungal Biol Rev 24:47–55CrossRefGoogle Scholar
  60. 60.
    Strzelczyk AB (2004) Observations on aesthetic and structural changes induced in Polish historic objects by microorganisms. Int Biodeterior Biodegrad 53:151–156CrossRefGoogle Scholar
  61. 61.
    Sterflinger K, Pinzari F (2012) The revenge of time: fungal deterioration of cultural heritage with particular reference to books, paper and parchment. Environ Microbiol 14:559–566CrossRefGoogle Scholar
  62. 62.
    Pournou A, Bogomolova E (2009) Fungal colonization on excavated prehistoric wood: implications for in-situ display. Int Biodeterior Biodegrad 63:371–378CrossRefGoogle Scholar
  63. 63.
    Tavzes C, Pohleven J, Pohleven F, Koestler RJ (2003) Anoxic eradication of fungi in wooden objects. In: Koestler RJ, Koestler VH, Charola AE, Nieto-Fernandez FE (eds) Art, biology, and conservation: biodeterioration of works of art. The Metropolitan Museum of Art, New York, pp 426–439Google Scholar
  64. 64.
    Blanchette RA (2000) A review of microbial deterioration found in archaeological wood from different environments. Int Biodeterior Biodegrad 46:189–204CrossRefGoogle Scholar
  65. 65.
    Fazio AT, Papinutti L, Gómez BA, Parera SD, Rodríguez Romero A, Siracusano G, Maier MS (2010) Fungal deterioration of a Jesuit South American polychrome wood sculpture. Int Biodeterior Biodegrad 64:694–701CrossRefGoogle Scholar
  66. 66.
    Ortiz R, Navarrete H, Navarrete J, Párraga M, Carrasco I, de la Vega E, Ortiz M, Herrera P, Blanchette RA (2014) Deterioration, decay and identification of fungi isolated from wooden structures at the Humberstone and Santa Laura saltpeter works: a world heritage site in Chile. Int Biodeterior Biodegrad 86:309–316CrossRefGoogle Scholar
  67. 67.
    Rosado T, Silva M, Pereira C, Mirão J, Candeias A, Caldeira AT (2015) Gilded woodcarving alteration: assessment of filamentous fungi action. Int J Conserv Sci 6:499–506Google Scholar
  68. 68.
    Zyani M, Mortabit D, Mostakim M, Iraqui M, Haggoud A, Ettayebi M, Koraichi SI (2009) Cellulolytic potential of fungi in wood degradation from an old house at the Medina of Fez. Ann Microbiol 59:699–704CrossRefGoogle Scholar
  69. 69.
    Ebrahimi A, Karimi S, Lotfalian S, Majidi F (2011) Allergenic fungi in deteriorating historic objects of Shahrekord Museum, in Iran. Jundishapur J Microbiol 4:261–265Google Scholar
  70. 70.
    Bruez E, Haidar R, Alou MT, Vallance J, Bertsch C, Mazet F, Fermaud M, Deschamps A, Guerin-Dubrana L, Compant S, Rey P (2015) Bacteria in a wood fungal disease: characterization of bacterial communities in wood tissues of esca-foliar symptomatic and asymptomatic grapevines. Front Microbiol 6:1137CrossRefGoogle Scholar
  71. 71.
    Ulyshen MD (2014) Wood decomposition as influenced by invertebrates. Biol Rev Biol Proc Cambridge Philos Soc 91:70–85CrossRefGoogle Scholar
  72. 72.
    Holt DM, Jones EBG (1983) Bacterial degradation of lignified wood cell walls in anaerobic aquatic habitats. Appl Environ Microbiol 46:722–727PubMedPubMedCentralGoogle Scholar

Copyright information

© The Japan Wood Research Society 2018

Authors and Affiliations

  • Paola Cennamo
    • 1
    Email author
  • Maria Rosaria Barone Lumaga
    • 2
  • Claudia Ciniglia
    • 3
  • Ottavio Soppelsa
    • 2
  • Aldo Moretti
    • 2
  1. 1.Facoltà di LettereUniversity Suor Orsola Benincasa of NaplesNaplesItaly
  2. 2.Department of BiologyUniversity of Naples Federico IINaplesItaly
  3. 3.Department of Environmental, Biological and Pharmaceutical Science and TechnologySecond University of NaplesCasertaItaly

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