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Occurrence of indoor wood decay basidiomycetes in Europe
f u n g a l b i o l o g y r e v i e w s x x x ( 2 0 1 7 ) 1 e6
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Review
Occurrence of indoor wood decay basidiomycetes in Europe Jirı GABRIEL*, Karel SVEC ska 1083, 142 20 Prague 4, Krc, Laboratory of Environmental Microbiology, Institute of Microbiology AS CR, Vıden Czech Republic
article info
abstract
Article history:
Brown-rot fungi are considered to be the most important wood-inhabiting fungi econom-
Received 1 March 2017
ically, as they also deteriorate the wood that has been used in buildings. In the northern
Received in revised form
hemisphere, coniferous wood is the main source of interior structural timber. White-rot
9 May 2017
fungi, which degrade lignin and preferentially attack hardwood, are less common.
Accepted 9 May 2017
Emphasis is usually placed on Serpula lacrymans or Coniophora puteana, which are the most common indoor basidiomycetes found in buildings in Europe. In this review, we sum-
Keywords:
marize available data on the occurrence of wood decay fungi in the Czech Republic, Poland,
Basidiomycetes
Germany (both former East and West), Belgium, France, Norway, Denmark, Finland, Latvia,
Fungi
Estonia, Romania and Albania reported in the past few decades. The total number of occur-
Indoor
rences was near 20,000; original data were collected between 1946 and 2008. The most
Serpula lacrymans
abundant basidiomycetes were S. lacrymans and C. puteana, with the exception of Norway, where the genus Antrodia was the most frequent. ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved.
1.
Introduction
Indoor wood decay fungi cause many problems worldwide; fungi that invade roofs, walls, ceilings, etc., represent a group of various basidiomycetes that are in many cases resistant to currently used fungicides. These fungi attack and damage wooden houses and other wooden constructions, and the most well-known of these, Serpula lacrymans (often regarded as the “cancer of buildings”), is responsible for many millions of USD of damage each year (Palfreyman, 1995). For example, the cost of fungal damage in France was estimated to be approximately V 30 million yearly (Maurice et al. 2011), and in the UK, the cost of repairing fungal damage to timber used in construction amounted to £ 3 million per week
(Rayner and Boddy 1988). The dry rot remediation business in the UK was estimated to be worth an excess of £ 400 million (Krzyzanowski et al. 1999). The decay of wood and wood-based products usually begins when the spores or mycelial fragments adhere to the wood surface. Wood moisture and temperature are the most important features in terms of the “building habitat”. Humphrey and Siggers (1933) previously studied the effect of temperature on the growth rate of 56 wood-decay fungi and found that none would grow below 12 C and that most would not grow above 40 C. According to many authors and guidelines for the protection of wood and wood products from attack by decay fungi, it is important and necessary to keep wood or wooden constructions at a moisture content below
* Corresponding author. http://dx.doi.org/10.1016/j.fbr.2017.05.002 1749-4613/ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Gabriel, J., Svec, K., Occurrence of indoor wood decay basidiomycetes in Europe, Fungal Biology Reviews (2017), http://dx.doi.org/10.1016/j.fbr.2017.05.002
J. Gabriel, K. Svec
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20 % (Carll and Highley 1999). Schmidt (2007) reported minimum and maximum humidity requirements for fungi identified by means of ITS sequencing (to avoid unreliable data for incorrectly identified species; Table 1). As stated by Carll and Highley (1999), the spores of wood decay fungi do not germinate and fungal hyphae do not grow at moisture levels much below the fibre saturation point, which is at approximately 30 % moisture. However, only the part of water that is not bound by dissolved substances (salts, sugars) is available to fungi; a detailed description of the optimum conditions for wood decay in terms of water activity (aw), water potential or relative air humidity (RH) can be found, e.g., in the abovementioned review of Schmidt (2007). However, data on fungal development under fluctuating moisture conditions that are more common in nature are not yet available. Other factors, such as wood species, local climate, design details, exposure conditions (esp. in roofs and trusses, cellars, and door frames) and coatings might have an indirect effect on wood decay (e.g., Thybring 2017, Meyer and Brischke 2015). Under ideal moisture and temperature conditions, fungal growth may occur even within days. In theory, wood decay fungi need free water as a diffusion medium for their extracellular digestive enzymes. In the case of brown-rot (or dry-rot) fungi, other factors in addition to enzymatic processes are involved in wood degradation. Low molecular weight compounds, such as oxalate, veratryl alcohol, variegatic acid and others (Goodell et al. 1997; Eastwood et al. 2011; Watkinson and Eastwood 2012), contribute to lignocellulose decay, as do Fe and most likely other bivalent ions. These chemicals generate hydroxyl, peroxyl and hydroxylperoxyl radicals in Fenton and Fenton-like systems. Inorganic elements play an important role in the physiology and control of at least S. lacrymans growth (Schilling 2010; Watkinson and Eastwood 2012). As has been demonstrated (Low et al. 2000), S. lacrymans removes calcium, silicon and iron from sandstone and calcium, sulphur and iron from traditional plaster. The sequestered elements are located in its hyphae, particularly in the form of calcium oxalate.
2.
Detection and identification of decay fungi
Fruiting bodies are normally preferentially used for field identification (e.g., Abrego and Salcedo 2015, Nicolotti et al. 2010). Some species rarely fructify in buildings but form mycelial
strands (cords). Frankl (2014) found vital mycelia or active fruiting bodies only in only 7 % of his observations (but the remains were found in 95 %). Many studies address the diagnostics of wood decaying fungi based on their macromorphology and micromorphology; i.e., the typical shape and colour of fruiting bodies or spores, cell wall thickness of hyphae, type of branching, presence of dolipore septa, clamp connections or aggregates on the surface or inside the cells, etc. Typical visible properties (brown or white discolouration, eventually cracking into roughly cubical pieces) of degraded wood are also very important. Following the crucial work of Falck (1912), newer diagnostic keys including drawings or colour ski (1972), photographs have been published, e.g., by Doman Stalpers (1978), Hanlin (1998), Schmidt (2006), Huckfeldt and Schmidt (2006), Buchalo et al. (2009) and Stancheva et al. (2009). Precise molecular methods were not available for the identification of indoor wood decay fungi until the 1980s. These methods include species-specific priming PCR (SSPP), rDNA ITS region sequence analysis, restriction fragment length polymorphism analysis (RFLP), random amplified polymorphic DNA analysis (RAPD), amplified fragment length polymorphism analysis (AFLP) and sequence-specific oligonucleotide probe analysis (SSO). For more information, see the work of Maurice et al. (2011) or the recent paper by Raja et al. (2017) and references cited herein. Methods based on DNA analyses can provide efficient, sensitive and rapid diagnostic tools for the detection and identification of wood decay fungi without requiring a prior fungal isolation step (Glaeser and Lindner 2011, Gonthier et al. 2015). In the case of wood decay basidiomycetes, methods based on ribosomal DNA (ITS 1 or 2 rDNA region) sequencing have been established as routine techniques for the identification of fungi to the species level, esp. for those that are hardly or not at all distinguishable by species, such as Antrodia, Coniophora and Leucogyrophana (Schmidt 2006, Jarosch and Besl, 2001; Binder and Hibbett, 2006, Coetzee et al., 2003; Schmidt et al., 2012). In the last ten years, sequencing technologies have changed dramatically, offering multiple options in throughput, accuracy and cost for answering different biological questions. Some other alternative techniques are based on the production of typical volatile organic compounds (VOC) by fungi (e.g., Schmidt and Kallow, 2005). In addition to 1-octen-3-ol (Ewen et al. 2004), which causes the typical smell of mushrooms, several other compounds typical of fungi have been described (e.g., Anton et al. 2016, Konuma et al. 2015, Korpia
Table 1 e Humidity requirements (wood moister content; %) of selected fungi with respect to the colonization and decay of wood (after Schmidt 2007). Species Serpula lacrymans Leucogyrophana pinastri Coniophora puteana Antrodia vaillantii Donkioporia expansa Gloeophyllum abietinum Gloeophyllum sepiarium Gloeophyllum trabeum
Minimum for colonization
Minimum for decay
Optimum for decay
Maximum for decay
21 30 18 22 21 20 28 25
26 37 22 29 26 22 30 31
45e140 44e151 36e210 52e150 34e126 40e208 46e207 46e179
240 184 262 209 256 256 225 191
Please cite this article in press as: Gabriel, J., Svec, K., Occurrence of indoor wood decay basidiomycetes in Europe, Fungal Biology Reviews (2017), http://dx.doi.org/10.1016/j.fbr.2017.05.002
Occurrence of indoor wood decay
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et al. 1998). In a study focused on wood decay fungi, Konuma et al. (2015) reported 110 organic compounds, some of them produced only when fungi were cultivated on wood. Based on this, the use of dogs trained to sniff out S. lacrymans in buildings should also be noted (Watkinson and Eastwood, 2012), mostly as a curiosity.
3. Abundance of wood decay basidiomycetes in Europe The abundance of indoor wood decay basidiomycetes reported in Europe in the past few years is summarized in Table 2. Schmidt (2007) also listed species found in Danish buildings (after Bech-Andersen 1995) but without percentage incidence; the list includes the white-rot basidiomycetes Coprinus domesticus, Fomes fomentarius, Hyphoderma puberum, Hypholoma fasciculare, Perenniporia medulla-panis, Phellinus nigrolimitatus, Phlebiopsis gigantea, Physisporinus vitreus and Sistoterma brinkmannii; the only brown-rot fungi mentioned are Dacromyces tortus, Daedalea quercina, Laetiporus sulphureus and Oligoporus caesius. Alfredsen et al. (2005) also give a detailed survey of fungi found in publications from several Nordic countries. A list of 40 wood decay species found in the roofs or cellars of damaged buildings in the Czech Republic was published a few years ago (Vampola 2008). The author did not provide the percent incidence, but the most abundant species were Antrodia serialis, Coniophora puteana, Coniophora marmorata, Donkioporia expansa, Fomitopsis rosea, Gloeophyllum trabeum, P. gigantea and S. lacrymans. The author also demonstrated the occurrence of some rare species (Amyloporia xantha, Asterostroma ochroleucum, Hypochnicium bombycinum, O. caesius and Tubulicrinis thermometrus, etc.). Unlike other fungi, A. ochroleucum belongs to the rare species found in buildings; Vampola (2008) reported only two occurrences in historical buildings in the Czech Republic. He also stated that Coniophora confluens is a good indicator of elevated moisture content in buildings, and roof leaks should primarily be evaluated in this case.
The author also speculated about the origin of F. rosea in damaged buildings. According to him, wood timbers previously infected by this fungus were used for building houses, and F. rosea is able to survive in this substrate for many (tens or even hundreds) years, but this speculation is of course questionable. Nevertheless, Vampola (2008) reported the formation of fruiting bodies of F. rosea on a timber removed from the roof after being deposited in the fcourtyard of a historical building over 2e3 weeks; the timber was estimated to be ca. 200 y old. The same species was also reported in historic monuments in Romania (Bucs¸a and Bucs¸a 2009b). The most abundant basidiomycete across Europe is S. lacrymans, as is clearly shown in Table 2, followed by C. puteana. The literature about both fungi and their properties or requirements is so exhaustive that it is neither necessary nor possible to list them here. Antrodia damage seems to be more common in Norway than in other countries. One explanation for why Antrodia is most common in Norway might be climate; other explanations might be building traditions and the spore rain inoculum potential. Alfredsen et al. (2005) stated that Antrodia sp. demands much more moisture than S. lacrymans and slightly more than C. puteana since its optimum lies between 35 % and 55 % wood moisture content. According to Bech-Andersen (1996), A. sinuosa was found mostly in roof constructions, such as unventilated attics under the roofing felt, often in competition with Gloeophyllum. The occurrence of multiple fungi at one site is likely common; Schultze-Dewitz (1985) reported that S. lacrymans was often found together with C. puteana or Poria placenta. Recently, Pottier et al. (2014) studied fungal contamination in homes located in Low Normandy in France and reported that S. lacrymans was sometimes detected with the co-occurrence of other basidiomycete wood decay species like such as D. expansa; Maurice et al. (2011) repeatedly detected S. lacrymans, D. expansa and C. puteana, and in another sample from northwestern France, the occurrence of white-rot species Trametes versicolor and Hyphodontia sp. In a supplementary table, the authors listed 76 isolates of S. lacrymans from Norway,
Table 2 e Species abundance (%) of indoor basidiomycetes reported in Europe. Species Serpula lacrymans Coniophora puteana Antrodia vaillantii Antrodia sinuosa Gloeophyllum sp. Donkioporia expansa Poria placenta Total number of occurrences Total number of species Data since until Identification method**
Polanda BRDb DDRc DDRc Belgiumd Norwaye Latviaf Denmarke Finlande Estoniag Romaniah 54 22 2 9 2 e e 3050 29 1950 1960 m
27 17 10 2 6 10 e 748 31 2000 2006 n/a
29 18 e e 1 e 6 1005 11 1966 1980 n/a
22 17 e e e e 13 498 11 1980 1984 n/a
60 10 1 2 1 10 e 749 26 1985 1991 n/a
16 16 18* e 3 10 e 3434 35 2001 2003 n/a
47 6 13* e 3 e e 338 60 1996 2007 m
20 34 0,1* e 5 e e 8293 n/a 1946 1983 n/a
45 12 12* e 2 e e 1237 n/a 1978 1988 n/a
79 7 e e e e e 633 n/a 2002 2008 m
32 60 21 e 11 21 e n/a 75 1979 2009 m
_ References: aWazny and Czajnik (1963); bSchmidt (2007); cSchultze-Dewitz (1985); dGuillitte (1992); eAlfredsen et al. (2005); fIrbe and Andersone g (2008); Pilt et al. (2009); hBucs¸a and Bucs¸a (2009a). * Data given for Antrodia sp.; BRD ¼ Bundesrepublik Deutschland (former “West Germany”), DDR ¼ Deutsche Demokratische Republik (former “East Germany”). ** m e morphology.
Please cite this article in press as: Gabriel, J., Svec, K., Occurrence of indoor wood decay basidiomycetes in Europe, Fungal Biology Reviews (2017), http://dx.doi.org/10.1016/j.fbr.2017.05.002
J. Gabriel, K. Svec
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Finland, the UK, Germany, Belgium, and France isolated between 1939 (Berlin, Germany) and 2011 (Brest, France). In this study, ITS or beta-tubuline analyses were used in some cases. Frankl (2014) described fungi from sixteen smaller churches in different places in the Czech Republic (1999e2012) and reported the combined occurrences of the genera Coniophora with Gloeophyllum (3), Serpula (8), Stereum (6) and Trametes (19); Gloeophyllum with Serpula (1) or Trametes (10) and Trametes with Stereum (2) or Antrodia (1). In some cases, he found a combination of three different genera (e.g., Coniophora, Gloeophyllum and Trametes e 5). The repeated detection of various fungi in a single place could make the interpretation of some tables ambiguous. In an exhaustive work by Bucs¸a and Bucs¸a (2009a), the authors reported the results of an investigation of more than 400 historic monuments (castles, palaces, citadels, churches of all faiths, etc.) in Romania. The authors presented a list of 74 fungal species found in more than 1200 buildings. With the exception of Dacrymyces stillatus, which is found mostly on spruce shingle roofings (in 270 buildings), the most frequent infections were caused by Hyphodontia breviseta (80), Gl. abietinum (78) and sepiarium (67), T. versicolor (54), C. puteana (45), S. hirsutum (42) and D. expansa (40). The data for Romania given in Table 2 were taken from the summary reported for wood, masonry and plastered wood buildings together. Wood decay basidiomycetes from unusual locations have also been sometimes reported. For example, Lentinus suffrutesmec 1941), as well as Poscens was found in mine timbering (Ne c ek 1957). We found S. tia stiptica and Postia caesia (Rypa lacrymans forming unusual white branching fruiting bodies ınka in the Czech on timbering in a uranium mine in Dolnı Roz _ Republic (unpublished). Wazny and Czajnik (1963) reported the occurrence of S. lacrymans, Poria vaillantii, Corticium laeve, Corticium byssinum and Peniophora setigera on wooden and concrete structures in the Warsaw subway. In another case study, Kazartsev et al. (2014) found S. lacrymans and A. xantha, both stated as common indoor wood decay fungi in St. Petersburg, in wooden structures of the hotel “Mikhaylovskaya” and in a wooden pavilion of the Narcological dispensary situated in the historical city centre of St. Petersburg. Shumka et al. (2010) investigated 5 post-byzantine churches in the Prespa area (Albania), where fungal attack was caused only by C. g et al. (2014) studied wooden puteana. In another study, Koziro barracks as well as wooden elements of brick buildings (doors, floors, bunks, door and window frames, and structural walls and beams) in the former Auschwitz II e Birkenau camp. The authors found S. lacrymans, Corticium leave and Poria vaporaria on bunks, beams and floors. Although S. lacrymans is found in buildings in temperate regions in Eurasia, North and South America, and Oceania (Australia/New Zealand), in contrast to the frequent indoor occurrence of S. lacrymans, its absence in nature has remained an enigma for many years. In their review on S. lacrymans (2012), Kauserud et al. reported that some of the first reliable reports are from wooden sailing vessels in the 17th century, where it presumably caused severe damage (Ramsbottom, 1937). Up to now, the fungus has been reported in India, Pakistan, China, the USA, Russia (Kauserud et al. 2012) and the Czech Republic (Kotlaba 1992, 2012).
Some works describing fungi found in the wood of urban trees have also been published (e.g., Schmidt et al. 2012, Guglielmo et al. 2007 and literature cited herein), but from the viewpoint of possible building damage, they do not seem to be very important (perhaps with the exception of Gloeophyllum sp.).
4.
Summary
S. lacrymans and C. puteana are the most frequently found fungi reported in damaged buildings in Europe. This is likely a result of the common knowledge of these fungi, which form typical fruiting bodies. The occurrence of other wood decay fungi may not necessarily be reported to specialized laboratories/facilities and could not be fully included in the available statistics. Some other questions might arise with the development of new molecular methods for the identification of fungi that were previously difficult to distinguish. Nevertheless, the damage caused by S. lacrymans and C. puteana is so well documented that there is no doubt about their “leading role” across the Europe.
Acknowledgements This work was supported by the Institute of Microbiology CAS (RVO61388971) and by the Czech Science Foundation (GACR 17-05497S).
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Kazartsev, I.A., Serova, T.A., Titova, Y.A., Gannibal, P.B., 2014. Identification of wood-inhabiting fungal communities in two historical buildings of St. Petersburg. Mikol. Fitopatol. 48, 172e181. Konuma, R., Umezawa, K., Mizukoshi, A., Kawarada, K., Yoshida, M., 2015. Analysis of microbial volatile organic compounds produced by wood-decay fungi. Biotechnol. Lett. 37, 1845e1852. http://dx.doi.org/10.1007/s10529-015-1870-9. Korpia, A., Pasanen, A.-L., Viitanenb, H., 1998. Volatile metabolites of Serpula lacrymans, Coniophora puteana, Poria placenta, Stachybotrys chartarum and Chaetomium globosum. Build. Environ. 34, 205e211. http://dx.doi.org/10.1016/S0360-1323(98) 00011-0. lezy drevomorky doma cı e Serpula lacrymans Kotlaba, F., 1992. Na . (Findings of Serpula lacrymans in nature). Czech v prırode Mycol. 46, 143e147 (in Czech). m” Kotlaba, F., 2012. To the mycoflora of a forest called “V Stare dice, South Bohemia. Acta Musei Bohemiae MerNW of Nedve Bude jovice e Sci. Nat. 52, 119e132 (in Czech). idionalis Cesk e g, A., Otlewska, A., Piotrowska, M., Rajkowska, K., NowKoziro icka-Krawczyk, P., Hachu1ka, M., Wolski, G.J., Gutarowska, B., ska, A., Libudzisz, Z., Zakowska, Z., ZydzikKunicka-Styczyn Bia1ek, A., 2014. Colonising organisms as a biodegradation factor affecting historical wood materials at the former concentration camp of Auschwitz II e Birkenau. Int. Biodeterior. Biodegr. 86, 171e178. http: //dx.doi.org/10.1016/j.ibiod.2013.08.004. Krzyzanowski, N., Oduyemi, K., Jack, N., Ross, N.M., Palfreyman, J.W., 1999. The Management and Control of Dry Rot: A Survey of Practitioners Views and Experiences, pp. 143e154. http://dx.doi.org/10.1006/jema.1999.0301. Low, G.A., Young, M.E., Martin, P., Palfreyman, J.W., 2000. Assessing the relationship between the dry rot fungus Serpula lacrymans and selected forms of masonry. Int. Biodeterior. Biodegr. 46, 141e150. http://dx.doi.org/10.1016/S0964-8305(00)00089-5. re , M., Barbier, G., 2011. Maurice, S., Le Floch, G., Le Bras-Que Improved molecular methods to characterise Serpula lacrymans and other Basidiomycetes involved in wood decay. J. Microbiol. Methods 84, 208e215. http: //dx.doi.org/10.1016/j.mimet.2010.11.018. Meyer, L., Brischke, C., 2015. Fungal decay at different moisture levels of selected European-grown wood species. Int. Biodeterior. Biodegrad. 103, 23e29. http: //dx.doi.org/10.1016/j.ibiod.2015.04.009. mec, B., 1941. Zivot Ne rostlin. B. Janda, Sfinx, Praha (in Czech). Nicolotti, G., Gonthier, P., Guglielmo, F., 2010. Advances in detection and identification of wood rotting fungi in timber and standing trees. Chapter. In: Molecular Identification of Fungi, pp. 251e276. Palfreyman, J.W., 1995. The Impact of Current Research on the Treatment of Infestations by the Dry Rot Fungus Serpula lacrymans 8305, pp. 369e395. Pilt, K., Oja, J., Pau, K., 2009. The wood-destroying fungi in buildings in Estonia. WIT Trans. Built Environ. 109, 243e251. http: //dx.doi.org/10.2495/STR090221. Pottier, D., Andre, V., Rioult, J., Bourreau, A., Duhamel, C., Bouchart, V.K., Richard, E., Guibert, M., Verite, P., Garon, D., 2014. Airborne molds and mycotoxins in Serpula lacrymansedamaged homes. Atmos. Pollut. Res. 5, 325e334. http: //dx.doi.org/10.5094/APR.2014.038. Raja, H.A., Miller, A.N., Pearce, C.J., Oberlies, N.H., 2017. Fungal identification using molecular tools: a primer for the Natural Products Research Community. J. Nat. Prod. 80 (3), 756e770. http: //dx.doi.org/10.1021/acs.jnatprod.6b01085. Epub 2017 Feb 15. Ramsbottom, J., 1937. Dry rot in ships. Essex Nat. 25, 231e267. Cited in: Kauserud 2012. Rayner, A.D.M., Boddy, L., 1988. Fungal Decomposition of Wood: its Biology and Ecology. Wiley, Chichester.
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c ek, V., 1957. Biologie drevokazny ch hub. NCSAV, Rypa Praha. See € render Pilze. Fischer. Jena 1966. also Biologie holzzersto Shumka, L., Marku, M., Shumka, S., 2010. The study of biological decay with church wooden materials in Prespa Lake area, Albania. Nat. Montenegrina, Podgor. 9, 827e831. Schilling, J.S., 2010. Effects of calcium-based materials and iron impurities on wood degradation by the brown rot fungus Serpula lacrymans. Holzforschung Int. J. Biol. Chem. Phys. Technol. Wood 64, 93e99. Schmidt, O., 2007. Indoor wood-decay basidiomycetes: damage, causal fungi, physiology, identification and characterization, prevention and control. Mycol. Prog. 6, 261e279. http: //dx.doi.org/10.1007/s11557-007-0534-0. Schmidt, O., Gaiser, O., Dujesiefken, D., 2012. Molecular Identification of Decay Fungi in the Wood of Urban Trees, pp. 885e891. http://dx.doi.org/10.1007/s10342-011-0562-9. Schmidt, O., 2006. Wood and Tree Fungi. Biology, Damage, Protection and Use. Springer. Schmidt, O., Kallow, W., 2005. Differentiation of indoor wood decay fungi with MALDI-TOF mass spectrometry. Holzforschung 59, 374e377. http://dx.doi.org/10.1515/HF.2005.062.
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€ digende Organismen in der Schultze-Dewitz, G., 1985. Holzscha Altbausubstanz. Bauzeitung 39, 565e566. Stalpers, J.A., 1978. Identification of Wood-Inhabiting Aphyllophorales in Pure Culture. Centraalbureau voor Schimmelcultures, Baarn. Stancheva, Y., Bencheva, S., Pavlidis, T., Ilieva, M., 2009. Atlas of Wood Decaying Fungi. Pensoft, Sofia-Moscow. Thybring, E.T., 2017. Water relations in untreated and modified wood under brown-rot and white-rot decay. Int. Biodeterior. Biodegrad. 118 (2017), 134e142. http: //dx.doi.org/10.1016/j.ibiod.2017.01.034. houby v budova ch. Mykol. listy. Vampola, P., 2008. Drevokazne ISSN: 1213-5887 104, 21e25 (in Czech). Watkinson, S.C., Eastwood, D.C., 2012. Serpula lacrymans, wood and buildings. Adv. Appl. Microbiol. 78, 121e149. http: //dx.doi.org/10.1016/B978-0-12-394805-2.00005-1. w _ Wazny, H., Czajnik, M., 1963. Wyste˛powanie grzybo niszcza˛cych drewno w budynkach na terenie Polski. Folia For. Pol. B 5, 5e17 (in Polish).
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Review
Occurrence of indoor wood decay basidiomycetes in Europe Jirı GABRIEL*, Karel SVEC ska 1083, 142 20 Prague 4, Krc, Laboratory of Environmental Microbiology, Institute of Microbiology AS CR, Vıden Czech Republic
article info
abstract
Article history:
Brown-rot fungi are considered to be the most important wood-inhabiting fungi econom-
Received 1 March 2017
ically, as they also deteriorate the wood that has been used in buildings. In the northern
Received in revised form
hemisphere, coniferous wood is the main source of interior structural timber. White-rot
9 May 2017
fungi, which degrade lignin and preferentially attack hardwood, are less common.
Accepted 9 May 2017
Emphasis is usually placed on Serpula lacrymans or Coniophora puteana, which are the most common indoor basidiomycetes found in buildings in Europe. In this review, we sum-
Keywords:
marize available data on the occurrence of wood decay fungi in the Czech Republic, Poland,
Basidiomycetes
Germany (both former East and West), Belgium, France, Norway, Denmark, Finland, Latvia,
Fungi
Estonia, Romania and Albania reported in the past few decades. The total number of occur-
Indoor
rences was near 20,000; original data were collected between 1946 and 2008. The most
Serpula lacrymans
abundant basidiomycetes were S. lacrymans and C. puteana, with the exception of Norway, where the genus Antrodia was the most frequent. ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved.
1.
Introduction
Indoor wood decay fungi cause many problems worldwide; fungi that invade roofs, walls, ceilings, etc., represent a group of various basidiomycetes that are in many cases resistant to currently used fungicides. These fungi attack and damage wooden houses and other wooden constructions, and the most well-known of these, Serpula lacrymans (often regarded as the “cancer of buildings”), is responsible for many millions of USD of damage each year (Palfreyman, 1995). For example, the cost of fungal damage in France was estimated to be approximately V 30 million yearly (Maurice et al. 2011), and in the UK, the cost of repairing fungal damage to timber used in construction amounted to £ 3 million per week
(Rayner and Boddy 1988). The dry rot remediation business in the UK was estimated to be worth an excess of £ 400 million (Krzyzanowski et al. 1999). The decay of wood and wood-based products usually begins when the spores or mycelial fragments adhere to the wood surface. Wood moisture and temperature are the most important features in terms of the “building habitat”. Humphrey and Siggers (1933) previously studied the effect of temperature on the growth rate of 56 wood-decay fungi and found that none would grow below 12 C and that most would not grow above 40 C. According to many authors and guidelines for the protection of wood and wood products from attack by decay fungi, it is important and necessary to keep wood or wooden constructions at a moisture content below
* Corresponding author. http://dx.doi.org/10.1016/j.fbr.2017.05.002 1749-4613/ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved.
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J. Gabriel, K. Svec
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20 % (Carll and Highley 1999). Schmidt (2007) reported minimum and maximum humidity requirements for fungi identified by means of ITS sequencing (to avoid unreliable data for incorrectly identified species; Table 1). As stated by Carll and Highley (1999), the spores of wood decay fungi do not germinate and fungal hyphae do not grow at moisture levels much below the fibre saturation point, which is at approximately 30 % moisture. However, only the part of water that is not bound by dissolved substances (salts, sugars) is available to fungi; a detailed description of the optimum conditions for wood decay in terms of water activity (aw), water potential or relative air humidity (RH) can be found, e.g., in the abovementioned review of Schmidt (2007). However, data on fungal development under fluctuating moisture conditions that are more common in nature are not yet available. Other factors, such as wood species, local climate, design details, exposure conditions (esp. in roofs and trusses, cellars, and door frames) and coatings might have an indirect effect on wood decay (e.g., Thybring 2017, Meyer and Brischke 2015). Under ideal moisture and temperature conditions, fungal growth may occur even within days. In theory, wood decay fungi need free water as a diffusion medium for their extracellular digestive enzymes. In the case of brown-rot (or dry-rot) fungi, other factors in addition to enzymatic processes are involved in wood degradation. Low molecular weight compounds, such as oxalate, veratryl alcohol, variegatic acid and others (Goodell et al. 1997; Eastwood et al. 2011; Watkinson and Eastwood 2012), contribute to lignocellulose decay, as do Fe and most likely other bivalent ions. These chemicals generate hydroxyl, peroxyl and hydroxylperoxyl radicals in Fenton and Fenton-like systems. Inorganic elements play an important role in the physiology and control of at least S. lacrymans growth (Schilling 2010; Watkinson and Eastwood 2012). As has been demonstrated (Low et al. 2000), S. lacrymans removes calcium, silicon and iron from sandstone and calcium, sulphur and iron from traditional plaster. The sequestered elements are located in its hyphae, particularly in the form of calcium oxalate.
2.
Detection and identification of decay fungi
Fruiting bodies are normally preferentially used for field identification (e.g., Abrego and Salcedo 2015, Nicolotti et al. 2010). Some species rarely fructify in buildings but form mycelial
strands (cords). Frankl (2014) found vital mycelia or active fruiting bodies only in only 7 % of his observations (but the remains were found in 95 %). Many studies address the diagnostics of wood decaying fungi based on their macromorphology and micromorphology; i.e., the typical shape and colour of fruiting bodies or spores, cell wall thickness of hyphae, type of branching, presence of dolipore septa, clamp connections or aggregates on the surface or inside the cells, etc. Typical visible properties (brown or white discolouration, eventually cracking into roughly cubical pieces) of degraded wood are also very important. Following the crucial work of Falck (1912), newer diagnostic keys including drawings or colour ski (1972), photographs have been published, e.g., by Doman Stalpers (1978), Hanlin (1998), Schmidt (2006), Huckfeldt and Schmidt (2006), Buchalo et al. (2009) and Stancheva et al. (2009). Precise molecular methods were not available for the identification of indoor wood decay fungi until the 1980s. These methods include species-specific priming PCR (SSPP), rDNA ITS region sequence analysis, restriction fragment length polymorphism analysis (RFLP), random amplified polymorphic DNA analysis (RAPD), amplified fragment length polymorphism analysis (AFLP) and sequence-specific oligonucleotide probe analysis (SSO). For more information, see the work of Maurice et al. (2011) or the recent paper by Raja et al. (2017) and references cited herein. Methods based on DNA analyses can provide efficient, sensitive and rapid diagnostic tools for the detection and identification of wood decay fungi without requiring a prior fungal isolation step (Glaeser and Lindner 2011, Gonthier et al. 2015). In the case of wood decay basidiomycetes, methods based on ribosomal DNA (ITS 1 or 2 rDNA region) sequencing have been established as routine techniques for the identification of fungi to the species level, esp. for those that are hardly or not at all distinguishable by species, such as Antrodia, Coniophora and Leucogyrophana (Schmidt 2006, Jarosch and Besl, 2001; Binder and Hibbett, 2006, Coetzee et al., 2003; Schmidt et al., 2012). In the last ten years, sequencing technologies have changed dramatically, offering multiple options in throughput, accuracy and cost for answering different biological questions. Some other alternative techniques are based on the production of typical volatile organic compounds (VOC) by fungi (e.g., Schmidt and Kallow, 2005). In addition to 1-octen-3-ol (Ewen et al. 2004), which causes the typical smell of mushrooms, several other compounds typical of fungi have been described (e.g., Anton et al. 2016, Konuma et al. 2015, Korpia
Table 1 e Humidity requirements (wood moister content; %) of selected fungi with respect to the colonization and decay of wood (after Schmidt 2007). Species Serpula lacrymans Leucogyrophana pinastri Coniophora puteana Antrodia vaillantii Donkioporia expansa Gloeophyllum abietinum Gloeophyllum sepiarium Gloeophyllum trabeum
Minimum for colonization
Minimum for decay
Optimum for decay
Maximum for decay
21 30 18 22 21 20 28 25
26 37 22 29 26 22 30 31
45e140 44e151 36e210 52e150 34e126 40e208 46e207 46e179
240 184 262 209 256 256 225 191
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Occurrence of indoor wood decay
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et al. 1998). In a study focused on wood decay fungi, Konuma et al. (2015) reported 110 organic compounds, some of them produced only when fungi were cultivated on wood. Based on this, the use of dogs trained to sniff out S. lacrymans in buildings should also be noted (Watkinson and Eastwood, 2012), mostly as a curiosity.
3. Abundance of wood decay basidiomycetes in Europe The abundance of indoor wood decay basidiomycetes reported in Europe in the past few years is summarized in Table 2. Schmidt (2007) also listed species found in Danish buildings (after Bech-Andersen 1995) but without percentage incidence; the list includes the white-rot basidiomycetes Coprinus domesticus, Fomes fomentarius, Hyphoderma puberum, Hypholoma fasciculare, Perenniporia medulla-panis, Phellinus nigrolimitatus, Phlebiopsis gigantea, Physisporinus vitreus and Sistoterma brinkmannii; the only brown-rot fungi mentioned are Dacromyces tortus, Daedalea quercina, Laetiporus sulphureus and Oligoporus caesius. Alfredsen et al. (2005) also give a detailed survey of fungi found in publications from several Nordic countries. A list of 40 wood decay species found in the roofs or cellars of damaged buildings in the Czech Republic was published a few years ago (Vampola 2008). The author did not provide the percent incidence, but the most abundant species were Antrodia serialis, Coniophora puteana, Coniophora marmorata, Donkioporia expansa, Fomitopsis rosea, Gloeophyllum trabeum, P. gigantea and S. lacrymans. The author also demonstrated the occurrence of some rare species (Amyloporia xantha, Asterostroma ochroleucum, Hypochnicium bombycinum, O. caesius and Tubulicrinis thermometrus, etc.). Unlike other fungi, A. ochroleucum belongs to the rare species found in buildings; Vampola (2008) reported only two occurrences in historical buildings in the Czech Republic. He also stated that Coniophora confluens is a good indicator of elevated moisture content in buildings, and roof leaks should primarily be evaluated in this case.
The author also speculated about the origin of F. rosea in damaged buildings. According to him, wood timbers previously infected by this fungus were used for building houses, and F. rosea is able to survive in this substrate for many (tens or even hundreds) years, but this speculation is of course questionable. Nevertheless, Vampola (2008) reported the formation of fruiting bodies of F. rosea on a timber removed from the roof after being deposited in the fcourtyard of a historical building over 2e3 weeks; the timber was estimated to be ca. 200 y old. The same species was also reported in historic monuments in Romania (Bucs¸a and Bucs¸a 2009b). The most abundant basidiomycete across Europe is S. lacrymans, as is clearly shown in Table 2, followed by C. puteana. The literature about both fungi and their properties or requirements is so exhaustive that it is neither necessary nor possible to list them here. Antrodia damage seems to be more common in Norway than in other countries. One explanation for why Antrodia is most common in Norway might be climate; other explanations might be building traditions and the spore rain inoculum potential. Alfredsen et al. (2005) stated that Antrodia sp. demands much more moisture than S. lacrymans and slightly more than C. puteana since its optimum lies between 35 % and 55 % wood moisture content. According to Bech-Andersen (1996), A. sinuosa was found mostly in roof constructions, such as unventilated attics under the roofing felt, often in competition with Gloeophyllum. The occurrence of multiple fungi at one site is likely common; Schultze-Dewitz (1985) reported that S. lacrymans was often found together with C. puteana or Poria placenta. Recently, Pottier et al. (2014) studied fungal contamination in homes located in Low Normandy in France and reported that S. lacrymans was sometimes detected with the co-occurrence of other basidiomycete wood decay species like such as D. expansa; Maurice et al. (2011) repeatedly detected S. lacrymans, D. expansa and C. puteana, and in another sample from northwestern France, the occurrence of white-rot species Trametes versicolor and Hyphodontia sp. In a supplementary table, the authors listed 76 isolates of S. lacrymans from Norway,
Table 2 e Species abundance (%) of indoor basidiomycetes reported in Europe. Species Serpula lacrymans Coniophora puteana Antrodia vaillantii Antrodia sinuosa Gloeophyllum sp. Donkioporia expansa Poria placenta Total number of occurrences Total number of species Data since until Identification method**
Polanda BRDb DDRc DDRc Belgiumd Norwaye Latviaf Denmarke Finlande Estoniag Romaniah 54 22 2 9 2 e e 3050 29 1950 1960 m
27 17 10 2 6 10 e 748 31 2000 2006 n/a
29 18 e e 1 e 6 1005 11 1966 1980 n/a
22 17 e e e e 13 498 11 1980 1984 n/a
60 10 1 2 1 10 e 749 26 1985 1991 n/a
16 16 18* e 3 10 e 3434 35 2001 2003 n/a
47 6 13* e 3 e e 338 60 1996 2007 m
20 34 0,1* e 5 e e 8293 n/a 1946 1983 n/a
45 12 12* e 2 e e 1237 n/a 1978 1988 n/a
79 7 e e e e e 633 n/a 2002 2008 m
32 60 21 e 11 21 e n/a 75 1979 2009 m
_ References: aWazny and Czajnik (1963); bSchmidt (2007); cSchultze-Dewitz (1985); dGuillitte (1992); eAlfredsen et al. (2005); fIrbe and Andersone g (2008); Pilt et al. (2009); hBucs¸a and Bucs¸a (2009a). * Data given for Antrodia sp.; BRD ¼ Bundesrepublik Deutschland (former “West Germany”), DDR ¼ Deutsche Demokratische Republik (former “East Germany”). ** m e morphology.
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Finland, the UK, Germany, Belgium, and France isolated between 1939 (Berlin, Germany) and 2011 (Brest, France). In this study, ITS or beta-tubuline analyses were used in some cases. Frankl (2014) described fungi from sixteen smaller churches in different places in the Czech Republic (1999e2012) and reported the combined occurrences of the genera Coniophora with Gloeophyllum (3), Serpula (8), Stereum (6) and Trametes (19); Gloeophyllum with Serpula (1) or Trametes (10) and Trametes with Stereum (2) or Antrodia (1). In some cases, he found a combination of three different genera (e.g., Coniophora, Gloeophyllum and Trametes e 5). The repeated detection of various fungi in a single place could make the interpretation of some tables ambiguous. In an exhaustive work by Bucs¸a and Bucs¸a (2009a), the authors reported the results of an investigation of more than 400 historic monuments (castles, palaces, citadels, churches of all faiths, etc.) in Romania. The authors presented a list of 74 fungal species found in more than 1200 buildings. With the exception of Dacrymyces stillatus, which is found mostly on spruce shingle roofings (in 270 buildings), the most frequent infections were caused by Hyphodontia breviseta (80), Gl. abietinum (78) and sepiarium (67), T. versicolor (54), C. puteana (45), S. hirsutum (42) and D. expansa (40). The data for Romania given in Table 2 were taken from the summary reported for wood, masonry and plastered wood buildings together. Wood decay basidiomycetes from unusual locations have also been sometimes reported. For example, Lentinus suffrutesmec 1941), as well as Poscens was found in mine timbering (Ne c ek 1957). We found S. tia stiptica and Postia caesia (Rypa lacrymans forming unusual white branching fruiting bodies ınka in the Czech on timbering in a uranium mine in Dolnı Roz _ Republic (unpublished). Wazny and Czajnik (1963) reported the occurrence of S. lacrymans, Poria vaillantii, Corticium laeve, Corticium byssinum and Peniophora setigera on wooden and concrete structures in the Warsaw subway. In another case study, Kazartsev et al. (2014) found S. lacrymans and A. xantha, both stated as common indoor wood decay fungi in St. Petersburg, in wooden structures of the hotel “Mikhaylovskaya” and in a wooden pavilion of the Narcological dispensary situated in the historical city centre of St. Petersburg. Shumka et al. (2010) investigated 5 post-byzantine churches in the Prespa area (Albania), where fungal attack was caused only by C. g et al. (2014) studied wooden puteana. In another study, Koziro barracks as well as wooden elements of brick buildings (doors, floors, bunks, door and window frames, and structural walls and beams) in the former Auschwitz II e Birkenau camp. The authors found S. lacrymans, Corticium leave and Poria vaporaria on bunks, beams and floors. Although S. lacrymans is found in buildings in temperate regions in Eurasia, North and South America, and Oceania (Australia/New Zealand), in contrast to the frequent indoor occurrence of S. lacrymans, its absence in nature has remained an enigma for many years. In their review on S. lacrymans (2012), Kauserud et al. reported that some of the first reliable reports are from wooden sailing vessels in the 17th century, where it presumably caused severe damage (Ramsbottom, 1937). Up to now, the fungus has been reported in India, Pakistan, China, the USA, Russia (Kauserud et al. 2012) and the Czech Republic (Kotlaba 1992, 2012).
Some works describing fungi found in the wood of urban trees have also been published (e.g., Schmidt et al. 2012, Guglielmo et al. 2007 and literature cited herein), but from the viewpoint of possible building damage, they do not seem to be very important (perhaps with the exception of Gloeophyllum sp.).
4.
Summary
S. lacrymans and C. puteana are the most frequently found fungi reported in damaged buildings in Europe. This is likely a result of the common knowledge of these fungi, which form typical fruiting bodies. The occurrence of other wood decay fungi may not necessarily be reported to specialized laboratories/facilities and could not be fully included in the available statistics. Some other questions might arise with the development of new molecular methods for the identification of fungi that were previously difficult to distinguish. Nevertheless, the damage caused by S. lacrymans and C. puteana is so well documented that there is no doubt about their “leading role” across the Europe.
Acknowledgements This work was supported by the Institute of Microbiology CAS (RVO61388971) and by the Czech Science Foundation (GACR 17-05497S).
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