Skip to main content
SpringerLink
Log in

Molecular assessment of fungi in ‘‘black spots’’ that deface murals in the Takamatsuzuka and Kitora Tumuli in Japan: Acremonium sect. Gliomastix including Acremonium tumulicola sp. nov. and Acremonium felinum comb. nov.

  • Full Paper
  • Published:
Mycoscience

Abstract

Unidentified black spots (or stains) appeared on the plaster walls of the Takamatsuzuka and Kitora Tumuli in the village of Asuka, Nara Prefecture, Japan. Public attention was drawn to the biodeterioration of the colorful 1,300-year-old murals. A total of 46 isolates of Acremonium sect. Gliomastix were obtained from various samples (mainly black spots) of the Takamatsuzuka Tumulus (TT) (sampling period, May 2004–December 2006) and the Kitora Tumulus (KT) (June 2004–May 2007). These isolates were assignable to four known taxa and a new species in the ‘series Murorum’ sensu W. Gams as inferred from the integrated analysis of phenotypic and genotypic (i.e., ITS and 28S rDNA-D1/D2 sequences) characters: these were Acremonium masseei, A. murorum, A. felinum comb. nov. with the neotype designation, A. polychromum, and A. tumulicola sp. nov., which have been accommodated in the validated series Murorum in the section Gliomastix. The black spots on the murals of the TT and KT were caused mainly by A. masseei and A. murorum, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Arai H (1984) Microbiological studies on the conservation of mural paintings in tumuli. In: Ito N, Emoto Y, Miura S (eds) International symposium on the conservation and restoration of cultural property: conservation and restoration of mural paintings (1). Tokyo National Institute of Cultural Properties, Tokyo, pp 117–124

    Google Scholar 

  • Arai H (1987) Microbiological environments and the counterplan for the Takamatsuzuka Tumulus mural paintings (in Japanese). In: The Agency for Cultural Affairs (ed) National treasures, the Takamatsuzuka Tumulus mural paintings: conservation and repair (in Japanese). The Agency for Cultural Affairs, Tokyo, pp 186–196

  • Arai H, Kenjo T, Nakasato T, Miura S, Mori H, Emoto Y, Ito N (1991) Studies on the conservation of Shinto and Buddhist buildings in Nikko designated as national treasure and important cultural property (in Japanese). Sci Conserv 30:65–128

    Google Scholar 

  • Bastian F, Alabouvette C (2009) Lights and shadows on the conservation of a rock art cave: the case of Lascaux Cave. Int J Speleol 38:55–60

    Google Scholar 

  • Bastian F, Jurado V, Nováková A, Alabouvette C, Saiz-Jiménez C (2010) The microbiology of Lascaux Cave. Microbiology 156:644–652

    Article  CAS  PubMed  Google Scholar 

  • Berner M, Wanner G, Lubitz W (1997) A comparative study of the fungal flora present in medieval wall paintings in the chapel of the castle Herberstein and in the parish church of St. Georgen in Styria, Austria. Int Biodeterior Biodegrad 40:53–61

    Article  Google Scholar 

  • Bills GE, Foster MS (2004) Formulae for selected materials used to isolate and study fungi and fungal allies. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier, Amsterdam, pp 595–618

    Google Scholar 

  • Caneva G, Nugari MP, Salvadori O (2008) Plant biology for cultural heritage. The Getty Conservation Institute, Los Angeles

    Google Scholar 

  • Ciferri O (1999) Microbial degradation of paintings. Appl Environ Microbiol 65:879–885

    CAS  PubMed  Google Scholar 

  • Crous PW, Verkley GJM, Groenewald JZ, Samson RA (eds) (2009) Fungal biodiversity. CBS-KNAW Fungal Biodiversity Centre, Utrecht, p 62

  • Dhawan S, Garg KL, Pathak N (1993) Microbial analysis of Ajanta wall paintings and their possible control in situ. In: Toishi K, Arai H, Kenjo T, Yamano K (eds) Biodeterioration of cultural property 2. International Communications Specialists, Tokyo, pp 245–262

    Google Scholar 

  • Diakumaku E, Gorbushina AA, Krumbein WE, Panina L, Soukharjevski S (1995) Black fungi in marble and limestones: an aesthetical, chemical and physical problem for the conservation of monuments. Sci Total Environ 167:295–304

    Article  CAS  Google Scholar 

  • Dickinson CH (1968) Gliomastix Guéguen. Mycol Pap 115:1–24

    Google Scholar 

  • Domsch KH, Gams W, Anderson T-H (2007) Compendium of soil fungi, 2nd edn. IHW-Verlag, Eching

    Google Scholar 

  • Dupont J, Jacquet C, Dennetière B, Lacoste S, Bousta F, Orial G, Cruaud C, Couloux A, Roquebert M-F (2007) Invasion of the French Paleolithic painted cave of Lascaux by members of the Fusarium solani species complex. Mycologia 99:526–533

    Article  CAS  PubMed  Google Scholar 

  • Emoto Y, Emoto Y (1974) Microbiological investigation of ancient tombs with paintings: Ozuka tomb in Fukuoka and Chibusan tomb in Kumamoto (in Japanese). Sci Conserv 12:95–102

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenetics: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gams W (1971) Cephalosporium-artige Schimmelpilze (Hyphomycetes). Gustav Fischer Verlag, Stuttgart

    Google Scholar 

  • Gams W (1975) Cephalosporium-like hyphomycetes. Trans Br Mycol Soc 64:389–404

    Article  Google Scholar 

  • Gams W, van der Aa HA, van der Plaats-Niterink AJ, Samson SA, Stalpers JA (1987) CBS course of mycology, 3rd edn. Centraalbureau voor Schimmelcultures, Baarn

  • Garg KL, Jain KK, Mishra AK (1995) Role of fungi in the deterioration of wall paintings. Sci Total Environ 167:255–271

    Article  CAS  Google Scholar 

  • Glenn AE, Bacon CW, Price R, Hanlin RT (1996) Molecular phylogeny of Acremonium and its taxonomic implication. Mycologia 88:369–383

    Article  CAS  Google Scholar 

  • Guéguen F (1905) Gliomastix (Torula) chartarum n. gen. n. sp.; contribution à l’étude de la formation endogène des conidies. Bull Soc Mycol Fr 21:230–241

    Google Scholar 

  • Guglielminetti M, Morghen CG, Radaelli A, Bistoni F, Carruba G, Spera G, Caretta G (1994) Mycological and ultrastructural studies to evaluate biodeterioration of mural paintings: detection of fungi and mites in frescos of the Monastery of St. Damian in Assisi. Int Biodeterior Biodegrad 33:269–283

    Article  Google Scholar 

  • Hammill TM (1970) Paecilomyces clavisporis sp. nov., Trichoderma saturnisporum sp. nov., and other noteworthy soil fungi from Georgia. Mycologia 62:107–122

    Article  CAS  PubMed  Google Scholar 

  • Hammill TM (1981) On Gliomastix murorum and G. felina. Mycologia 73:229–237

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Hughes SJ (1958) Revisiones Hyphomycetum aliquot cum appendice de nominibus rejiciendis. Can J Bot 36:727–836

    Article  Google Scholar 

  • Hughes SJ, Dickinson CH (1968) New Zealand fungi 11. Gliomastix Guéguen. N Z J Bot 6:106–114

    Google Scholar 

  • Karbowska-Berent J (2003) Microbiodeterioration of mural paintings: a review. In: Koestler RJ, Koestler VH, Charola AE, Nietro-Fernandez FE (eds) Art, biology, and conservation: biodeterioration of works of art. The Metropolitan Museum of Art, New York, pp 267–301

    Google Scholar 

  • Kigawa R, Sano C, Ishizaki T, Miura S (2006) Concept and measures of the conservation of Takamatsuzuka Tumulus for thirty years and the present situation of biodeterioration (in Japanese). Sci Conserv 45:33–58

    Google Scholar 

  • Kigawa R, Sano C, Ishizaki T, Miura S (2007a) Circumstances of microorganisms in Takamatsuzuka Tumulus in 2006 (in Japanese). Sci Conserv 46:209–219

    Google Scholar 

  • Kigawa R, Sano C, Mabuchi H, Miura S (2007b) Investigation of issues in Kitora Tumulus during its restoration work (3) (in Japanese). Sci Conserv 46:227–233

    Google Scholar 

  • Kigawa R, Mabuchi H, Sano C, Miura S (2008) Biological issues in Kitora Tumulus during relocation work of the mural paintings (2007) (in Japanese). Sci Conserv 47:129–133

    CAS  Google Scholar 

  • Kigawa R, Sano C, Ishizaki T, Miura S, Sugiyama J (2009) Biological issues in the conservation of mural paintings of Takamatsuzuka and Kitora tumuli in Japan. In: Sano C (ed) International symposium on the conservation and restoration of cultural property: study of environmental conditions surrounding cultural properties and their protective measures. National Research Institute for Cultural Properties, Tokyo, Tokyo, pp 43–50

  • Kiyuna T, An K-D, Kigawa R, Sano C, Miura S, Sugiyama J (2008) Mycobiota of the Takamatsuzuka and Kitora tumuli in Japan, focusing on the molecular phylogenetic diversity of Fusarium and Trichoderma. Mycoscience 49:298–311

    Article  CAS  Google Scholar 

  • Korneup A, Wanscher JH (1978) Methuen handbook of colour, 3rd edn. Eyre Methuen, London

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Lechat C, Farr DF, Hirooka Y, Minnis AM, Rossman AY (2010) A new species of Hydropisphaera, H. bambusicola, is the sexual state of Gliomastix fusigera. Mycotaxon 111:95–102

    Article  Google Scholar 

  • Matsushima T (1975) Icones microfungorum a Matsushima lectorum. Published by the author, Kobe

  • Mau B, Newton M, Larget B (1999) Bayesian phylogenetic inference via Markov chain Monte Carlo methods. Biometrics 55:1–12

    Article  CAS  PubMed  Google Scholar 

  • Nieto-Fernández FE, Centeno SA, Wypyski MT, Di Bonaventura MP, Baldwin AM, Koestler RJ (2003) Enzymatic approach to removal of fungal spots from drawings on paper. In: Koestler RJ, Koestler VH, Charola AE, Nietro-Fernandez FE (eds) Art, biology, and conservation: biodeterioration of works of art. The Metropolitan Museum of Art, New York, pp 111–127

  • Nugari MP, Realini M, Roccardi A (1993) Contamination of mural paintings by indoor airborne fungal spores. Aerobiologia 9:131–139

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest 2.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and plemorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233

    Google Scholar 

  • Orial G, Mertz J-D (2006) Lascaux: une grotte vivante. Étude et suivi des phénomènes microbiologiques. Monumental 2:76–87

    Google Scholar 

  • Orial G, Bousta F, François A (2009) Lascaux cave: monitoring of microbiological activities. In: Sano C (ed) International symposium on the conservation and restoration of cultural property: study of environmental conditions surrounding cultural properties and their protective measures. National Research Institute for Cultural Properties, Tokyo, pp 31–40

  • Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311

    Article  CAS  PubMed  Google Scholar 

  • Rossman AY, McKemy JM, Pardo-Schultheiss RA, Schroers H-J (2001) Molecular studies of the Bionectriaceae using large subunit rDNA sequences. Mycologia 93:100–110

    Article  CAS  Google Scholar 

  • Saiz-Jiménez C (1995) Microbial melanins in stone monuments. Sci Total Environ 167:273–286

    Article  Google Scholar 

  • Sano C, Inuzuka M, Mabuchi H, Kigawa R, Yoshida N, Morii M, Kato M, Furihata J, Ishizaki T, Miura S (2008) Environmental conditions of Kitora Tumulus in 2007: monitoring of biological damage (in Japanese). Sci Conserv 47:135–171

    CAS  Google Scholar 

  • Seifert KA, Louis-Seize G, Sampson G (2003) Myrothecium acadiense, a new hyphomycete isolated from the weed Tussilago farfara. Mycotaxon 87:317–327

    Google Scholar 

  • Sigler L, Zuccaro A, Summerbell RC, Mitchell J, Paré JA (2004) Acremonium exuviarum sp. nov., a lizard-associated fungus with affinity to Emericellopsis. Stud Mycol 50:409–413

    Google Scholar 

  • Sugiyama J, Kiyuna T, An K-D, Koide T, Kigawa R, Sano C, Miura S (2008) Microbiological survey of the stone chambers of Takamatsuzuka and Kitora tumuli, Nara Prefecture, Japan: a milestone in elucidating the cause of biodeterioration of mural paintings. In: 31st international symposium on the conservation and restoration of cultural property, Tokyo, Japan, Feb. 5–7, pp 34–36

  • Sugiyama J, Kiyuna T, An K-D, Nagatsuka Y, Handa Y, Tazato N, Hata-Tomita J, Nishijima M, Koide T, Yaguchi Y, Kigawa R, Sano C, Miura S (2009) Microbiological survey of the stone chambers of Takamatsuzuka and Kitora tumuli, Nara Prefecture, Japan: a milestone in elucidating the cause of biodeterioration of mural paintings. In: Sano C (ed) International symposium on the conservation and restoration of cultural property: study of environmental conditions surrounding cultural properties and their protective measures. National Research Institute for Cultural Properties, Tokyo, pp 51–73

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (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, New York, pp 315–322

    Google Scholar 

  • Zare R, Gams W, Starink-Willemse M, Summerbell RC (2007) Gibellulopsis, a suitable genus for Verticillium nigrescens, and Musicillium, a new genus for V. theobromae. Nova Hedwig 85:463–489

    Article  Google Scholar 

  • Zuccaro A, Schulz B, Mitchell JI (2003) Molecular detection of ascomycetes associated with Fucus serratus. Mycol Res 107:1451–1466

    Article  CAS  PubMed  Google Scholar 

  • Zuccaro A, Summerbell RC, Gams W, Schroers H-J, Mitchell JI (2004) A new Acremonium species associated with Fucus spp., and its affinity with a phylogenetically distinct marine Emericellopsis clade. Stud Mycol 50:283–297

    Google Scholar 

Download references

Acknowledgments

Our studies and the reproduction of the portions of the photos shown in Fig. 1 were permitted by the Agency for Cultural Affairs, Japan. We sincerely thank Dr. Walter Gams, one of the reviewers, for his critical comments and helpful suggestions, without which this paper could not have been improved. The comments and suggestions of Dr. Gen Okada as the Editor also helped improving the manuscript. We are grateful to Ms. Carolyn Babcock, Curator of Canadian Collection of Fungus Cultures (CCFC/DAOM) in Ottawa; and the curators of Centraalbureau voor Schimmelcultures (CBS) in Utrecht, RIKEN-Japan Collection of Microorganisms (JCM) in Wako, and NITE-Biological Resource Center (NBRC) in Kazusa for providing the strains (including ex-type) of Acremonium and Gliomastix spp. This study was financially supported in part by a Research Grant from the Institute for Fermentation, Osaka (IFO), to K.-D. An (2008–) and in part by Grants-in-Aid for Scientific Research (A) (No. 17206060 to S.M., 2005–2007; No. 19200057 to C. Sano, 2007–) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

Author information

Author notes

  1. Kwang-Deuk An

    Present address: Microbe Division/Japan Collection of Microorganisms, RIKEN BioResource Center, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

Authors and Affiliations

  1. NCIMB Group, TechnoSuruga Laboratory Co., Ltd., 330 Nagasaki, Shimizu-ku, Shizuoka, Shizuoka, 424-0065, Japan

    Tomohiko Kiyuna & Kwang-Deuk An

  2. Independent Administrative Institution, National Research Institute for Cultural Properties, Tokyo, 13-43 Ueno Park, Taito-ku, Tokyo, 110-8713, Japan

    Rika Kigawa, Chie Sano & Sadatoshi Miura

  3. TechnoSuruga Laboratory Co., Ltd., Chiba Branch Office & Lab, 2102-10 Dainichi, Yotsukaido, Chiba, 284-0001, Japan

    Junta Sugiyama

Authors
  1. Tomohiko Kiyuna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kwang-Deuk An
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rika Kigawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chie Sano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sadatoshi Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Junta Sugiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Junta Sugiyama.

Additional information

T. Kiyuna and K.-D. An contributed equally to this work.

About this article

Cite this article

Kiyuna, T., An, KD., Kigawa, R. et al. Molecular assessment of fungi in ‘‘black spots’’ that deface murals in the Takamatsuzuka and Kitora Tumuli in Japan: Acremonium sect. Gliomastix including Acremonium tumulicola sp. nov. and Acremonium felinum comb. nov.. Mycoscience 52, 1–17 (2011). https://doi.org/10.1007/s10267-010-0063-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10267-010-0063-6

Keywords

Search

Navigation