The Effect of Temperature, Water Activity, pH and Time on the Growth of Aspergillus niger, Alternaria alternate and Penicillium sp. in the historical papers

Authors

1 PhD Student, Preservation of Cultural and Historical Artefacts, Isfahan University of Fine Arts, Isfahan, I. R. Iran.

2 Assistant Professor, Historical and Cultural Objects Restoration, Arts University of Isfahan, Isfahan, I.R.Iran

3 Associate Professor, The School of Architecture and Environmental Design, Iran University of Science and Technology, Tehran, I. R. Iran.

Abstract

Purpose: To examine material the effect of microorganisms responsible for the biodegradation process of old paper.
Method and Research Design: The effect of temperature (5–40 °C), water activity (aw; 0•80-0.99) on Munktel paper 393 (100% cellose) with pH values of 3 to 9 in 168 hour and their interactions with the temporal rates of germination and mycelial growth of three mycotoxigenic strains of Aspergillus niger(PTCC 5251), Alternaria alternate (PTCC: 5224) and Penicillium sp. (PTCC: 5224) in vitro was measured on historical papers. The aw of the media was controlled with glycerol. 
Findings and Conclusion: The most important factor influencing the growth of the above mentioned fungi is water activity, then temperature and finally pH. Therefore, the most effective way to prevent biodegradation of papers of art works is to reduce water activity in them. Reducing water activity along with temperature control and deacidification minimizes the process of biodegradation.
 C, aw: 0.98 and, pH: 6.5 for Alternaria alternate.° C, aw: 0.97 and, pH: 6.5 for Aspergillus niger and T:25°C, aw: 0.99, pH:6 for Penicillium sp., T:30°The optimum growth occurred at T: 25

Keywords

Main Subjects


Resource English translation
 
Abdel‑Hadi, Ahmed; Naresh,Magan. (2009). “Influence of physiological factors on growth, sporulation and ochratoxin A/B production of new Aspergillus ochraceus grouping”. World Mycotoxin Journal, 2(4): pp 429-434.
Abdel‑Kareem, Omar. (2010). “Monitoring, controlling and prevention of the fungal deterioration of textile artifacts in the museum of Jordanian heritage”. Mediterranean Archaeology and Archaeometry, 10(2), PP 85-96.
Abe, K. (2010). “Assessment of the environmental conditions in a museum storehouse by use of a fungal index”. International Biodeterioration & Biodegradation, 64, pp 32–40.
Araujo, Ricardo; Rodrigues, Acacio G; Pina-Vaz, Cidalia. (2004). “A fast, practical and reproducible procedure for thestandardization of the cell density of an Aspergillus suspension”. Journal of Medical Microbiology, 53, pp 783-786.
Atanda, S. A.; Pessu, P. O.; Agoda, S.; Isong, I. U.; Adekalu, O. A.; Echendu, M. A.; Falade, T. C. (2011). “Fungi and mycotoxins in stored foods”. African Journal of Microbiology Research, 5(25), pp 4373-4382.
Ayerst, G. (1969). “The effects of moisture and temperature on growth and spore germination in some fungi”. Journal of Stored Products Research, 5(2), pp 127-141.
Berovic, M. (2003). “Biodeterioration studies on pastels and oil-based paintings”. In: Art, Biology, and Conservation: Biodeterioration of Works of Art. Koestler, Robert. J.; Koestler, Victoria. H.; Charola, A. Elena.; Nieto-Fernandez, Fernando. E. (Eds.). Metropolitan Museum of Art, New York, USA, pp 50–59.
Borrego, S.; Guiamet, P.; Gómez de Saravia, S.; Batistini, P.; Garcia, M.; Lavin, P.; Perdomo, I. (2010). “The quality of air at archives and the biodeterioration of photographs”. International Biodeterioration & Biodegradation, 64(2), pp 139-145. https://www.researchgate.net/publication/248436861_The_quality_of_air_at_archives_and_the_biodeterioration_of_photographs.
CLSI. (2002). “Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi”; Approved Standard. CLSI document M38-A [ISBN 1-56238-470-8]. CLSI, Pennsylvania, USA 2002.
Dagnas, S.; Onno, B.; Membré, J. M. (2014). “Modeling growth of three bakery product spoilage molds as a function of water activity, temperature and pH”. International Journal of Food Microbiology, 1(186), pp 95-104.
Dallyn, H. (1978). “Effect of substrate water activity on growth of certain xerophilic fungi”. Ph.D. thesis. South Bank University, London.
Dantigny, Philippe; Bensoussan, Maurice; Vasseur, Valerie; Lebrihi, Ahmed; Buchet, Claude; Ismaili-Alaoui, Mustapha; Devlieghere, Frank; Roussos, Sevastianos. (2006). “Standardisation of methods for assessing mould germination: a workshop report”. International Journal of Food Microbiology, 108(2), pp 286‑291.
EC, European Commission. (1994). Mycotoxins in human nutrition and health. Agroindustrial research division of the European Commission Directorate-General XII for scientific research and development, 36.
Feller, R. L. (1994). “Accelerated aging: Photochemical and thermal aspects”. Getty Conservation Institute.
Florian, M. L. (1997). Heritage Eaters: Insects and Fungi in Heritage Collections. James and James (Scientific Publishers) Ltd, London.
Florian, Mary-Lou. E. (2004). Fungal Facts: Solving Fungal Problems in Heritage Collections. Archetype Publications, Great Britain. pp 90-97.
Ghahri, Mohammad. (1391/2012). Avāmel-e mikrobi-ye āsib-resān be mavād-e āršivi va ketābxāne-’i (Damaging germ-carrying elements in archives and library). Tehran: Sāzmān-e Asnād va Ketābxāne-ye Melli-ye Irān.
Ghahri, Mohammad. (1385/2007). “ Moruri bar avāmel-e qārči-ye moxareb-e kāqaz, āsib-šenāsi va rāh-hā-ye pišgiri va moqābele (A review of fungal elements decaying paper, its pathology and prevention)”. Maremat & pežuheš (Maremat & pezhouhesh). autumn and winter (1), pp. 27-42.
Gock, Melissa. A.; Hocking, Ailsa. D.; Pitt, John. I.; Poulos, Peter. G. (2003). “Influence of temperature, water activity and pH on growth of some xerophilic fungi”. International Journal of Food Microbiology, 81(1), pp 11-19.
Goldfarb, Barry; Nelson, Earl. E; Hansen, Everett. M. (1989). “Trichoderma spp.: growth rates and antagonism to Phellinus weirii in vitro”. Mycologia, 81(3), pp 375–381.
Gorski, Theodore. W; Ritzert, Roger. W. (1977). “pH Measurements of Agar Culture Media by Using a Flat-Bottom Electrode”.  Applied and Environmental Microbiology, 34(2), pp 242–243.
Gutarowska, Beata; Rembisz, Daria; Pietrzak, Katarzyna; Skóra, Justyna; Szynkowska, Malgorzata; Gliścińska, Eulalia; Koziróg, Anna. (2012). “Optimization and application of the misting method with silver nanoparticles for disinfection of the historical objects”. International Biodeterioration & Biodegradation, 75, pp 167-175.
Haines, John. H.; Kohler, Stuart. A. (1986). “An Evaluation of Ortho-Phenyl Phenol as a Fungicidal Fumigant for Archives and Libraries”. Journal of the American Institute for Conservation, 25(1), pp 49-55.
Hidalgo, Yahumila; Borrego, Sofía. (2006). “Aislamiento y caracterización de hongos en documentos de la Biblioteca Nacional “José Martí”. Bibliotecas, online at: http://revistas.bnjm.cu/index.php/anales/article/view/194.Accessed: 11/08/2013.
Hocking, Ailsa. D.; Pitt, John. I. (1979). “Water relations of some penicillium species at 25 degrees Celsius”. Transactions of the British Mycological Society, 73(1), pp 141-145.

ISO 6588-1. (2005). “Paper, board and pulps -- Determination of pH of aqueous extracts -- Part 1: Cold extraction”. https://www.iso.org/standard/41368.html

ISO 18787. (2017). “Foodstuffs - Determination of water activity”. https://www.iso.org/standard/63379.html
Konkol, Nick; J McNamara, Christopher; Mitchell, Ralph. (2010). “Fluorometric detection and estimation of fungal biomass on cultural heritage materials”. Journal of Microbiological Methods, 80(2), pp 178‑182.
Kowalik, Romuald. (1980). “Microbiodeterioration of library materials”. Part 1, chapters 1-3. Restaurator, 4, pp 99-114.
Ljaljević Grbić, Milica;Vukojević, Jelena;Stupar,Miloš. (2008). “Fungal colonization of air-conditioning systems”. Archives of Biological Sciences, 60(2), PP 201-206.
Magan, N.; Lacey, J. (1984). “Effect of water activity, temperature and substrate on interactions between field and storage fungi”. Transactions of the British Mycological Society(Trans Br Mycol Soc), 82(1), PP 83-93.
Marı´n, Sonia; Sanchis, V.; Teixido´, A.; Saenz, R.; Ramos, Antonio J; Vin˜as, Immaculada; Magan, Naresh. (1996). “Water and temperature relations and microconidial germination of Fusarium moniliforme and Fusarium proliferatum from maize”. Canadian Journal of Microbiology, 42(10), PP 1045–1050.
Martens, M. H. J. (2012). Climate risk assessment in museums: degradation risks determined from temperature and relative humidity data. Eindhoven: Technische Universiteit Eindhoven. 51-53.
Mesquita, Nuno; Portugal, António; Rodrigues Videira, Sandra Isabel; Rodríguez-Echeverría, Susana; Bandeira, A.M.L; Santos, M.J.A; Freitas, Helena. (2009). “Fungal diversity in ancient documents: a case study on the Archive of the University of Coimbra”. International Biodeterioration and Biodegradation, 63(5), pp 626-629.
Michaelsen, Astrid; Pinzari, Flavia; Barbabietola, Nicoletta; Piñar, Guadalupe. (2013). “Monitoring the effects of different conservation treatments on paper-infecting fungi”. International Biodeterioration & Biodegradation, 84, pp 333-341.
Mo’assese-ye ’Estāndārd va Tahqiqāt-e San’ati-ye Irān (Iran National Standards Organiztion). (1374/1995). Standard no. ISIRI: 133: “Raveš-e nemune-bardāri az kāqaz va moqavā barāye āzmun (The method of biopsy of paper and cardboard for test)”, 1st revision. 2nd impression.
Mo’assese-ye ’Estāndārd va Tahqiqāt-e San’ati-ye Irān (Iran National Standards Organiztion). (1378/1999). Standard no. ISIRI: 4706: “Raveš-e tasri’ dar kohne šodan-e kāqaz va moqāva dar damā-ye 80 daraje-ye selsiyus va rotubat-e 65 dar-sad (The method of expediting in the process of  paper and cardboard getting old in 80 Celsius and 65% humidity)”.
Mo’assese-ye ’Estāndārd va Tahqiqāt-e San’ati-ye Irān (Iran National Standards Organiztion). (1382/2004). Standard no. ISIRI: 106-A1: “Šarāyet-e mohiti-ye ’estāndārd-e mašrut kardan, marāhel-e nezārat bar šarāyet-e mohiti va mašrut kardan va āzmun-e nemune-hā-ye āzmuni-ye xamir-e kāqaz,kāqaz va moqavā (Environmental condition of conditioning standard, steps of control over environmental condition, conditioning and test the tesable samples of paper dough, paper and cardboard)”. 1st impression.
Mo’assese-ye ’Estāndārd va Tahqiqāt-e San’ati-ye Irān (Iran National Standards Organiztion). (1386/2008). Standard no. ISIRI 9597: “Mikrobioloži-ye raveš-hā-ye setarvan-sāzi-ye mohit-e kešt va vasāyel-e āzmāyešgāhi-āy’in- kār (The microbiology of the methods of the sterilization of cultivating environment and lab instuments-codes of conduct)”.
National Committee for Clinical Laboratory Standards (NCCLS). (1998). “Reference method for broth dilution antifungal susceptibility testing of conidium-forming filamentous fungi: proposed standard”. M38-P, v. 18, no. 13 (Nov. 1998), Wayne, Pa.
Nguyen Van Long, Nicolas; Rigalma, Karim; Coroller, Louis; Dadure, Robin; Debaets, Stella; Mounier, Jerome; Vasseur, Valérie. (2017). “Modelling the effect of water activity reduction by sodium chloride or glycerol on conidial germination and radial growth of filamentous fungi encountered in dairy foods”. International journal of food microbiology, 68, pp 7-15.
Nielsen, Kristian; Holm, G; P. Uttrup, L; Nielsen, P. A. (2004). “Mould growth on building materials under low water activities. Influence of humidity and temperature on fungal growth and secondary metabolism”. International Biodeterioration & Biodegradation, 54(4), pp 325-336.
Nitterus, M. (2000).“Fungi in archives and libraries”.Restaurator, 21(1), pp 25-40
Ontario Association of Architects. (2003). OAA Mould Control Practice Guide. Ontario.
Parker, Thomas. A. (1988). “Study on integrated pest management for libraries and archives”. volume PGI-88/WS/20. United Nations Educational, Scientific and Cultural Organization (UNESCO), Paris.
Pasanen, Pertti; Kasanen, Jukka-Pekka; Rautiala, Sirpa; Ikäheimo, Marko; Rantamäki, Jouko; Kääriäinen, Hannu; Kalliokoski, Pentti. (2000). “Fungal growth and survival in building materials under fluctuating moisture and temperature conditions”. International Biodeterioration & Biodegradation, 46(2), pp 117-127.
Paule-Marina Nanguy, Sidjè; Perrier-Cornet, Jean-Marie; Bensoussan, Maurice; Dantigny, Philippe. (2010). “Impact of water activity of diverse media on spore germination of Aspergillus and Penicillium species”. International journal of food microbiology, 142(1‑2), pp 273-276.
Petrikkou, Eva; Rodriguez-Tudela, Juan; Cuenca-Estrella, Manuel; Gómez, Alicia; Molleja, Ana; Mellado, Emilia. (2001). “Inoculum Standardization for Antifungal Susceptibility Testing of Filamentous Fungi Pathogenic for Humans”. Journal of Clinical Microbiology, 39(4), pp 1345-1347.
Omidi Tabrizi, Nasim. (1383/2005). “Arzyābi-ye asarāt-e zed-qārči-ye barg-e okāliptus bar ruye čand gyne-ye šāye’-e dermātofit va moqāyese-ye ān bā grizeofulin dar šarāyet-e in vitro (Assessment of the antifungal affects of eucalyptus leaf on some common dermatophytes and comparing that with griseofulvin in vitro condition)”. Master dissertation of medical fungology, Iran University of Medical Sciences, document no. 12703.
Pinzari, Flavia; Pasquariello, Giovanna; De Mico, Antonella. (2006). “Biodeterioration of paper: a SEM study of fungal spoilage reproduced under controlled conditions”. Macromolecular Symposia. 238(1), pp 57–66.
Pitt, John. I.; Hocking, Ailsa. D. (1977). “Influence of solute and hydrogen ion concentration on the water relations of some xerophilic fungi”. Journal of General Microbiology, 101, pp 35–40.
Plaza, Pilar; Usall, Josep; Teixidó, Neus; Vinas, Immaculada. (2003). “Effect of water activity and temperature on germination and growth of Penicillium digitatum, P. italicum and Geotrichum candidum”. Journal of Applied Microbiology, 94(4), pp 549-554.
Rakotonirainy, Malalanirina; Juchauld, Frederique; Gillet, Martine; Othman-Choulak, Monzer; Lavédrine, Bertrand. (2007). “The Effect of Linalool Vapour on Silver-Gelatine Photographs and Bookbinding Leathers”. Restaurator, 28(2), pp 95-111.
Raquel Neves, Eva; Schäfer, Stephan; Phillips, Alan; Canejo, João; Macedo, Maria. (2009). “Antifungal effect of different methyl and propyl paraben mixtures on the treatment of paper biodeterioration”. International Biodeterioration & Biodegradation, 63(3), pp 267-272.
Reis-Menezes, A. A.; Gambale, W.; Giudice, M. C.; Shirakawa, M. A. (2011). “Accelerated testing of mold growth on traditional and recycled book paper”. International Biodeterioration & Biodegradation, 65, pp 423-428.
Schleibinger, Hans; Laussmann, D; Bornehag, C-G; Eis, D; Rueden, H. (2008). “Microbial volatile organic compounds in the air of mold and mold-free indoor environments”. Indoor Air, 18(2), pp 113-124.
Shamsian, A.; Fatah, Abdolmajid; Mohajeri, Masood; Ghazvini, Kiarash. (2006). “Fungal contaminations in historical manuscripts at Astan Quds Museum Library, Mashhad, Iran”. International Journal of Agriculture & Biology, 8(3), pp 420-422.
Sidhu, G. S. (2002). “Mycotoxin Genetics and Gene Clusters”. European journal of Plant Pathology, 108(7), PP 705-711.
Strzelczyk, Alicja. B. (2004). “Observations on aesthetic and structural changes induced in Polish historic objects by microorganisms”. International Biodeterioration and Biodegradation, 53(3), PP 151-156.
Viitanen, H. A.; Bjurman, J. (1995). “Mould growth on wood under fluctuating humidity conditions”. Material und Organismen, 29(1), PP 27-46.
Zajic, J. E.; Inculet, I. I.; Martin, P. (1982). “Basic concepts in microbial aerosols”. In: Space and terrestrial biotechnology. vol 22, Fiechter A, (editor). Berlin: Akademie-Verlag. PP 51-91.
Zotti, Mirca; Ferroni, Alice; Calvini, P. (2008). “Microfungal biodeterioration of historic paper: preliminary FTIR and microbiological analysis”. International Biodeterioration & Biodegradation, 62(2), PP 186-194.
Zotti, Mirca; Ferroni, Alice; Calvini, P., (2011). “Mycological and FTIR analysis of biotic foxing on paper substrates”. International Biodeterioration and Biodegradation, 65(4), PP 569-578. (in Polish). In: Zyska, B., Zakowska, Z. (Eds.), Microbiology of Materials. Polytechnic of Lodz, Lodz.