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Asian Origin and Rapid Global Spread of the Destructive Dry Rot Fungus

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Asian Origin and Rapid Global Spread of the Destructive Dry Rot Fungus Molecular Ecology (2007) 16, 3350–3360 doi: 10.1111/j.1365-294X.2007.03387.x AsianBlackwell Publishing Ltd origin and rapid global spread of the destructive dry rot fungus Serpula lacrymans HÅVARD KAUSERUD,* INGEBORG BJORVAND SVEGÅRDEN,* GLENN-PETER SÆTRE,† HENNING KNUDSEN,‡ ØYVIND STENSRUD,* OLAF SCHMIDT,§ SHUICHI DOI,¶ TOMOAKI SUGIYAMA** and NILS HÖGBERG†† *Department of Biology, University of Oslo, PO Box 1066 Blindern, N-0316 Oslo, Norway, †Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, PO Box 1066 Blindern, N-0316 Oslo, Norway, ‡Botanical Museum, Gothersgade 130, DK-1123 Copenhagen K., Denmark, §Wood Biology, University of Hamburg, Leuschnerstr. 91, D-21031 Hamburg, Germany, ¶Institute of Agricultural and Forest Engineering, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan, **Hokkaido Forest Products Research Institute, 1-10 Nishikagura, Asahikawa, Hokkaido 071-0198, Japan, ††Department of Forest Mycology & Pathology, Box 7026, Swedish University of Agricultural Sciences, S-750 07 Uppsala, Sweden Abstract The dry rot fungus Serpula lacrymans (Basidiomycota) is the most damaging destroyer of wood construction materials in temperate regions. While being a widespread aggressive indoor biodeterioration agent, it is only found in a few natural environments. The geo- graphical source of spread and colonization by this fungus in human environments is thus somewhat of an enigma. Employing genetic markers (amplified fragment length polymor- phisms, DNA sequences and microsatellites) on a worldwide sample of specimens, we show that the dry rot fungus is divided into two main lineages; one nonaggressive residing naturally in North America and Asia (var. shastensis), and another aggressive lineage including specimens from all continents, both from natural environments and buildings (var. lacrymans). Our genetic analyses indicate that the two lineages represent well-differentiated cryptic species. Genetic analyses pinpoint mainland Asia as the origin of the aggressive form var. lacrymans. A few aggressive genotypes have migrated worldwide from Asia to Europe, North and South America and Oceania followed by local population expansions. The very low genetic variation in the founder populations indicate that they have established through recent founder events, for example by infected wood materials transported over land or sea. A separate colonization has happened from mainland Asia to Japan. Our data also indicate that independent immigration events have happened to Oceania from different continents followed by admixture. Keywords: dispersal, dry rot fungus; founder events, invasive species, phylogeography, Serpula lacrymans Received 17 December 2006; revision received 6 March 2007; accepted 4 April 2007 damaging destroyer of indoor wood construction materials Introduction in temperate regions (Jennings & Bravery 1991; Schmidt Microbial damage of buildings has followed man since 2006). It was originally described in 1781 as Boletus lacrymans early civilization and is for example well described in the Wulfen, at that time being a well-known problem in Bible (Leviticus) as ‘leprosy on houses’. In contrast to plant European buildings and on sailing ships where it caused and animal pathogens, little attention has been paid to severe brown rot (Ramsbottom 1937). Today, it has a the population biology of fungi that infest construction widespread distribution in buildings in temperate regions materials. The dry rot fungus Serpula lacrymans (Wulfen: of Asia, Europe, North America and Oceania (Harmsen Fr.) Schroeter apud Cohn (Basidiomycota) is the most 1960; Jennings & Bravery 1991; Schmidt 2006). It has a maximum growth at 19–21 °C and does not tolerate high Correspondence: Håvard Kauserud, Fax: +47 22854726; E-mail: temperatures (Jennings & Bravery 1991), which probably [email protected] explain its absence from the tropics and regions with high © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd ASIAN ORIGIN OF SERPULA LACRYMANS 3351 1954; White et al. 2001; Palfreyman et al. 2003; Kauserud et al. 2004). The Himalayas has often been favoured as the most likely origin (Bagchee 1954; White et al. 2001), since it was first detected in natural environments in this region. Judged mainly from nuclear ribosomal DNA (nrDNA) internal transcribed spacer (ITS) sequences, it has previously been suggested that S. lacrymans has low genetic diversity (White et al. 2001; Palfreyman et al. 2003). However, in a recent study, it was shown that specimens from Northern California possessed divergent ITS sequences (Kauserud et al. 2004), indicating that some genetic substructure could exist within S. lacrymans. Specimens from California have been ascribed to the variety var. shastensis (Harmsen 1960). The fruit bodies produced by var. shastensis are slightly thinner than those produced by var. lacrymans (Fig. 1a, b). As far as we know, all known collections of var. shastensis are from high elevations in nature (over 3000 m above sea level), while most collections of var. lacrymans are from buildings, except the few collections from natural environ- ments in the Czech Republic, the Himalayas and East Asia. In this study, we have investigated the evolutionary origin and spread of this destructive species by means of population genetic and phylogeographical analyses of a comprehensive collection of isolates and dried specimens from man-made and natural habitats, covering basically its Fig. 1 Fruit bodies of Serpula lacrymans. (a) The aggressive entire known worldwide distribution. Recently collected form var. lacrymans that predominantly occurs in buildings in specimens from natural environments in Czech Republic, temperate regions worldwide. (b) The nonaggressive form var. California and East Asia gave us the opportunity to analyse shastensis that only has been detected in mountainous regions in the evolutionary origin of the dry rot fungus more exhaus- California and the Caucasus. (c) Section of a dikaryotic var. tive than earlier (White et al. 2001; Palfreyman et al. 2003; lacrymans × var. shastensis isolate producing minute fruit bodies (basidiocarps). No living monokaryotic progeny were obtained Kauserud et al. 2004). Three independent DNA data sets from the fruit bodies. were obtained; DNA sequences (haplotypes) from three nuclear loci (ITS, gpd and tub), microsatellite data from 15 recently characterized markers (Högberg et al. 2006), and 160 summer temperatures. Serpula lacrymans forms pancake- polymorphic amplified fragment length polymorphism like fruit bodies (basidiocarps) that produce billions of (AFLP) markers. wind-spread basidiospores (Fig. 1a). It has an outcrossing (heterothallic) reproductive mode (Harmsen 1960; Schmidt Materials and methods 2006) and the typical life cycle of basidiomycetes, including a short-lived monokaryotic phase succeeded by the dikaryotic Materials stage. The dikaryotic mycelium represents the dominant stage that can attack large parts of buildings (Fig. 1a), and DNA was extracted from 106 isolates and 45 dried after some time of expansion produce basidiocarps. The specimens of Serpula lacrymans (see Supplementary material) dry rot fungus is also capable of vegetative local spread via using a cetyltrimethyl ammonium bromide (CTAB) extraction mycelial strands (rhizomorphs) with the potential to grow protocol (Murray & Thompson 1980). several meters across inorganic material (Jennings & Bravery 1991; Schmidt 2006). AFLP analysis While being a widespread aggressive indoor biodeterio- ration agent, it has only been found in a few natural environ- A subset of 91 S. lacrymans isolates were analysed by AFLP ments, namely in the Himalayas (Bagchee 1954; White analysis (see Supplementary material). Because of high et al. 2001) and Northern California (Cook 1955; Harmsen contamination risks, only DNA extracted from living auxenic 1960) and more recently in the Czech Republic (Kotlaba isolates were used in AFLP analysis. The AFLP analysis 1992) and in East Asia (Kauserud et al. 2004). This paradox was performed essentially as described by Vos et al. (1995). has generated a lot of speculations as to its origin (Bagchee The restriction-ligation samples consisted of 5.5 µL undiluted © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd 3352 H. KAUSERUD ET AL. DNA extract and 5.5 µL restriction-ligation master mix: was mixed with 1.5 µL 6-FAM-labelled AFLP products µ µ µ µ 0.405 L milliQ-H2O, 1.100 L NaCl (0.5 m), 1.000 L EcoRI and 0.2 L of a GeneScan ROX-500 size standard kit adaptor pair (10 µm), 1.000 µL MseI adaptor pair (10 µm), (Applied Biosystems). The samples were denatured for 0.020 µL MseI (50 U/µL), 0.125 µL EcoRI (40 U/µL), 5 min at 95 °C, and thereafter placed on ice. After a 1-min 1.100 µL T4 DNA buffer 10×, 0.550 µL BSA (0.1%), 0.200 T4 centrifugation of the reaction plate at 300 g, electrophoresis DNA ligase (primers from MWG-Biotech; MseI from New was performed using an ABI 3100 genetic analyser England Biolabs, other reagents from Roche). The samples (Applied Biosystems) with POP4 polymer, default settings, were incubated for 3 h at 37 °C on an ABI 9700 (Applied and a 35-s injection time. The peak profiles were first checked Biosystems) thermocycler, and thereafter diluted 10 times and aligned using ABI genescan analysis software version in milliQ-H2O and mixed thoroughly. 3.7 (Applied Biosystems) and then viewed and scored as The preselective amplification reactions were performed binary characters in genographer
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