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Multiple Cryptic Species with Divergent Substrate Affinities in the Serpula

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FUNBIO104_proof ■ 3 November 2010 ■ 1/8 fungal biology xxx (2010) 1e8 1 66 2 67 3 68 4 69 5 70 6 71 7 journal homepage: www.elsevier.com/locate/funbio 72 8 73 9 74 10 75 11 Multiple cryptic species with divergent substrate affinities 76 12 Serpula himantioides 77 13 Q1 in the species complex 78 14 79 15 80 a, a b 16 Tor CARLSEN *, Ingeborg Bjorvand ENGH , Cony DECOCK , 81 17 Mario RAJCHENBERGc,Havard KAUSERUDa 82 18 83 19 aMicrobial Evolution Research Group (MERG), Department of Biology, University of Oslo, P.O. Box 1066, Blindern, N-0316 Oslo, Norway 84 20 bMycotheque de l’Universite Catholique de Louvain, Earth and Life Institute e Mycology, 1348 Louvain-la-Neuve, Belgium 85 c 86 21 Centro de Investigacion y Extension Forestal Andino Patagonico, C.C. 238, 9200 Esquel, Chubut, Argentina 22 87 23 88 24 article info abstract 89 25 90 26 91 Serpula himantioides 27 Article history: is a widespread saprotrophic morphospecies mainly colonising conifer- 92 28 Received 4 May 2010 ous wood in nature, but it appears frequently in buildings as well. From an earlier study, it 93 29 Received in revised form is known that at least three divergent lineages occur within the S. himantioides species 94 30 18 August 2010 complex. In this study, a broader sample of S. himantioides isolates has been analysed by 95 31 Accepted 15 October 2010 multi-locus sequencing, including new isolates from Asia, North and South America. Alto- 96 32 Corresponding Editor: gether five phylogenetical species (PS1e5) were detected, all recognised across indepen- 97 33 Karl-Henrik Larsson dent gene phylogenies. A new southern South American phylogenetic species (PS1) was 98 34 found, representing an early diverging lineage within the S. himantioides species complex. 99 35 100 Keywords: The two closely related PS2 and PS3 lineages included isolates from North America only, 36 101 Cryptic species and PS4 was also dominated by North American isolates. Most of the investigated isolates 37 102 Phylogenetic species (76 %) clustered into PS5, a lineage that has been found on most continents, including 38 103 39 Phylogeography North America. Overall, little phylogeographical structure was found in PS5, indicating fre- 104 40 Saprotrophic quent and recent long-distance dispersal events within this widespread lineage. Our anal- 105 41 Serpula himantioides yses indicate that South and North America are the centres of divergence for the 106 42 S. himantioides species complex. Some of the lineages seem adapted to various substrates, 107 43 but PS5 is able to decay a wide array of angiosperms and gymnosperms, which may have 108 44 facilitated the spread of this lineage throughout the world. 109 45 ª 2010 Published by Elsevier Ltd on behalf of The British Mycological Society. 110 46 111 47 112 48 113 49 114 50 Introduction differentiated lineages were detected within S. himantioides 115 51 across independent gene phylogenies (Kauserud et al. 2006). 116 52 Serpula himantioides (Fr.) P. Karst. is a saprotrophic morphospe- These three lineages also showed compatible mating within 117 53 118 cies with a wide geographical distribution, observed on all con- lineages, and incompatible mating between lineages. Thus, as 54 119 tinents except Antarctica. It is mainly found on dead wood of many other basidiomycetes (Nilsson et al. 2003; Geml et al. 55 120 56 various coniferous tree species, but do also commonly occur 2006; Kauserud et al. 2007a), S. himantioides seems to represent 121 57 in buildings. It produces thin, resupinate and brownish annual a species complex including multiple cryptic lineages. Espe- 122 58 basidiocarps and has a heterothallic tetrapolar mating system, cially when it comes to morphospecies that produces simple, 123 59 based on Northern Hemisphere specimens (Hwang 1955; resupinate fruiting structures, such as S. himantioides,itmight 124 60 Harmsen 1960). In a previous study, three genetically well- be problematic to detect species boundaries by morphological 125 61 126 62 127 63 * Corresponding author. Tel.: þ47 22854588; fax: þ47 22854726. 128 64 E-mail addresses: [email protected], [email protected], [email protected] 129 65 1878-6146/$ e see front matter ª 2010 Published by Elsevier Ltd on behalf of The British Mycological Society. 130 doi:10.1016/j.funbio.2010.10.004 Please cite this article in press as: Carlsen T et al., Multiple cryptic species with divergent substrate affinities in the Serpula himantioides species complex, Fungal Biology (2010), doi:10.1016/j.funbio.2010.10.004 FUNBIO104_proof ■ 3 November 2010 ■ 2/8 2 T. Carlsen et al. 131 means (Taylor et al. 2006). Likewise, multiple cryptic species has analyses. For Bayesian analyses, the different regions were 196 132 also been detected in several Coniophora species that also pro- analysed with an independent model for each partition 197 133 198 duce simple and resupinate fruiting bodies (Ainsworth & (ITS ¼ GTR þ I, LSU ¼ GTR, tub ¼ GTR þ G, and hsp ¼ SYM þ G). 134 199 Rayner 1990; Kauserud et al. 2007a). Genealogical sorting index (GSI) statistics (Cummings et al. 135 200 Biogeographical studies show that fungi have complex his- 2008) were performed to test for phylogenetic correlation 136 201 137 tories of vicariance and dispersal in the same way as plants between isolates from different substrates, continents, and 202 138 and animals (Taylor et al. 2006; Matheny et al. 2009). Although habitats. Substrates were categorized as Pinus, Picea, Nothofa- 203 139 long-distance dispersal events may be rare, it is the best ex- gus, unknown conifer, and unknown hardwood. Continents 204 140 planation for the present day distribution of many fungal were categorised according to geography and habitat catego- 205 141 taxa (Hibbett 2001; James et al. 2001; Zervakis et al. 2004; rized as indoor or outdoor. 206 142 Hosaka et al. 2008; Moncalvo & Buchanan 2008). For some 207 143 fungi, the natural biogeographical patterns may be blurred 208 144 by modern spread by man (Brasier & Buck 2001; Coetzee Results and discussion 209 145 210 et al. 2001; Slippers et al. 2001; Kauserud et al. 2007b). 146 211 In the dry rot fungus Serpula lacrymans that is closely related In Fig 1, a multi-locus phylogeny of the 67 analysed isolates of 147 212 148 to S. himantioides, there seems to have happened a specializa- Serpula himantioides is shown, demonstrating that the isolates 213 149 tion towards growing in buildings (Kauserud et al. 2007b). group into five different lineages with high support. A high 214 150 Serpula himantioides is also known as a common destroyer of congruence in topology was observed across the four investi- 215 151 wooden constructions, but whether any adaptations towards gated DNA regions when these were analysed separately 216 152 this growing habit have happened in any of the S. himantioides (Supplementary Information, Fig S1AeC). The five lineages 217 153 lineages is not clear. were named PS1ePS5 corresponding to phylogenetic species 218 154 In this study, a broader sample of S. himantioides is included under the phylogenetic species recognition definition (Taylor 219 155 compared to Kauserud et al. (2006), including newly obtained et al. 2000; Kroken & Taylor 2001, 2009). This, together with 220 156 221 isolates from Asia and both of the American continents. The earlier mating experiments that has shown that there are 157 222 aims of this study were to (1) analyse whether even more phy- compatible matings within the lineages PS3, PS4, and PS5 158 223 logenetic species can be found within S. himantioides, (2) check but incompatible across lineages (Harmsen 1960; Kauserud 159 224 e 160 whether a biogeographical structure of various S. himantioides et al. 2006), indicate that PS1 PS5 represent different biologi- 225 161 lineages can be observed, and (3) analyse whether any sub- cal species. As there is only one sample in PS2, and no exper- 226 162 strate specialization has happened during the diversification imental crosses could be performed, it may be premature to 227 163 of the S. himantioides species complex. To illuminate these conclude with certainty that this is a distinct species. But as 228 164 topics, the isolates where analysed by multi-locus sequencing the genetic divergence between PS2 and PS3 is comparable 229 165 of three independent DNA regions. to the divergence to the other phylogenetic species within 230 166 S. himantioides, we will treat it as a separate entity here. 231 167 A recent dated molecular phylogeny of the family Serpula- 232 168 233 Material and methods ceae has dated the oldest divergence of the cryptic lineages of 169 234 S. himantioides to approx. 12 million years ago (Engh et al. in 170 235 171 The material included in this study is listed in Table 1. Com- prep). A similar time estimate was made for the split between 236 172 pared to Kauserud et al. (2006), 40 new isolates of Serpula Serpula lacrymans var. lacrymans and Serpula lacrymans var. 237 173 himantioides were included in this study. DNA was extracted shastensis that are still able to mate in vitro (Harmsen 1960). 238 174 from the new cultures following a 2 % CTAB (cetyltrimethy- Lineage PS1 is sister to the other lineages and includes five 239 175 lammonium bromide) miniprep method described by South American isolates. PS2, PS3, and PS4 include mainly 240 176 Murray & Thompson (1980) with minor modifications: DNA North American isolates. However, the sample size here is 241 177 m 242 was resuspended in 100 L distilled sterile H2O at the final too small to conclude that the lineages are mainly restricted 178 step of extraction. The four DNA markers ITS, LSU, hsp and to this continent. PS5 is a widely distributed lineage that has 243 179 244 tub, were PCR amplified and sequenced as outlined in been detected on all continents except for South America 180 245 Kauserud et al.
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    MOLECULAR ANALYSIS OF THE DRY ROT FUNGUS Serpula lacrymans♦ Anne Vigrow B.Sc., P.G.C.E. This thesis is presented to the Council for National Academic Awards in partial fulfilment of the requirements for the award of the degree of Doctor of Philosophy. Department of Molecular and Life Sciences, Dundee Institute of Technology. September, 1992. I certify that this thesis is the true and accurate version of the thesisvapproved by the examiners. S i g n e d D a t e i e s ) Sarah, John and I wish to dedicate this thesis to P e t e r . 1971 - 1985. Acknowledgements. I would like to express my gratitude to my supervisors Professor Bernard King and Drs David Button and John Palfreyman for their encouragement, supervision and guidance throughout this project and for constructive criticism of this manuscript. I hope that completion of this work is adequate recompense for the debt which I undoubtedly owe them, the last named in particular, for having faith in my scientific abilities at a time when I had neither faith nor ability. I am grateful to Professor W. Emond for enabling me to have a year's secondment in order to complete this work; and I also wish to thank my external advisor, Dr. J.A. Carey of the Building Research Establishment, for her advice. Other members of staff at DIT who deserve thanks are Mr. George Hunter and Mr. Charles Craig, for the preparation of photographs; Miss Margot Dunnachie, for the maps and drawings; and Miss Moira Malcolm and the operations' staff of the computer centre, who guided me in the use of Massll.