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Nutritional Profile and Ecological Interactions of Yeast Symbionts Associated with North American Spruce Beetle (Dendroctonus rufipennis)

  • Invertebrate Microbiology
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Abstract

To better understand functional ecology of bark beetle-microbial symbioses, we characterized yeast associates of North American spruce beetle (Dendroctous rufipennis Kirby) across populations. Seven yeast species were detected; Wickerhamomyces canadensis (Wickerham) Kurtzman et al. (Sachharomycetales: Saccharomycetaceae) was the most common (74% of isolates) and found in all populations. Isolates of W. canadensis were subsequently tested for competitive interactions with symbiotic (Leptographium abietinum, = Grosmannia abietina) and pathogenic (Beauvaria bassiana) filamentous fungi, and isolates were nutritionally profiled (protein and P content). Exposure to yeast headspace emissions had isolate-dependent effects on colony growth of symbiotic and pathogenic fungi; most isolates of W. canadensis slightly inhibited growth rates of symbiotic (L. abietinum, mean effect: − 4%) and entomopathogenic (B. bassiana, mean effect: − 6%) fungi. However, overall variation was high (range: − 35.4 to + 88.6%) and some yeasts enhanced growth of filamentous fungi whereas others were consistently inhibitory. The volatile 2-phenylethanol was produced by W. canadensis and synthetic 2-phenylethanol reduced growth rates of both L. abietinum and B. bassiana by 36% on average. Mean protein and P content of Wickerhamomyces canadensis cultures were 0.8% and 7.2%, respectively, but isolates varied in nutritional content and protein content was similar to that of host tree phloem. We conclude that W. canadensis is a primary yeast symbiont of D. rufipennis in the Rocky Mountains and emits volatiles that can affect growth of associated microbes. Wickerhamomyces canadensis isolates vary substantially in limiting nutrients (protein and P), but concentrations are less than reported for the symbiotic filamentous fungus L. abietinum.

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Data Availability

Data will be made available for research purposes upon reasonable request to the authors.

References

  1. Adams AS, Six DL, Adams SM, Holben WE (2008) In vitro interactions between yeasts and bacteria and the fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae). Microb Ecol 56:460–466

    Article  PubMed  Google Scholar 

  2. 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 

  3. Adams AS, Aylward FO, Adams SE, Erbilgin N, Aukema BH, Currie CR et al (2013) Mountain pine beetles colonizing historical and naïve host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microb 79:3468–3475

    Article  CAS  Google Scholar 

  4. Aukema BH, Werner RA, Haberkern KE, Illman BL, Clayton MK, Raffa KF (2005) Quantifying sources of variation in the frequency of fungi associated with spruce beetles: implications for hypothesis testing and sampling methodology in bark beetle-symbiont relationships. For Ecol Manag 217:187–202

    Article  Google Scholar 

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

  6. Becher PG, Flick G, Rozpędowska E, Schmidt A, Hagman A, Lebreton S et al (2012) Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct Ecol 26:822–828

    Article  Google Scholar 

  7. Becher PG, Hagman A, Verschut V, Chakraborty A, Rozpędowska E, Lebreton S et al (2018) Chemical signaling and insect attraction is a conserved trait in yeasts. Ecol Evol 8:2962–2974

    Article  PubMed  PubMed Central  Google Scholar 

  8. Bentz BJ, Six DL (2006) Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae). Ann Entomol Soc Am 99:189–194

    Article  CAS  Google Scholar 

  9. 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 

  10. Callaham RZ, Shifrine M (1960) The yeasts associated with bark beetles. For Sci 6:146–154

    Google Scholar 

  11. Davis TS (2015) The ecology of yeasts in the bark beetle holobiont: a century of research revisited. Microb Ecol 69:723–732

    Article  PubMed  Google Scholar 

  12. Davis TS, Boundy-Mills K, Landolt PJ (2012) Volatile emissions from an epiphytic fungus are semiochemicals for eusocial wasps. Microb Ecol 64:1056–1063

    Article  CAS  PubMed  Google Scholar 

  13. Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as insect Semiochemicals. J Chem Ecol 39:840–859

    Article  CAS  PubMed  Google Scholar 

  14. 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 

  15. Davis TS, Horne FB, Yetter JC, Stewart JE (2018) Engelmann spruce chemotypes in Colorado and their effects on symbiotic fungi associated with the North American spruce beetle. J Chem Ecol 44:601–610

  16. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64:409–434

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Eshkol N, Sendovski M, Bahalul M, Katz-Ezov T, Kashi Y, Fishman A (2009) Production of 2-phenylethanol from L-phenylalanine by a stress tolerant Saccharomyces cerevisiae strain. J Appl Microbiol 106:534–542

    Article  CAS  PubMed  Google Scholar 

  19. Etschmann MMW, Sell D, Schrader J (2003) Screening of yeasts for the production of the aroma compound 2-phenylethanol in a molasses-based medium. Biotechnol Lett 25:531–536

    Article  CAS  PubMed  Google Scholar 

  20. Fogleman JC, Foster JL (1989) Microbial colonization of injured cactus tissue (Stenocereus gummosus) and its relationship to the ecology of cactophilic Drosophila mojavensis. Appl Environ Microbiol 55:100–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ganter PF, Starmer WT, Lachance M-A, Phaff HJ (1986) Yeast communities from host plants and associated Drosophila in southern Arizona: new isolations and analysis of the relative importance of hosts and vectors on community composition. Oecologia 70:386–392

    Article  PubMed  Google Scholar 

  22. Ganter PF (2006) Yeast and invertebrate associations. In: Péter G, Rosa C (eds) Biodiversity and Ecophysiology of Yeasts. Springer-Verlag, Berlin, Germany, pp 303–370

    Chapter  Google Scholar 

  23. Grosmann H (1930) Beiträge zur kenntnis der lebensgemeinschaft zwischen borkenkäfern un pilzen. Z f Parasitenkunde 3:56–102

    Article  Google Scholar 

  24. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

  25. Hansen AK, Pers D, Russell JA (2020) Symbiotic solutions to nitrogen limitation and amino acid imbalance in insect diets. Adv Insect Physiol 58:161–205

    Article  Google Scholar 

  26. Heath RR, Manukian A (1992) Development and evaluation of systems to collet volatile semiochemicals from insects and plants using charcoal-infused medium for air purification. J Chem Ecol 18:1209–1226

    Article  CAS  PubMed  Google Scholar 

  27. Herrera CM, Pozo MI, Medrano M (2013) Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94:273–279

    Article  PubMed  Google Scholar 

  28. Hicke JA, Meddens AJH, Kolden CA (2016) Recent tree mortality in the western United States from bark beetles and forest fires. For Sci 62:141–153

    Article  Google Scholar 

  29. Hua SS, Beck JJ, Sarreal SB, Gee W (2014) The major volatile compound 2-phenylethanol from the biocontrol yeast, Pichia anomala, inhibits growth and expression of aflatoxin biosynthetic genes of Aspergillus flavus. Mycotoxin Res 30:71–78

    Article  CAS  PubMed  Google Scholar 

  30. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

  31. Jenkins MJ, Hebertson EG, Munson SA (2014) Spruce beetle biology, ecology and management in the Rocky Mountains: an addendum to Spruce Beetle in the Rockies. Forests 5:21–71

  32. Lahr EC, Krokene P (2013) Conifer stored resources and resistance to a fungus associated with the spruce bark beetle Ips typographus. PLOS ONE 8:e72405

  33. Mann AJ, Davis TS (2020) Plant secondary metabolites and low temperature are the major limiting factors for Beauveria bassiana (Bals.-Criv.) Vuill. (Ascomycota: Hypocreales) growth and virulence in a bark beetle system. Biol Control 141:104310

  34. May CM, Doroszuk A, Zwaan BJ (2015) The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster. Ecol Evol 5:1156–1168

    Article  PubMed  PubMed Central  Google Scholar 

  35. Ott DS, Davis TS, Mercado JE (2021) Interspecific variation in spruce constitutive and induced defenses in response to a bark beetle-fungal symbiont provides insight into traits associated with resistance. Tree Physiol 41:1109–1121

    Article  CAS  PubMed  Google Scholar 

  36. Pisal A (2010) Determination of phosphorous, all forms – molybdate/ascorbic acid method with two reagents – method 365.3. In: Water and Environmental Analysis, LAMBDA XLS UV/V Spectrophotometer operating manual, PerkinElmer. pp. 40–45.

  37. Rozas JJ, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  38. Safranyik L, Shrimpton DM, Whitney HS (1983) The role of host–pest interaction in population dynamics of Dendroctonus rufipennis Kirby (Coleoptera: Scolytidae). In: Isaev AS, ed. IUFRO/ MAB Symposium Proceedings, Host–Pest Interactions, 24–27 August 1981, Irkutsk, USSR. Canadian Forest Service, Victoria, B.C. pp. 1–12.

  39. Sasaki T, Kawamura M, Ishikawa H (1996) Nitrogen recycling in the brown planthopper, Nilaparvata lugens: Involvement of yeast-like endosymbionts in uric acid metabolism. J Insect Physiol 42:125–129

    Article  CAS  Google Scholar 

  40. Scott JJ, Oh D-C, Yuceer MC, Klepzig KD, Clardy J, Currie CR (2008) Bacterial protection of a beetle-fungus mutualism. Science 322:63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Shi Z, Yang Q, Kuga S, Matsumoto Y (2015) Dissolution of wood pulp in aqueous NaoH/urea solution via dilute acid pretreatment. J Agric Food Chem 63:6113–6119

    Article  CAS  PubMed  Google Scholar 

  42. Six DL, Bentz BJ (2003) Fungi associated with the North American spruce beetle, Dendroctonus rufipennis. Can J For Res 33:1815–1820

    Article  Google Scholar 

  43. Six DL, Bracewell R (2015) Dendroctonus. In: Vega FE, Hofstetter RW (eds) Bark Beetles: Biology and Ecology of Native Species. Academic Press, Elsevier, pp 305–350

    Chapter  Google Scholar 

  44. Sobhy IS, Baets D, Goelen T, Herrera-Malaver B, Bosmans L, Van den Ende W et al (2018) Sweet scents: nectar specialist yeasts enhance nectar attraction of a generalist aphid parasitoid without affecting survival. Front Plant Sci 9:1009

    Article  PubMed  PubMed Central  Google Scholar 

  45. Stamps JA, Yang LH, Morales VM, Boundy-Mills KL (2012) Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLOS ONE 7:e42238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Vega FE, Biedermann PHW (2020) On interactions, associations, mycetangia, mutualists and symbiotes in insect-fungus symbioses. Fungal Ecol 44:100909

    Article  Google Scholar 

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Acknowledgements

We express our gratitude to the technicians that contributed to this project including Nathaniel Comai, Fione Horne, and Kristen Otto. We are also grateful to Danielle Malesky (USFS) and Sky Stephens (USFS), who assisted in locating beetle activity and collecting beetles.

Funding

This work was partially supported by funding from NSF Award #2046109 to TS Davis.

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TSD and JES designed the study. TSD collected isolates and performed interaction experiments. JES performed genetic identification of isolates. CVB and CC performed the nutritional analyses. TSD, JES, and CVB analyzed the data. TSD wrote the first draft of the manuscript and all authors contributed to editing the manuscript.

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Correspondence to Thomas S. Davis.

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Davis, T.S., Stewart, J.E., Clark, C. et al. Nutritional Profile and Ecological Interactions of Yeast Symbionts Associated with North American Spruce Beetle (Dendroctonus rufipennis). Microb Ecol 86, 1268–1280 (2023). https://doi.org/10.1007/s00248-022-02158-7

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