Advertisement

Microbial Ecology

, Volume 76, Issue 3, pp 762–770 | Cite as

Links Between Heathland Fungal Biomass Mineralization, Melanization, and Hydrophobicity

  • Mathias Lenaers
  • Wouter Reyns
  • Jan Czech
  • Robert Carleer
  • Indranil Basak
  • Wim Deferme
  • Patrycja Krupinska
  • Talha Yildiz
  • Sherilyn Saro
  • Tony Remans
  • Jaco Vangronsveld
  • Frederik De Laender
  • Francois Rineau
Soil Microbiology

Abstract

Comprehending the decomposition process is crucial for our understanding of the mechanisms of carbon (C) sequestration in soils. The decomposition of plant biomass has been extensively studied. It revealed that extrinsic biomass properties that restrict its access to decomposers influence decomposition more than intrinsic ones that are only related to its chemical structure. Fungal biomass has been much less investigated, even though it contributes to a large extent to soil organic matter, and is characterized by specific biochemical properties. In this study, we investigated the extent to which decomposition of heathland fungal biomass was affected by its hydrophobicity (extrinsic property) and melanin content (intrinsic property). We hypothesized that, as for plant biomass, hydrophobicity would have a greater impact on decomposition than melanin content. Mineralization was determined as the mineralization of soil organic carbon (SOC) into CO2 by headspace GC/MS after inoculation by a heathland soil microbial community. Results show that decomposition was not affected by hydrophobicity, but was negatively correlated with melanin content. We argue that it may indicate that either melanin content is both an intrinsic and extrinsic property, or that some soil decomposers evolved the ability to use surfactants to access to hydrophobic biomass. In the latter case, biomass hydrophobicity should not be considered as a crucial extrinsic factor. We also explored the ecology of decomposition, melanin content, and hydrophobicity, among heathland soil fungal guilds. Ascomycete black yeasts had the highest melanin content, and hyaline Basidiomycete yeasts the lowest. Hydrophobicity was an all-or-nothing trait, with most isolates being hydrophobic.

Keywords

Decomposition Fungal biomass Heathland Hydrophobicity Melanin 

Notes

Acknowledgements

The authors are thankful to the BOF (Special Research Fund) from Hasselt University for financing their research, as well as METHUZALEM provided to Jaco Vangronsveld under grant number 08M03VGRJ.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1167_MOESM1_ESM.docx (211 kb)
ESM 1 (DOCX 211 kb)

References

  1. 1.
    Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science (New York, NY) 304(5677):1623–1627CrossRefGoogle Scholar
  2. 2.
    Prentice IC, Farquhar GD, Fasham MJR, Goulden ML, Heimann M, Jaramillo VJ, Kheshgi HS, LeQuéré C, Scholes RJ, Wallace DWR (2001) The carbon cycle and atmospheric carbon dioxide. In: Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (eds) Climate Change 2001: the scientific basis. Contributions of working group I to the third assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 185–237Google Scholar
  3. 3.
    Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DA (2011) Persistence of soil organic matter as an ecosystem property. Nature 478(7367):49–56CrossRefPubMedGoogle Scholar
  4. 4.
    Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA, Ceulemans R, Polle A, Velthorst EJ, Scarascia-Mugnozza G, De Angelis P (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281(1–2):15–24CrossRefGoogle Scholar
  5. 5.
    Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233(2):167–177CrossRefGoogle Scholar
  6. 6.
    Cairney JW (2012) Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biol Biochem 47:198–208CrossRefGoogle Scholar
  7. 7.
    Ekblad A, Wallander H, Godbold D, Cruz C, Johnson D, Baldrian P, Björk R, Epron D, Kieliszewska-Rokicka B, Kjøller R (2013) The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil 366(1–2):1–27CrossRefGoogle Scholar
  8. 8.
    Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7(8):740–754CrossRefGoogle Scholar
  9. 9.
    Klein DA, McLendon T, Paschke M, Redente E (1995) Saprophytic fungal-bacterial biomass variations in successional communities of a semi-arid steppe ecosystem. Biol Fertil Soils 19(2–3):253–256CrossRefGoogle Scholar
  10. 10.
    Watkinson S, Bebber D, Darrah P, Fricker M, Tlalka M, Boddy L (2006) The role of wood decay fungi in the carbon and nitrogen dynamics of the forest floor. Fungi in Biogeochemical Cycles (British Mycological Society symposia; No. 24). Cambridge University Press, Cambridge, p 469Google Scholar
  11. 11.
    Holtkamp R, Kardol P, van der Wal A, Dekker SC, van der Putten WH, de Ruiter PC (2008) Soil food web structure during ecosystem development after land abandonment. Appl Soil Ecol 39(1):23–34CrossRefGoogle Scholar
  12. 12.
    Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205(4):1525–1536CrossRefPubMedGoogle Scholar
  13. 13.
    Butler M, Day A (1998) Fungal melanins: a review. Can J Microbiol 44(12):1115–1136CrossRefGoogle Scholar
  14. 14.
    Fernandez CW, Langley JA, Chapman S, McCormack ML, Koide RT (2016) The decomposition of ectomycorrhizal fungal necromass. Soil Biol Biochem 93:38–49CrossRefGoogle Scholar
  15. 15.
    Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Chang Biol 15(4):808–824CrossRefGoogle Scholar
  16. 16.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118CrossRefPubMedGoogle Scholar
  17. 17.
    Chau HW, Si BC, Goh YK, Vujanovic V (2009) A novel method for identifying hydrophobicity on fungal surfaces. Mycol Res 113(10):1046–1052CrossRefPubMedGoogle Scholar
  18. 18.
    Stalder AF, Melchior T, Müller M, Sage D, Blu T, Unser M (2010) Low-bond axisymmetric drop shape analysis for surface tension and contact angle measurements of sessile drops. Colloids Surf A Physicochem Eng Asp 364(1):72–81CrossRefGoogle Scholar
  19. 19.
    Gadd G, Griffiths A (1980) Effect of copper on morphology of Aureobasidium pullulans. Trans Br Mycol Soc 74(2):387–392CrossRefGoogle Scholar
  20. 20.
    McDowell WH, Zsolnay A, Aitkenhead-Peterson JA, Gregorich E, Jones DL, Jödemann D, Kalbitz K, Marschner B, Schwesig D (2006) A comparison of methods to determine the biodegradable dissolved organic carbon from different terrestrial sources. Soil Biol Biochem 38(7):1933–1942CrossRefGoogle Scholar
  21. 21.
    Fernandez CW, Koide RT (2014) Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biol Biochem 77:150–157CrossRefGoogle Scholar
  22. 22.
    R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
  23. 23.
    Rillig MC, Caldwell BA, Wösten HA, Sollins P (2007) Role of proteins in soil carbon and nitrogen storage: controls on persistence. Biogeochemistry 85(1):25–44CrossRefGoogle Scholar
  24. 24.
    Kersten P, Cullen D (2007) Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Fungal Genet Biol 44(2):77–87CrossRefPubMedGoogle Scholar
  25. 25.
    Ray R, Desai J (1984) Effect of melanin on enzymatic hydrolysis of cellulosic waste. Biotechnol Bioeng 26(7):699–701CrossRefPubMedGoogle Scholar
  26. 26.
    Ron EZ, Rosenberg E (2001) Natural roles of biosurfactants. Environ Microbiol 3(4):229–236CrossRefPubMedGoogle Scholar
  27. 27.
    Unestam T, Sun Y-P (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5(5):301–311CrossRefGoogle Scholar
  28. 28.
    Loidi J, Biurrun I, Campos JA, García-Mijangos I, Herrera M (2010) A biogeographical analysis of the European Atlantic lowland heathlands. J Veg Sci 21(5):832–842CrossRefGoogle Scholar
  29. 29.
    Smits TH, Wick LY, Harms H, Keel C (2003) Characterization of the surface hydrophobicity of filamentous fungi. Environ Microbiol 5(2):85–91CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Mathias Lenaers
    • 1
  • Wouter Reyns
    • 1
    • 2
  • Jan Czech
    • 3
  • Robert Carleer
    • 3
  • Indranil Basak
    • 4
  • Wim Deferme
    • 4
  • Patrycja Krupinska
    • 5
  • Talha Yildiz
    • 5
  • Sherilyn Saro
    • 5
  • Tony Remans
    • 5
  • Jaco Vangronsveld
    • 1
  • Frederik De Laender
    • 2
  • Francois Rineau
    • 1
  1. 1.Centre for Environmental Sciences, Research Group Environmental BiologyHasselt UniversityDiepenbeekBelgium
  2. 2.Research Unit in Environmental and Evolutionary BiologyUniversity of NamurNamurBelgium
  3. 3.Centre for Environmental Sciences, Research Group of Applied and Analytical ChemistryHasselt UniversityDiepenbeekBelgium
  4. 4.Institute for Materials Research IMO-IMOMECHasselt UniversityDiepenbeekBelgium
  5. 5.PXLDiepenbeekBelgium

Personalised recommendations