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Vector Affinity and Diversity of Geosmithia Fungi Living on Subcortical Insects Inhabiting Pinaceae Species in Central and Northeastern Europe

  • Invertebrate Microbiology
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Abstract

Fungi from the genus Geosmithia (Ascomycota: Hypocreales) are associated with bark beetles (Coleoptera: Scolytinae), though little is known about ecology, diversity, and distribution of these fungi across beetle and its host tree species. This study surveyed the diversity, distribution and vector affinity of Geosmithia isolated from subcortical insects that colonized trees from the family Pinaceae in Central and Northeastern Europe. Twelve Geosmithia species were isolated from 85 plant samples associated with 23 subcortical insect species (including 14 bark beetle species). Geosmithia community composition was similar across different localities and vector species; although the fungal communities associated with insects that colonized Pinus differed from that colonizing other tree species (Abies, Larix, and Picea). Ten Geosmithia species from four independent phylogenetic lineages were not reported previously from vectors feeding on other plant families and seem to be restricted to the vectors from Pinaceae only. We conclude that presence of such substrate specificity suggests a long and stable association between Geosmithia and bark beetles.

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References

  1. Kirisits T (2004) Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In: Lieutier F (ed) Bark and wood boring insects in living trees in Europe, a synthesis. Kluwer Academic Publishers, Dordrecht, pp 181–235

    Chapter  Google Scholar 

  2. Beaver RA (1989) Insect-fungus relationships in the bark and ambrosia beetles. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic, London, pp 121–143

    Chapter  Google Scholar 

  3. Six DL (2003) Bark beetle-fungus symbiosis. In: Bourtzis K, Miller TA (eds) Insect symbiosis. CRC Press, Baton Rouge, pp 99–116

    Google Scholar 

  4. Hofstetter RW, Cronin JT, Klepzig KD, Moser JC, Ayres MP (2006) Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle. Oecologia 147:679–691

    Article  PubMed  Google Scholar 

  5. Batra LR (1967) Ambrosia fungi: a taxonomic revision, and nutritional studies of some species. Mycologia 59:976–1017

    Article  Google Scholar 

  6. Harrington TC (2005) Ecology and evolution of mycetophagous bark beetles and their fungal partners. In: Vega FE, Blackwell M (eds) Insect-fungal association, ecology and evolution. Oxford University Press, New York, pp 257–291

    Google Scholar 

  7. Ayres PM, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E (2000) Nitrogen budget of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81:2198–2210

    Article  Google Scholar 

  8. Bleiker KP, Six DL (2007) Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics. Environ Entomol 36:1384–1396

    Article  CAS  PubMed  Google Scholar 

  9. Klepzig KD, Moser JC, Lombardero FJ, Hofstetter RW, Ayres MP (2001) Review article. Symbiosis and competition: complex interactions among beetles, fungi and mites. Symbiosis 30:83–96

    Google Scholar 

  10. Davis TS, Hofstetter RW, Foster JT, Foote NE, Keim P (2011) Interactions between the yeast Ogataea pini and filamentous fungi associated with the western pine beetle. Microb Ecol 61:626–634

    Article  PubMed  Google Scholar 

  11. Six DL, Wingfield MJ (2011) The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annu Rev Entomol 56:255–272

    Article  CAS  PubMed  Google Scholar 

  12. Lieutier F, Yart A, Salle A (2009) Stimulation of tree defenses by ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann For Sci 66:801–822

    Article  Google Scholar 

  13. Brasier CM (1991) Ophiostoma novo-ulmi sp. nov., causative agent of current Dutch elm disease pandemics. Mycopathol 115:151–161

    Article  Google Scholar 

  14. Kirschner R (2001) Diversity of filamentous fungi in bark beetle galleries in Central Europe. In: Misra JK, Horn BW (eds) In trichomycetes and other fungal groups: professor Robert W. Lichtwardt commemoration volume. Science Publishers, Enfield, pp 175–196

    Google Scholar 

  15. Kolařík M, Kubátová A, Hulcr J, Pažoutová S (2008) Geosmithia fungi are highly diverse and consistent bark beetle associates: evidence from their community structure in temperate Europe. Microb Ecol 55:65–80

    Article  PubMed  Google Scholar 

  16. Kolařík M, Kirkendall LR (2010) Evidence for a new lineage of primary ambrosia fungi in geosmithia pitt (ascomycota: hypocreales). Fungal Biol 114:676–689

    Article  PubMed  Google Scholar 

  17. Kolařík M, Freeland E, Utley C, Tisserat N (2011) Geosmithia morbida sp. nov., a new phytopathogenic species living in symbiosis with the walnut twig beetle (Pityophthorus juglandis) on Juglans in USA. Mycologia 103:325–332

    Article  PubMed  Google Scholar 

  18. Kolařík M, Kubátová A, Pažoutová S, Šrůtka P (2004) Morphological and molecular characterisation of Geosmithia putterillii, G. pallida comb. nov. and G. flava sp. nov., associated with subcorticolous insects. Mycol Res 108:1053–1069

    Article  PubMed  Google Scholar 

  19. Kolařík M, Kubátová A, Čepička I, Pažoutová S, Šrůtka P (2005) A complex of three new white-spored, sympatric, and host range limited Geosmithia species. Mycol Res 109:1323–1336

    Article  PubMed  Google Scholar 

  20. Kolařík M, Kostovčík M, Pažoutová S (2007) Host range and diversity of the genus Geosmithia (Ascomycota: Hypocreales) living in association with bark beetles in the Mediterranean area. Mycol Res 111:1298–1310

    Article  PubMed  Google Scholar 

  21. Pitt JI, Hocking AD (2009) Fungi and food spoilage, 3rd edn. Springer, Dordrecht

    Book  Google Scholar 

  22. Sakalidis ML, Hardy GES, Burgess TI (2011) Endophytes as potential pathogens of the baobab species Adansonia gregorii: a focus on the Botryosphaeriaceae. Fungal Ecol 4:1–14

    Article  Google Scholar 

  23. Tisserat N, Cranshaw W, Leatherman D, Utley C, Alexander K (2009) Black walnut mortality in Colorado caused by the walnut twig beetle and Thousand cankers disease. Plant Health Prog:11 August 2009

  24. Kubátová A, Kolařík M, Prášil K, Novotný D (2004) Bark beetles and their galleries: well-known niche for little known fungi, case of Geosmithia. Czech Mycol 55

  25. Linnakoski R, de Beer ZW, Rousi M, Niemelä P, Pappinen A, Wingfield MJ (2008) Fungi, including Ophiostoma karelicum sp. nov., associated with Scolytus ratzeburgi infesting birch in Finland and Russia. Mycol Res 112:1475–1488

    Article  PubMed  Google Scholar 

  26. Jankowiak R, Rossa R (2008) Associations between Pityogenes bidentatus and fungi in young managed Scots pine stands in Poland. For Pathol 38:169–177

    Article  Google Scholar 

  27. Jankowiak R, Kot M (2011) Ophiostomatoid fungi associated with bark beetles (Coleoptera: Scolytidae) colonizing branches of Pinus sylvestris in southern Poland. Pol Bot J 56:287–293

    Google Scholar 

  28. Jankowiak R, Kolařík M (2010) Fungi associated with the fir bark beetle Cryphalus piceae in Poland. For Pathol 40:133–144

    Article  Google Scholar 

  29. Jankowiak R, Rossa R, Mista K (2007) Survey of fungal species vectored by Ips cembrae to European larch trees in Raciborskie forests (Poland). Czech Mycol 59:227

    Google Scholar 

  30. Wright E (1938) Further investigations of brown-staining fungi associated with engraver beetles (Scolytus) in white fir. J Agric Res 57:759–773

    Google Scholar 

  31. Kirschner R (1998) Diversität mit Borkenkäfern assoziierter filamentöser Mikropilze. Disertation, Eberhard-Karls Universität, Tübingen

  32. Jankowiak R, Kurek M (2006) The early stages of fungal succession in Pinus sylvestris phloem and sapwood infested by Tomicus piniperda. Dendrobiology 56:27–36

    Google Scholar 

  33. Jankowiak R (2006) Mycobiota associated with Hylurgops palliatus (Gyll.) on Pinus sylvestris L. in Poland. Acta Soc Bot Pol 75:333–338

    Article  Google Scholar 

  34. Jankowiak R, Bilański P (2007) Fungal flora associated with Tomicus piniperda L. in an area close to a timber yard in southern Poland. J Appl Entomol 131:579–584

    Article  Google Scholar 

  35. Jankowiak R, Hilszczański J (2005) Ophiostomatoid fungi associated with Ips typographus (L.) on Picea abies [(L.) H. Karst.] and Pinus sylvestris L. in north-eastern Poland. Acta Soc Bot Pol 74:345–350

    Article  Google Scholar 

  36. Jankowiak R (2005) Fungi associated with Ips typographus on Picea abies in southern Poland and their succession into the phloem and sapwood of beetle-infested trees and logs. For Pathol 35:37–55

    Article  Google Scholar 

  37. Persson Y, Vasaitis R, Långström B, Öhrn P, Ihrmark K, Stenlid J (2009) Fungi vectored by the bark beetle Ips typographus following hibernation under the bark of standing trees and in the forest litter. Microb Ecol 58:651–659

    Article  PubMed  Google Scholar 

  38. Jankowiak R (2008) Fungi associated with Tomicus minor on Pinus sylvestris in Poland and their succession into the sapwood of beetle-infested windblown trees. Can J For Res 38:2579–2588

    Article  Google Scholar 

  39. Jankowiak R, Rossa R (2007) Filamentous fungi associated with Monochamus galloprovincialis and Acanthocinus aedilis (Coleoptera: Cerambycidae) in Scots pine. Pol Bot J 52:140–143

    Google Scholar 

  40. Jankowiak R, Kacprzyk M, Młynarczyk M (2009) Diversity of ophiostomatoid fungi associated with bark beetles (Coleoptera: Scolytidae) colonizing branches of Norway spruce (Picea abies) in southern Poland. Biologia (Bratisl) 64:1170–1177

    Article  Google Scholar 

  41. Pitt JI (1979) The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic, London

    Google Scholar 

  42. Gardes M, Bruns D (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  44. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330

    PubMed Central  CAS  PubMed  Google Scholar 

  45. O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116

    Article  PubMed  Google Scholar 

  46. Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556

    Article  CAS  Google Scholar 

  47. Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808

    Article  CAS  PubMed  Google Scholar 

  48. Hulcr J, Kolarik M, Kirkendall LR (2007) A new record of fungus-beetle symbiosis in Scolytodes bark beetles (Scolytinae, Curculionidae, Coleoptera). Symbiosis 43:151–159

    Google Scholar 

  49. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RAxML web-servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  51. Miller MA, Pfeiffer W, Schwartz T (2010) The CIPRES portal for inference of phylogenetic trees In: Proceedings of the gateway computing environments workshop (GCE), New Orleans, LA, 14 Nov. 2010, pp. 1–8

  52. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

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

  54. Rambaut A, Drummond AJ (2007) Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer

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

    Article  CAS  Google Scholar 

  56. Roe AD, James PMA, Rice AV, Cooke JEK, Sperling FAH (2011) Spatial community structure of mountain pine beetle fungal symbionts across a latitudinal gradient. Microb Ecol 62:347–360

    Article  PubMed Central  PubMed  Google Scholar 

  57. Hofstetter RW, Dempsey TD, Klepzig KD, Ayres MP (2007) Temperature-dependent effects on mutualistic, antagonistic, and commensalistic interactions among insects, fungi and mites. Community Ecol 8:47–56

    Article  Google Scholar 

  58. Christiansen E, Glosli AM (1996) Mild drought enhances the resistance of Norway spruce to a bark beetle-transmitted blue-stain fungus. US Dep Agric For Serv Gen Tech Rep NC-183, pp. 192–199

  59. Six DL, Bentz BJ (2007) Temperature determines symbiont abundance in a multipartite bark beetle-fungus ectosymbiosis. Microb Ecol 54:112–118

    Article  CAS  PubMed  Google Scholar 

  60. Jankowiak R, Kolarik M (2010) Diversity and pathogenicity of ophiostomatoid fungi associated with Tetropium species (Coleoptera: Cerambycidae) colonizing Picea abies in Poland. Folia Microbiol 55:145–154

    Article  CAS  Google Scholar 

  61. Adams AS, Currie CR, Cardoza Y, Klepzig KD, Raffa KF (2009) Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can J For Res 39:1133–1147

    Article  CAS  Google Scholar 

  62. ter Braak CJF, Šmilauer P (2002) Canoco reference manual and CanoDraw for Windows user’s guide. Software for Canonical community ordination (version 4.5) Microcomputer Power, Ithaca, NY, USA

  63. Postner M (1974) Scolytidae (=ipidae), borkenkaäfer. In: Schwenke W (ed) Die forstschaädlinge Europas, II Käfer, vol 2. Verlag Paul Parey, Hamburg, pp 334–482

    Google Scholar 

  64. Foit J (2010) Distribution of early-arriving saproxylic beetles on standing dead Scots pine trees. Agric For Entomol 12:133–141

    Article  Google Scholar 

  65. Ellenberg HH, Strutt GK (1988) Vegetation ecology of Central Europe. Cambridge University Press, Cambridge

    Google Scholar 

  66. Linnakoski R, De Beer ZW, Ahtiainen J, Sidorov E, Niemelä P, Pappinen A, Wingfield MJ (2010) Ophiostoma spp. associated with pine- and spruce-infesting bark beetles in Finland and Russia. Persoonia 25:72–93

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Nkuekam GK, Solheim H, De Beer ZW, Grobbelaar JW, Jacobs K, Wingfield MJ, Roux J (2010) Ophiostoma species, including Ophiostoma borealis sp. nov., infecting wounds of native broad-leaved trees in Norway. Cryptogam Mycol 31:285–303

    Google Scholar 

  68. Higgins KL, Arnold AE, Miadlikowska J, Sarvate SD, Lutzoni F (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogen Evol 42:543–555

    Article  CAS  Google Scholar 

  69. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  70. Sieber T (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89

    Article  Google Scholar 

  71. Kelley ST, Farrell BD (1998) Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolytidae). Evolution:1731–1743

  72. Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011–2027

    Article  CAS  PubMed  Google Scholar 

  73. Schwenke W (1974) Die forstschaädlinge Europas, II Käfer, vol 2. Die forstschaädlinge Europas, II Käfer. Verlag Paul Parey, Hamburg

    Google Scholar 

  74. Pfeffer A (1995) Zentral-und westpaläarktische Borken-und Kernkäfer (Coleoptera: Scolytidae, Platypodidae), vol 17. Entomologica Basiliensa. Pro Entomologica, Naturhistorisches Museum Basel, Basel

    Google Scholar 

  75. Wood SL (1982) The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin Nat Mem 6:1–1359

    Google Scholar 

  76. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206

    Article  CAS  PubMed  Google Scholar 

  77. Pitt JI (1979) Geosmithia gen. nov. for Penicillium lavendulum and related species. Can J Bot 57:2021–2030

    Article  Google Scholar 

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Acknowledgments

We are grateful to Miloš Knížek, Petr Šrůtka, and Kateřina Nováková for bark beetle identification and to Wilhelm de Beer for bringing to our attention the S. anomala papers and for valuable comments on the final manuscript. We thanks to anonymous reviewers for helpful comments and suggestions. This work was supported by the grants GACR P506/11/2302 and N N309 049037.

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Correspondence to Miroslav Kolařík.

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Overview of the distribution and host affinity of Geosmithia spp. based on our and published data. (DOCX 18 kb)

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Kolařík, M., Jankowiak, R. Vector Affinity and Diversity of Geosmithia Fungi Living on Subcortical Insects Inhabiting Pinaceae Species in Central and Northeastern Europe. Microb Ecol 66, 682–700 (2013). https://doi.org/10.1007/s00248-013-0228-x

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