Versão em português
N.º 32
2019
pp. 18-27

 

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Article
Fungal stains on paper: is what you see what you get?

Sílvia O. Sequeira1,2,, Hugo Paiva de Carvalho3 , Nuno Mesquita3 , António Portugal3 , Maria Filomena Macedo1,2 

1 Departamento de Conservação e Restauro, Universidade NOVA de Lisboa, 2829-516 Caparica, Portugal

2 VICARTE, Universidade NOVA de Lisboa, 2829-516 Caparica, Portugal

3 Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, 3000-456 Coimbra, Portugal

* sos11865@campus.fct.unl.pt

Abstract

Mitigation of fungal biodeterioration on paper documents and artworks represents a challenge to conservators worldwide. Numerous lists of fungal species have been identified from paper collections, but are those species responsible for the respective biodeterioration phenomena or just environmental contaminants? The present work was aimed at obtaining an association between specific fungal stains and causative fungal species. 23 stains from three paper documents were sampled. Fungal structures observed in situ with optical and scanning electron microscopy were compared with the identification of isolates by molecular biology tools. Correlation between the observed fungal structures and the identified fungal isolates was achieved, varying from 13% to 64% of the samples within the three studied documents. Grey/black and dark brown stains were associated with Chaetomium globosum, C. murorum, Penicillium chrysogenum, P. commune, Myxotrichum deflexum and Stachybotrys chartarum. Eurotium rubrum was isolated from a foxing stain and Penicillium citrinum was identified on light orange stains.

Keywords

Fungal stains
Paper conservation
Identification of fungi
SEM
DNA

Language

English

DOI

10.14568/cp2018007

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Citation

Conservar Património | APA | Chicago | NP405 | ABNT

Conservar Património:
Sequeira, S. O.; Carvalho, H. P.; Mesquita, N.; Portugal, A.; Macedo, M. F., 'Fungal stains on paper: is what you see what you get?', Conservar Património 32 (2019) 18-27, https://doi.org/10.14568/cp2018007.

APA:
Sequeira, S. O., Carvalho, H. P., Mesquita, N., Portugal, A., & Macedo, M. F. Fungal stains on paper: is what you see what you get?. Conservar Património 32:18-27. DOI:10.14568/cp2018007.

Chicago:
Sequeira, S. O., Hugo Paiva de Carvalho, Nuno Mesquita, António Portugal, and Maria Filomena Macedo. "Fungal stains on paper: is what you see what you get?." Conservar Património 32:18-27. doi:10.14568/cp2018016.

NP405:
SEQUEIRA, S. O. [et al.] – Fungal stains on paper: is what you see what you get?. Conservar Património. [Em linha]. 32 (2019) 18-27 [Consult. ]. Disponível em WWW: <URL:https://doi.org/10.14568/2018007>. ISSN 21829942.

ABNT:
SEQUEIRA, S. O. et al. Fungal stains on paper: is what you see what you get?. Conservar Património, Lisboa, v. 32, p. 18-27, 2019. Disponível em: <https://doi.org/10.14568/cp2018007>. Acesso em: .

History

Received: 2018-3-7
Revised: 2018-9-21
Accepted: 2018-10-12
Online: 2018-11-16

References

1 Sequeira, S. O.; Cabrita, E. J.; Macedo, M. F., 'Fungal biodeterioration of paper: how are paper and book conservators dealing with it? An International Survey', Restaurator 35(2) (2014) 181-199, https://doi.org/10.1515/res-2014-0005.

2 Florian, M., Fungal Facts - Solving Fungal Problems in Heritage Collections, Archetype Publications, London (2002).

3 Rakotonirainy, M. S.; Heude, E.; Lavédrine, B., 'Isolation and attempts of biomolecular characterization of fungal strains associated to foxing on a 19th century book', Journal of Cultural Heritage 8(2) (2007) 126-133, https://doi.org/10.1016/j.culher.2007.01.003.

4 Allsopp, D.; Seal, K.; Gaylarde, C., Introduction to Biodeterioration, 2nd ed., Cambridge University Press, Cambridge (2004), https://doi.org/10.1017/CBO9780511617065.

5 Szczepanowska, H.; Lovett, C. M.; 'A study of the removal and prevention of fungal stains on paper', Journal of the American Institute for Conservation 31(2) (1992), 147-160, https://doi.org/10.2307/3179489.

6 Karakasidou, K.; Nikolouli, K.; Amoutzias, G. D.; Pournou, A.; Manassis, C.; Tsiamis, G.; Mossialos, D., 'Microbial diversity in biodeteriorated Greek historical documents dating back to the 19th and 20th century: a case study', MicrobiologyOpen (2018), https://doi.org/10.1002/mbo3.596.

7 El Bergadi, F.; Laachari, F.; Elabed, S.; Mohammed, I. H.; Ibnsouda, S. K., 'Cellulolytic potential and filter paper activity of fungi isolated from ancients manuscripts from the Medina of Fez', Annals of Microbiology 64(2) (2014) 815-822, https://doi.org/10.1007/s13213-013-0718-6.

8 Borrego, S.; Lavin, P.; Perdomo, I.; Gómez de Saravia, S.; Guiamet, P., 'Determination of indoor air quality in archives and biodeterioration of the documentary Heritage', ISRN Microbiology 2012 (2012), 680598, https://doi.org/10.5402/2012/680598.

9 Coronado-Ruiz, C.; Avendaño, R.; Escudero-Leyva, E.; Conejo-Barboza, G.; Chaverri, P.; Chavarría, M., 'Two new cellulolytic fungal species isolated from a 19th-century art collection', Scientific Reports 8(1) (2018) 1-9, https://doi.org/10.1038/s41598-018-24934-7.

10 Polo, A.; Cappitelli, F.; Villa, F.; Pinzari, F., 'Biological invasion in the indoor environment: the spread of Eurotium halophilicum on library materials', International Biodeterioration & Biodegradation 118 (2017) 34-44, https://doi.org/10.1016/j.ibiod.2016.12.010.

11 Kraková, L.; Soltys, K.; Otlewska, A.; Pietrzak, K.; Purkrtová, S.; Savická, D.; Puskárová, A.; Buková, M.; Szemes, T.; Budis, J.; Demnerová, K.; Gutarowska, B.; Pangallo, D., 'Comparison of methods for identification of microbial communities in book collections: culture-dependent (sequencing and MALDI-TOF MS) and culture-independent (Illumina MiSeq)', International Biodeterioration & Biodegradation 131 (2018) 51-59, https://doi.org/10.1016/j.ibiod.2017.02.015.

12 Sanmartín, P.; DeAraujo, A.; Vasanthakumar, A., 'Melding the old with the new: trends in methods used to identify, monitor, and control microorganisms on Cultural Heritage materials', Microbial Ecology 76(1) (2018) 64-80, https://doi.org/10.1007/s00248-016-0770-4.

13 Michaelsen, A.; Piñar, G.; Montanari, M.; Pinzari, F., 'Biodeterioration and restoration of a 16th-century book using a combination of conventional and molecular techniques: a case study', International Biodeterioration & Biodegradation 63(2) (2009) 161-168, https://doi.org/10.1016/j.ibiod.2008.08.007.

14 Michaelsen, A.; Piñar, G.; Pinzari, F., 'Molecular and microscopical investigation of the microflora inhabiting a deteriorated Italian manuscript dated from the thirteenth century', Microbial Ecology 60(1) (2010) 69-80, https://doi.org/10.1007/s00248-010-9667-9.

15 Piñar, G.; Sterflinger, K.; Pinzari, F., 'Unmasking the measles-like parchment discoloration: molecular and microanalytical approach', Environmental Microbiology 17(2) (2015) 427-443, https://doi.org/10.1111/1462-2920.12471.

16 Piñar, G.; Tafer, H.; Sterflinger, K.; Pinzari, F., 'Amid the possible causes of a very famous foxing: Molecular and microscopic insight into Leonardo da Vinci's self-portrait', Environmental Microbiology Reports 7(6) (2015) 849-859, https://doi.org/10.1111/1758-2229.12313.

17 Schabereiter-Gurtner, C.; Piñar, G.; Lubitz, W.; Rölleke, S., 'Analysis of fungal communities on historical church window glass by denaturing gradient gel electrophoresis and phylogenetic 18S rDNA sequence analysis', Journal of Microbiological Methods 47(3) (2001) 345-354, https://doi.org/10.1016/S0167-7012(01)00344-X.

18 Lupan, I.; Popescu, O. 'Metagenomics and future perspectives for biodeterioration and biodegradation studies', Annals of the Romanian Society for Cell Biology 17(2) (2012) 37-42.

19 Rosado, T.; Mirão, J.; Candeias, A.; Caldeira, A. T., 'Microbial communities analysis assessed by pyrosequencing - A new approach applied to conservation state studies of mural paintings', Analytical and Bioanalytical Chemistry 406(3) (2014) 887- 895, https://doi.org/10.1007/s00216-013-7516-7.

20 Li, Q.; Zhang, B.; He, Z.; Yang, X., 'Distribution and diversity of bacteria and fungi colonization in stone monuments analyzed by high-throughput sequencing', PLoS One 11(9) (2016) 1-17, https://doi.org/10.1371/journal.pone.0163287.

21 Chimienti, G.; Piredda, R.; Pepe, G.; van der Werf, I. D.; Sabbatini, L.; Crecchio, C.; Ricciuti, P.; D'Erchia, A.; Manzari, M. C.; Pesole G., 'Profile of microbial communities on carbonate stones of the medieval church of San Leonardo di Siponto (Italy) by Illumina-based deep sequencing', Applied Microbiology and Biotechnology 100(19) (2016) 8537-8548, https://doi.org/10.1007/s00253-016-7656-8.

22 Szulc, J.; Otlewska, A.; Ruman, T.; Kubiak, K.; Karbowska-Berent, J.; Kozielec, T.; Gutarowska, B., 'Analysis of paper foxing by newly available omics techniques', International Biodeterioration & Biodegradation 132 (2018) 157-165, https://doi.org/10.1016/j.ibiod.2018.03.005.

23 Micheluz, A.; Manente, S.; Tigini, V.; Prigione, V.; Pinzari, F.; Ravagnan, G.; Varese, G.C., 'The extreme environment of a library: xerophilic fungi inhabiting indoor niches', International Biodeterioration & Biodegradation 99 (2015) 1-7. https://doi.org/10.1016/j.ibiod.2014.12.012.

24 Pinzari, F.; Montanari, M.; Michaelsen, A.; Piñar, G., 'Analytical protocols for the assessment of biological damage in historical documents', Coalition 19 (2010) 6-13.

25 Watanabe, T., Pictorial Atlas of Soil and Seed Fungi: Morphologies of Cultured Fungi and Key to Species, 2nd ed., CRC Press, Boca Raton (2002), https://doi.org/10.1201/9781420040821.

26 Seifert, K.; Morgan-Jones, G.; Gams, W.; Kendrick, B., The Genera of Hyphomycetes, CBS-KNAW Fungal Biodiversity Centre, Utrecht (2011).

27 Samson, R. A.; Hoekstra, E. S.; Frisvad, J. C.; O. Filtenborg (eds.), Introduction to Food and Airborne Fungi, 6th ed., Centraalbureau Voor Schimmelculture, Utrecht (2000).

28 Pitt, J. I.; Hocking, A. D., Fungi and Food Spoilage, 3rd ed., Springer, New York (2009), https://doi.org/10.1007/978-0-387-92207-2.

29 Mesquita, N.; Portugal, A.; Videira S.; Rodriguez-Echeverria, S.; Bandeira, A. M. L.; Santos, M. J. A.; Freitas, H., 'Fungal diversity in ancient documents. A case study on the Archive of the University of Coimbra', International Biodeterioration & Biodegradation 63 (2009) 626-629, https://doi.org/10.1016/j.ibiod.2009.03.010.

30 Sharma, D.; Shukla, A. K.; 'Starch hydrolysis and alpha-amylase activity of Aspergillus and Chaetomium', Asian Journal of Biochemistry 3(5) (2008) 284-289, https://doi.org/10.3923/ajb.2008.284.289.

31 Abdel-Azeem, A. M.; Gherbawy, Y. A.; Sabry, A. M., 'Enzyme profiles and genotyping of Chaetomium globosum isolates from various substrates', Plant Biosystems 150(3) (2016) 420-428, https://doi.org/10.1080/11263504.2014.984791.

32 Houbraken, J.; Frisvad, J. C.; Samson, R. A., 'Taxonomy of Penicillium section Citrina', Studies in Mycology 70 (2011) 53-138, https://doi.org/10.3114/sim.2011.70.02.

33 da Silva, M.; Moraes, A. M. L.; Nishikawa, M. M.; Gatti, M. J. A.; de Alencar, M. A. V.; Brandao, L. E.; Nobrega, A., 'Inactivation of fungi from deteriorated paper materials by radiation', International Biodeterioration & Biodegradation 57(3) (2006) 163-167, https://doi.org/10.1016/j.ibiod.2006.02.003.

34 Corte, A. M.; Ferroni, A.; Salvo, V. S., 'Isolation of fungal species from test samples and maps damaged by foxing, and correlation between these species and the environment', International Biodeterioration & Biodegradation 51 (2003) 167-173, https://doi.org/10.1016/S0964-8305(02)00137-3.

35 Oetari, A.; Susetyo-Salim, T.; Sjamsuridzal, W.; Suherman, E. A.; Monica, M.; Wongso, R.; Fitri, R.; Nurlaili, D. G.; Ayu, D. C.; Teja, T. P., 'Occurrence of fungi on deteriorated old dluwang manuscripts from Indonesia', International Biodeterioration & Biodegradation 114 (2016) 94-103, https://doi.org/10.1016/j.ibiod.2016.05.025.

36 Gopinath, S. C. B.; Anbu, P.; Hilda, A. 'Extracellular enzymatic activity profiles in fungi isolated from oil-rich environments', Mycoscience 46(2) 119-126, https://doi.org/10.1007/S10267-004-0221-9.

37 Florian, M. L. E.; Manning, L., 'SEM analysis of irregular fungal fox spots in an 1854 book: population dynamics and species identification', International Biodeterioration & Biodegradation 46 (2000) 205-220, https://doi.org/10.1016/S0964-8305(00)00062-7.

38 Karbowska-Berent, J.; Jarmiko, J.; Czuczko, J., 'Fungi in fox spots of a drawing by Leon Wyczókowski', Restaurator 35(2) (2014) 159-179, https://doi.org/10.1515/res-2014-1000.

39 Das, M. K. L.; Prasad, J. S.; Ahmad, S. K., 'Endoglucanase production by paper-degrading mycoflora', Letters in Applied Microbiology 25(5) (1997) 313-315, https://doi.org/10.1046/j.1472-765X.1997.00217.x.

40 Ricelli, A.; Fabbri, A.A.; Fanelli,C.; Menicagli, R.; Samaritani, S.; Pini, D.; Rapaccini, S.M.; Salvadori, P., 'Fungal growth on samples of paper: Inhibition by new antifungals', Restaurator 20(2) (1999) 97-107, https://doi.org/10.1515/rest.1999.20.2.97.

41 De La Rosa, J.M.; Martin-Sanchez, P.M.; Sanchez-Cortes, S.; Hermosin, B.; Knicker, H.; Saiz-Jimenez, C., 'Structure of melanins from the fungi Ochroconis lascauxensis and Ochroconis anomala contaminating rock art in the Lascaux Cave', Scientific Reports 7 (2017) 13441, https://doi.org/10.1038/s41598-017-13862-7.

42 Foladi, S.; Hedayati, M.T.; Shokohi, T.; Mayahi, S., 'Study on fungi in archives of offices, with a particular focus on Stachybotrys chartarum', Journal de Mycologie Medicale 23(4) (2013) 242-246, https://doi.org/10.1016/j.mycmed.2013.09.003.

43 Wang, X. W.; Houbraken, J.; Groenewald, J. Z.; Meijer, M.; Andersen, B.; Nielsen, K. F.; Crous, P. W.; Samson, R. A., 'Diversity and taxonomy of Chaetomium and chaetomium-like fungi from indoor environments', Studies in Mycology 84 (2016) 145-224, https://doi.org/10.1016/j.simyco.2016.11.005.

44 Zyska, B., 'Fungi isolated from library materials: A review of the literature', International Biodeterioration & Biodegradation 40(1) (1997) 43-51, https://doi.org/10.1016/S0964-8305(97)00061-9.

45 Pietrzak, K.; Otlewska, A.; Dybka, K.; Danielewicz, D.; Pangallo, D.; Demnerová, K.; Durovic, M.; Kraková; Scholtz, L. V.; Bucková, M.; Puskarová, A.; Kucerová, I.; Skrdlantová, M.; Drabková, K.; Surma-Slusarska, B.; Gutarowska, B., 'A modern approach to biodeterioration assessment and disinfection of historical book', in A Modern Approach to Biodeterioration Assessment and the Disinfection of Historical Book Collections, ed. G. Beata, Institute of Fermentation Technology and Microbiology - Lodz University of Technology, Lódz (2016) 81-123.

46 Campbell, C. K.; Johnson, E. M.; Warnock, D. W., Identification of Pathogenic Fungi, 2nd ed., Wiley-Blackwell, Chichester (2013), https://doi.org/10.1002/9781118520055.

47 Y Sato, Y.; Aoki, M.; Kigawa, R., 'Microbial deterioration of tsunami-affected paper-based objects: A case study', International Biodeterioration & Biodegradation 88 (2014) 142-149, https://doi.org/10.1016/j.ibiod.2013.12.007.

Stable url: https://doi.org/10.14568/cp2018007

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