Skip to main content

Advertisement

Log in

The Fungicide Tebuconazole Confounds Concentrations of Molecular Biomarkers Estimating Fungal Biomass

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Due to their ecological importance, fungi are suitable indicator organisms for anthropogenic stress. To estimate fungal biomass, the fungal membrane molecule ergosterol is often quantified as a proxy. Estimates based on ergosterol may, however, be distorted by exposure to demethylase inhibiting (DMI) fungicides, interfering with sterol synthesis. To test this hypothesis, we exposed ten fungal species to the DMI fungicide tebuconazole and measured concentrations of ergosterol and DNA per unit dry mass of the fungal hyphae. The latter served as alternative biomass proxy that is not specifically targeted by tebuconazole. Effects of tebuconazole on ergosterol concentrations were species-specific, while concentrations were on average reduced by 13%. In contrast, DNA concentrations were on average increased by 13%. We demonstrate that DMI fungicides – at close to field relevant levels – can distort fungal biomass estimation, complicating the use of this endpoint for environmental management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544

    Article  Google Scholar 

  • Bärlocher F (ed) (1992) The ecology of aquatic hyphomycetes. Springer, Berlin, New York

    Google Scholar 

  • Baschien C, Tsui CK-M, Gulis V, Szewzyk U, Marvanová L (2013) The molecular phylogeny of aquatic hyphomycetes with affinity to the Leotiomycetes. Fungal Biol 117:660–672

    Article  Google Scholar 

  • Baudy P, Zubrod JP, Röder N, Baschien C, Feckler A, Schulz R, Bundschuh M (2019) A glance into the black box: novel species-specific quantitative real-time PCR assays to disentangle aquatic hyphomycete community composition. Fungal Ecol 42:100858

    Article  Google Scholar 

  • Bundschuh M, Zubrod JP, Kosol S, Maltby L, Stang C, Duester L, Schulz R (2011) Fungal composition on leaves explains pollutant-mediated indirect effects on amphipod feeding. Aquat Toxicol 104:32–37

    Article  CAS  Google Scholar 

  • Dighton J, White JF (eds) (2017) The fungal community: its organization and role in the ecosystem. CRC Press, Boca Raton

    Google Scholar 

  • Duarte S, Pascoal C, Garabétian F, Cássio F, Charcosset J (2009) Microbial decomposer communities are mainly structured by trophic status in circumneutral and alkaline streams. Appl Environ Microbiol 75:6211–6221

    Article  CAS  Google Scholar 

  • Feckler A, Goedkoop W, Konschak M, Bundschuh R, Kenngott KGJ, Schulz R, Zubrod JP, Bundschuh M (2017) History matters: heterotrophic microbial community structure and function adapt to multiple stressors. Glob Change Biol. https://doi.org/10.1111/gcb.13859

    Article  Google Scholar 

  • Fernández D, Voss K, Bundschuh M, Zubrod JP, Schäfer RB (2015) Effects of fungicides on decomposer communities and litter decomposition in vineyard streams. Sci Total Environ 533:40–48

    Article  Google Scholar 

  • Fungicide Resistance Action Committee (2018) FRAC code list 2018: fungicides sorted by mode of action (including FRAC code numbering)

  • Gessner MO (2005) Ergosterol as a measure of fungal biomass. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 189–195

    Chapter  Google Scholar 

  • Gessner MO, Chauvet E (1993) Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microbiol 59:502–507

    Article  CAS  Google Scholar 

  • Hakala K, Hannukkala AO, Huusela-Veistola E (2011) Pests and diseases in a changing climate a major challenge for Finnish crop production. Agric Food Sci 20:3–14

    Article  Google Scholar 

  • Hvězdová M, Kosubová P, Košíková M, Scherr KE, Šimek Z, Brodský L, Šudoma M, Škulcová L, Sáňka M, Svobodová M, Krkošková L, Vašíčková J, Neuwirthová N, Bielská L, Hofman J (2018) Currently and recently used pesticides in Central European arable soils. Sci Total Environ 613–614:361–370

    Article  Google Scholar 

  • Jones OAH, Voulvoulis N, Lester JN (2006) Partitioning behavior of five pharmaceutical compounds to activated sludge and river sediment. Arch Environ Contam Toxicol 50:297–305

    Article  CAS  Google Scholar 

  • Joseph-Horne T, Hollomon D, Loeffler RST, Kelly SL (1995a) Altered P450 activity associated with direct selection for fungal azole resistance. FEBS Lett 374:174–178

    Article  CAS  Google Scholar 

  • Joseph-Horne T, Carelli A, Hollomon D, Kelly SL (1995b) Investigation of azole resistance in the Ustilago maydis sterol demethylase mutant erg 40. Pestic Sci 44:33–38

    Article  CAS  Google Scholar 

  • Kang Z, Huang L, Krieg U, Mauler-Machnik A, Buchenauer H (2001) Effects of tebuconazole on morphology, structure, cell wall components and trichothecene production of Fusarium culmorum in vitro. Pest Manag Sci 57:491–500

    Article  CAS  Google Scholar 

  • Manerkar MA, Seena S, Bärlocher F (2008) Q-RT-PCR for assessing archaea, bacteria, and fungi during leaf decomposition in a stream. Microb Ecol 56:467–473

    Article  CAS  Google Scholar 

  • Mateu-Vicens G, Khokhlova A, Sebastian-Pastor T (2014) Epiphytic foraminiferal indices as bioindicators in mediterranean seagrass meadows. J Foramin Res 44:325–339

    Article  Google Scholar 

  • Murugan R, Loges R, Taube F, Sradnick A, Joergensen RG (2014) Changes in soil microbial biomass and residual indices as ecological indicators of land use change in temperate permanent grassland. Microb Ecol 67:907–918

    Article  CAS  Google Scholar 

  • Pesce S, Zoghlami O, Margoum C, Artigas J, Chaumot A, Foulquier A (2016) Combined effects of drought and the fungicide tebuconazole on aquatic leaf litter decomposition. Aquat Toxicol 173:120–131

    Article  CAS  Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rabiet M, Margoum C, Gouy V, Carluer N, Coquery M (2010) Assessing pesticide concentrations and fluxes in the stream of a small vineyard catchment Effect of sampling frequency. Environ Pollut 158:737–748

    Article  CAS  Google Scholar 

  • Rajapaksha RMCP, Tobor-Kapłon MA, Bååth E (2004) Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 70:2966–2973

    Article  CAS  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109:6241–6246

    Article  CAS  Google Scholar 

  • Solé M, Fetzer I, Wennrich R, Sridhar KR, Harms H, Krauss G (2008) Aquatic hyphomycete communities as potential bioindicators for assessing anthropogenic stress. Sci Total Environ 389:557–565

    Article  Google Scholar 

  • Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48

    Article  Google Scholar 

  • Zanne AE, Abarenkov K, Afkhami ME, Aguilar-Trigueros CA, Bates S, Bhatnagar JM, Busby PE, Christian N, Cornwell WK, Crowther TW, Flores-Moreno H, Floudas D, Gazis R, Hibbett D, Kennedy P, Lindner DL, Maynard DS, Milo AM, Nilsson RH, Powell J, Schildhauer M, Schilling J, Treseder KK (2020) Fungal functional ecology: bringing a trait-based approach to plant-associated fungi. Biol Rev 95:409–433

    Article  Google Scholar 

  • Zavrel M, Esquivel BD, White TC (2014) The ins and outs of azole antifungal drug resistance: molecular mechanisms of transport. In: Gotte M, Berghuis A, Matlashewski G, Wainberg M, Sheppard D (eds) Handbook of antimicrobial resistance. Springer, New York, pp 1–27

    Google Scholar 

  • Zhang J, Hu S, Xu Q, You H, Zhu F (2018) Baseline sensitivity and control efficacy of propiconazole against Sclerotinia sclerotiorum. Crop Prot 114:208–214

    Article  CAS  Google Scholar 

  • Zubrod JP, Bundschuh M, Feckler A, Englert D, Schulz R (2011) Ecotoxicological impact of the fungicide tebuconazole on an aquatic decomposer-detritivore system. Environ Toxicol Chem 30:2718–2724

    Article  CAS  Google Scholar 

  • Zubrod JP, Englert D, Wolfram J, Wallace D, Schnetzer N, Baudy P, Konschak M, Schulz R, Bundschuh M (2015) Waterborne toxicity and diet-related effects of fungicides in the key leaf shredder Gammarus fossarum (Crustacea: Amphipoda). Aquat Toxicol 169:105–112

    Article  CAS  Google Scholar 

  • Zubrod JP, Bundschuh M, Arts G, Brühl CA, Imfeld G, Knäbel A, Payraudeau S, Rasmussen JJ, Rohr J, Scharmüller A, Smalling K, Stehle S, Schulz R, Schäfer RB (2019) Fungicides: an overlooked pesticide class? Environ Sci Technol 53:3347–3365

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This study was funded by the German Research Foundation, Project AQUA–REG (DFG; SCHU227/14-1). We thank Therese Bürgi, Sebastian Pietz, and Britta Wahl–Ermel for their assistance in the laboratory.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Patrick Baudy or Mirco Bundschuh.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 68 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baudy, P., Konschak, M., Sakpal, H. et al. The Fungicide Tebuconazole Confounds Concentrations of Molecular Biomarkers Estimating Fungal Biomass. Bull Environ Contam Toxicol 105, 620–625 (2020). https://doi.org/10.1007/s00128-020-02977-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-020-02977-9

Keywords

Navigation