Skip to main content
SpringerLink
Log in

Interactions Between the Yeast Ogataea pini and Filamentous Fungi Associated with the Western Pine Beetle

  • Fungal Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Ecologically important microbes other than filamentous fungi can be housed within the fungal-transport structures (mycangia) of Dendroctonus bark beetles. The yeast Ogataea pini (Saccharomycetales: Saccharomycetaceae) was isolated from the mycangia of western pine beetle (Dendroctonus brevicomis) populations in northern Arizona (USA) with a frequency of 56%. We performed a series of in vitro assays to test whether volatile organic compounds produced by O. pini affected radial growth rates of mutualistic and antagonistic species of filamentous fungi that are commonly found in association with the beetle including Entomocorticium sp. B, Ophiostoma minus, Beauvaria bassiana, and an Aspergillus sp. We determined the compounds O. pini produced when grown on 2% malt extract agar using a gas chromatography/mass spectrometry (GC/MS) analysis of headspace volatiles. Volatiles produced by O. pini on artificial media significantly enhanced the growth of the mutualistic Entomocorticium sp. B, and inhibited growth of the entomopathogenic fungus B. bassiana. GC/MS revealed that O. pini produced ethanol, carbon disulfide (CS2), and Δ-3-carene in headspace. The results of these studies implicate O. pini as an important component in D. brevicomis community ecology, and we introduce multiple hypotheses for future tests of the effects of yeasts in the symbiont assemblages associated with Dendroctonus bark beetles.

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

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic Local Alignment Search Tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  3. Barras S, Perry T (1972) Fungal symbionts in the prothoracic mycangium of Dendroctonus frontalis (Coleopt.: Scolytidae). Z Angew Entomologie 71:95–104

    Article  Google Scholar 

  4. Barras SJ, Perry T (1971) Gland cells and fungi associated with prothoracic mycangium of Dendroctonus adjunctus (Coleoptera-Scolytidae). Ann Entomol Soc Am 64:123–126

    Google Scholar 

  5. 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  PubMed  CAS  Google Scholar 

  6. Bridges JR (1983) Mycangial fungi of Dendroctonus frontalis (Coleoptera, Scolytidae) and their relationship to beetle population trends. Environ Entomol 12:858–861

    Google Scholar 

  7. Bruce A, Stewart D, Verrall S, Wheatley RE (2003) Effect of volatiles from bacteria and yeast on the growth and pigmentation of sapstain fungi. Int Biodeter Biodegradation 51:101–108

    Article  CAS  Google Scholar 

  8. Byers JA (1989) Chemical ecology of bark beetles. Experientia 45:271–283

    Article  CAS  Google Scholar 

  9. Cardoza YJ, Vasanthakumar A, Suazo A, Raffa KF (2009) Survey and phylogenetic analysis of culturable microbes in the oral secretions of three bark beetle species. Entomol Exp Appl 131:138–147

    Article  Google Scholar 

  10. Chatonnet P, Dubourdieu D, Jn B, Lavigne V (1993) Synthesis of volatile phenols by Saccharomyces cerevisiae in wines. J Sci Food Agric 62:191–202

    Article  CAS  Google Scholar 

  11. Coppedge BR, Stephen FM, Felton GW (1995) Variation in female southern pine beetle size and lipid content in relation to fungal associates. Can Entomol 127:145–154

    Article  Google Scholar 

  12. Davis TS, Hofstetter RW, Klepzig KD, Foster JT, Keim P (2010) Interactions between multiple fungi isolated from two bark beetles, Dendroctonus brevicomis and D. frontalis (Coleoptera: Curculionidae). J Yeast Fungal Res 1:118–126

    Google Scholar 

  13. 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

    PubMed  CAS  Google Scholar 

  14. Fatzinger CW, Siegfried BD, Wilkinson RC, Nation JL (1987) Trans-verbenol, turpentine, and ethanol as trap baits for the black turpentine beetle, Dendroctonus terebrans, and other forest Coleoptera in north Florida. J Entomol Sci 22:201–209

    CAS  Google Scholar 

  15. Galef BG, Mason JR, Preti G, Bean NJ (1988) Carbon disulfide: a semiochemical mediating socially-induced diet choice in rats. Physiol Behav 42:119–124

    Article  PubMed  CAS  Google Scholar 

  16. Ganter PF (2006) Yeast and invertebrate associations. In: Rosa C, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer, New York, pp 303–370

    Chapter  Google Scholar 

  17. Gorton C, Webber JF (2000) Reevaluation of the status of the bluestain fungus and bark beetle associate Ophiostoma minus. Mycologia 92:1071–1079

    Article  Google Scholar 

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

    Google Scholar 

  19. Heed BW, Kircher HW (1965) Unique sterol in the ecology and nutrition of Drosophila pachea. Science 149:758–761

    Article  PubMed  CAS  Google Scholar 

  20. Heed WB, Starmer WT, Miranda M, Miller MW, Phaff HJ (1976) Analysis of the yeast flora associated with cactiphilic Drosophila and their host plants in the Sonoran desert and its relation to temperate and tropical associations. Ecology 57:151–160

    Article  Google Scholar 

  21. 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 

  22. Hofstetter RW, Mahfouz JB, Klepzig KD, Ayres MP (2005) Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. J Chem Ecol 31:539–560

    Article  PubMed  CAS  Google Scholar 

  23. Hsiau OT (1996) The taxonomy and phylogeny of the mycangial fungi from Dendroctonus brevicomis and Dendroctonus frontalis (Coleoptera: Scolytidae). Ph.D. thesis, Iowa State University, City.

  24. Hunt DWA, Borden JH (1990) Conversion of verbenols to verbenone by yeasts isolated from Dendroctonus ponderosae (Coleoptera, Scolytidae). J Chem Ecol 16:1385–1397

    Article  CAS  Google Scholar 

  25. Klepzig KD, Wilkens RT (1997) Competitive interactions among symbiotic fungi of the southern pine beetle. Appl Environ Microb 63:621–627

    CAS  Google Scholar 

  26. Klimetzek D, Kohler J, Vite JP, Kohnle U (1986) Dosage response to ethanol mediates host selection by secondary bark beetles. Naturwissenschaften 73:270–272

    Article  CAS  Google Scholar 

  27. Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Leeuwenhoek 73:331–371

    Article  PubMed  CAS  Google Scholar 

  28. Lorenzo MG, Manrique G, Pires HHR, Sanchez MGD, Diotaiuti L, Lazzari CR (1999) Yeast culture volatiles as attractants for Rhodnius prolixus: electroantennogram responses and captures in yeast-baited traps. Acta Trop 72:119–124

    Article  PubMed  CAS  Google Scholar 

  29. Mankowski ME, Morrell JJ (2004) Yeasts associated with the infrabuccal pocket and colonies of the carpenter ant Camponotus vicinus. Mycologia 96:226–231

    Article  PubMed  CAS  Google Scholar 

  30. Nasir H, Noda H (2003) Yeast-like symbiotes as a sterol source in anobiid beetles (Coleoptera, Anobiidae): possible metabolic pathways from fungal sterols to 7-dehydrocholesterol. Arch Insect Biochem 52:175–182

    Article  CAS  Google Scholar 

  31. Nout MJR, Bartelt RJ (1998) Attraction of a flying nitidulid (Carpophilus humeralis) to volatiles produced by yeasts grown on sweet corn and a corn-based medium. J Chem Ecol 24:1217–1239

    Article  CAS  Google Scholar 

  32. Paine TD, Birch MC (1983) Acquisition and maintenance of mycangial fungi by Dendroctonus brevicomis Leconte (Coleoptera, Scolytidae). Environ Entomol 12:1384–1386

    Google Scholar 

  33. Paine TD, Hanlon CC (1994) Influence of oleoresin constituents from Pinus ponderosa and Pinus jeffreyi on growth of mycangial fungi from Dendroctonus ponderosae and Dendroctonus jeffreyi. J Chem Ecol 20:2551–2563

    Article  CAS  Google Scholar 

  34. Phaff HJ, Starmer WT (1987) Yeasts associated with plants, insects, and soil. In: Rose AH, Harrison JS (eds) The Yeasts. Academic Press, New York, pp 123–180

    Google Scholar 

  35. Raffa KF, Smalley EB (1995) Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle fungal complexes. Oecologia 102:285–295

    Article  Google Scholar 

  36. Rivera FN, Gómez Z, González E, López N, Hernández Rodríguez CsH, Zúñiga G (2007) Yeasts associated with bark beetles of the genus Dendroctonus Erichson (Coleoptera: Curculionidae: Scolytinae): molecular identification and biochemical characterization. In: Proceedings from the Third Workshop on Genetics of Bark Beetles and Associated Microorganisms, Fort Collins, CO

  37. Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR (2008) Bacterial protection of beetle-fungus mutualism. Science 322:63–63

    Article  PubMed  CAS  Google Scholar 

  38. Shifrine M, Phaff HJ (1956) The association of yeasts with certain bark beetles. Mycologia 48:41–55

    Article  Google Scholar 

  39. Shihata AMEA, Mrak EM (1952) Intestinal yeast floras of successive populations of Drosophila. Evolution 6:325–332

    Article  Google Scholar 

  40. Six DL (2003) Bark beetle—fungus symbiosis. In: Bourtzis K, Miller TA (eds) Insect Symbioses, vol 3. CRC Press, Boca Raton, pp 97–110

    Chapter  Google Scholar 

  41. Six DL, Klepzig KD (2004) Dendroctonus bark beetles as model systems for studies on symbiosis. Symbiosis 37:207–232

    Google Scholar 

  42. Tanyeli E, Sevim A, Demirbag Z, Eroglu M, Demir I (2010) Isolation and virulence of entomopathogenic fungi against the great spruce bark beetle, Dendroctonus micans (Kugelann) (Coleoptera: Scolytidae). Biocontrol Sci Techn 20:695–701

    Article  Google Scholar 

  43. Vega FE, Dowd PF (2005) The role of yeasts as insect endosymbionts. In: Vega FE, Blackwell M (eds) Insect-Fungal Associations: Ecology and Evolution. Oxford University Press, New York, pp 211–243

    Google Scholar 

  44. 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, San Diego, CA, pp 315–322

    Google Scholar 

  45. Whitney HS (1982) Relationships between bark beetles and symbiotic organisms. In: Mitton JB, Sturgeon KB (eds) Bark beetles in North American conifers: a system for the study of evolutionary biology. University of Texas Press, Austin, TX, pp 183–211

    Google Scholar 

  46. Whitney HS, Cobb FW (1972) Non-Staining fungi associated with bark beetle Dendroctonus brevicomis (Coleoptera-Scolytidae) on Pinus ponderosa. Can J Bot 50:1943–1945

    Article  Google Scholar 

  47. Wood SL (1982) The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin Nat Mem 6:129–203

    Google Scholar 

  48. Zhang L, Clarke SR, Sun J (2009) Electrophysiological and behavioral responses of Dendroctonus valens (Coleoptera: Curculionidae: Scolytinae) to four bark beetle pheromones. Environ Entomol 38:472–477

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the NSF IGERT Program at NAU and the ARCS Foundation, Inc. (Phoenix, AZ) for providing funding that contributed to the completion of this work. Partial funding and work space was provided by the US Forest Service, Rocky Mountain Research Station (05-JV-11221615-104 and 08-JV-11221633-250). We thank Brandy Francis for assistance with DNA extractions and sequencing. We also thank C. Currie, W. Murray, and J. Hulcr for insights that improved the quality of this work, and Marilee Sellers for SEM imaging at the NAU Imaging and Histology Core Facility. The authors thank Impact Analytical for providing the technical expertise and laboratory support needed to perform the GC/MS analysis. Finally, we would like to acknowledge Kyria Boundy-Mills for clarifying yeast taxonomy.

Author information

Authors and Affiliations

  1. School of Forestry, Southwest Forest Science Complex (82), Northern Arizona University, PO Box 15018, 200 E Pine Knoll Dr, Flagstaff, AZ, 86001, USA

    Thomas S. Davis, Richard W. Hofstetter & Nathaniel E. Foote

  2. The Microbial Genomics and Genetics Center, Northern Arizona University, PO Box 4073, Flagstaff, AZ, 86001, USA

    Jeffrey T. Foster & Paul Keim

Authors
  1. Thomas S. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard W. Hofstetter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey T. Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nathaniel E. Foote
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paul Keim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas S. Davis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davis, T.S., Hofstetter, R.W., Foster, J.T. et al. Interactions Between the Yeast Ogataea pini and Filamentous Fungi Associated with the Western Pine Beetle. Microb Ecol 61, 626–634 (2011). https://doi.org/10.1007/s00248-010-9773-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-010-9773-8

Keywords

Search

Navigation