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The Mycosphere as a Hotspot for the Biotransformation of Contaminants in Soil

  • Lukas Y. Wick
  • Hauke Harms
Reference work entry
First Online:
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

In order to cope with heterogeneous environments mycelial fungi have developed a unique network-based growth form. Unlike bacteria, hyphae efficiently spread in heterogeneous habitats such as soil, penetrate air-water interfaces and cross over air-filled pores. Here we discuss the prevalent role of the mycosphere (i.e., the microhabitat that surrounds fungal hyphae and mycelia) as a hotspot for the degradation of organic contaminants. We highlight the impact of hyphal networks on the transport of chemicals and bacteria and discuss its effects on contaminant availability and degradation. Given the ubiquity and length of hyphae, we propose that the mycosphere is a hotspot for contaminant transformation and attenuation in soil.

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Notes

Acknowledgements

This work contributes to the research topic Chemicals in the Environment (CITE) within the research program Terrestrial Environment of the Helmholtz Association.

References

  1. Baldrian P (2008) Wood-inhabiting ligninolytic basidiomycetes in soils: ecology and constraints for applicability in bioremediation. Fun Ecol 1:4–12CrossRefGoogle Scholar
  2. Banitz T, Fetzer I, Johst K, Wick LY, Harms H, Frank K (2011a) Assessing biodegradation benefits from dispersal networks. Ecol Model 222:2552–2560CrossRefGoogle Scholar
  3. Banitz T, Wick LY, Fetzer I, Frank K, Harms H, Johst K (2011b) Dispersal networks for enhancing bacterial degradation in heterogeneous environments. Environ Pollut 159:2781–2788CrossRefPubMedGoogle Scholar
  4. Banitz T, Johst K, Wick LY, Schamfuss S, Harms H, Frank K (2013) Highways versus pipelines: contributions of two fungal transport mechanisms to efficient bioremediation. Environ Microbiol Rep 5:211–218CrossRefPubMedGoogle Scholar
  5. Bebber DP, Hynes J, Darrah PR, Boddy L, Fricker MD (2007) Biological solutions to transport network design. Proc R Soc B Biol Sci 274:2307–2315CrossRefGoogle Scholar
  6. Berthold T, Centler F, Hubschmann T, Remer R, Thullner M, Harms H et al (2016) Mycelia as a focal point for horizontal gene transfer among soil bacteria. Sci Rep 6:8CrossRefGoogle Scholar
  7. Boddy L, Wood J, Redman E, Hynes J, Fricker MD (2010) Fungal network responses to grazing. Fungal Genet Biol 47:522–530CrossRefPubMedGoogle Scholar
  8. Bourdel G, Roy-Bolduc A, St-Arnaud M, Hijri M (2016) Concentration of petroleum-hydrocarbon contamination shapes fungal endophytic community structure in plant roots. Front Microbiol 7:11CrossRefGoogle Scholar
  9. Cantrell SA (2017) Fungi in extreme and stressful environments. In: Dighton J, White JF (eds) The fungal community : its organization and role in the ecosystem, 4th revised edn. CRC Press, Boca Raton, pp 459–469Google Scholar
  10. Darrah PR, Tlalka M, Ashford A, Watkinson SC, Fricker MD (2006) The vacuole system is a significant intracellular pathway for longitudinal solute transport in basidiomycete fungi. Eukaryot Cell 5:1111–1125CrossRefPubMedPubMedCentralGoogle Scholar
  11. El Amrani A, Dumas AS, Wick LY, Yergeau E, Berthome R (2015) “Omics” insights into PAH degradation toward improved green remediation biotechnologies. Environ Sci Technol 49:11281–11291CrossRefPubMedGoogle Scholar
  12. Ferrari BC, Zhang CD, Dorst J (2011) Recovering greater fungal diversity from pristine and diesel fuel contaminated sub-Antarctic soil through cultivation using both a high and a low nutrient media approach. Front Microbiol 2:14CrossRefGoogle Scholar
  13. Fester T, Giebler J, Wick LY, Schlosser D, Kastner M (2014) Plant-microbe interactions as drivers of ecosystem functions relevant for the biodegradation of organic contaminants. Curr Opin Biotechnol 27:168–175CrossRefPubMedGoogle Scholar
  14. Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev 75:583–609CrossRefPubMedPubMedCentralGoogle Scholar
  15. Furuno S, Pazolt K, Rabe C, Neu TR, Harms H, Wick LY (2010) Fungal mycelia allow chemotactic dispersal of polycyclic aromatic hydrocarbon-degrading bacteria in water-unsaturated systems. Environ Microbiol 12:1391–1398PubMedGoogle Scholar
  16. Furuno S, Foss S, Wild E, Jones KC, Semple KT, Harms H et al (2012) Mycelia promote active transport and spatial dispersion of polycyclic aromatic hydrocarbons. Environ Sci Technol 46:5463–5470CrossRefPubMedGoogle Scholar
  17. Guhr A, Borken W, Spohn M, Matzner E (2015) Redistribution of soil water by a saprotrophic fungus enhances carbon mineralization. Proc Natl Acad Sci U S A 112:14647–14651CrossRefPubMedPubMedCentralGoogle Scholar
  18. Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192CrossRefPubMedGoogle Scholar
  19. Harms H, Wick LY, Schlosser D (2016) The fungal community in organically polluted systems. In: John Dighton JFW (ed) The fungal community: its organization and role in the ecosystem, 4th edn. RC Press, Boca RatonGoogle Scholar
  20. Heaton L, Obara B, Grau V, Jones N, Nakagaki T, Boddy L et al (2012) Analysis of fungal networks. Fungal Biol Rev 26:12–29CrossRefGoogle Scholar
  21. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefPubMedGoogle Scholar
  22. Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87:871–897CrossRefPubMedGoogle Scholar
  23. Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84CrossRefPubMedGoogle Scholar
  24. Johnston SR, Boddy L, Weightman AJ (2016) Bacteria in decomposing wood and their interactions with wood-decay fungi. FEMS Microbiol Ecol 92:12CrossRefGoogle Scholar
  25. Kendrick B. 2000. The Fifth Kingdom. 3rd edn. Newburyport, MA: Focus PublishingGoogle Scholar
  26. Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY (2005) Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol 39:4640–4646CrossRefPubMedGoogle Scholar
  27. Leveau JHJ, Preston GM (2008) Bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytol 177:859–876CrossRefPubMedGoogle Scholar
  28. Nakagaki T, Kobayashi R, Nishiura Y, Ueda T (2004) Obtaining multiple separate food sources: behavioural intelligence in the Physarum plasmodium. Proc R Soc B Biol Sci 271:2305–2310CrossRefGoogle Scholar
  29. Nazir R, Warmink JA, Boersma H, van Elsas JD (2010) Mechanisms that promote bacterial fitness in fungal-affected soil microhabitats. FEMS Microbiol Ecol 71:169–185CrossRefPubMedGoogle Scholar
  30. Olsson S, Bonfante P, Pawlowska TE (2016) Ecologey and evolution of fungal-bacterial interactions. In: Dighton J, White JF, Oudemans P (eds) The fungal community: its organization and tole in the ecosystem. 4th revised ed. CRC Press, Boca Raton, FL. 2017Google Scholar
  31. Otto S, Bruni EP, Harms H, Wick LY (2016) Catch me if you can: dispersal and foraging of Bdellovibrio bacteriovorus 109J along mycelia. ISME J 11:386CrossRefPubMedPubMedCentralGoogle Scholar
  32. Pion M, Bshary R, Bindschedler S, Filippidou S, Wick LY, Job D et al (2013) Gains of bacterial flagellar motility in a fungal world. Appl Environ Microbiol 79:6862–6867CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ritz K, Young IM (2004) Interactions between soil structure and fungi. Mycologist 18:52–59CrossRefGoogle Scholar
  34. Ross IK (1976) Nuclear migration rates in coprinus-congregatus – new record. Mycologia 68:418–422CrossRefGoogle Scholar
  35. Russell JR, Huang J, Anand P, Kucera K, Sandoval AG, Dantzler KW et al (2011) Biodegradation of polyester polyurethane by endophytic fungi. Appl Environ Microbiol 77:6076–6084CrossRefPubMedPubMedCentralGoogle Scholar
  36. Schamfuss S, Neu TR, van der Meer JR, Tecon R, Harms H, Wick LY (2013) Impact of mycelia on the accessibility of fluorene to PAH-degrading bacteria. Environ Sci Technol 47:6908–6915CrossRefPubMedGoogle Scholar
  37. Stefani FOP, Bell TH, Marchand C, de la Providencia IE, El Yassimi A, St-Arnaud M et al (2015) Culture-dependent and -independent methods capture different microbial community fractions in hydrocarbon-contaminated soils. PLoS One 10:16Google Scholar
  38. Suelmann R, Sievers N, Fischer R (1997) Nuclear traffic in fungal hyphae: in vivo study of nuclear migration and positioning in Aspergillus nidulans. Mol Microbiol 25:757–769CrossRefPubMedGoogle Scholar
  39. Taylor DL, Sinsabaugh RL (2015) The soil fungi: occurrence, phylogeny and ecology. In: Paul EA (ed) Soil microbiology, ecology and biochemistry. Elsevier, Amsterdam, pp 77–109CrossRefGoogle Scholar
  40. Tero A, Takagi S, Saigusa T, Ito K, Bebber DP, Fricker MD et al (2010) Rules for biologically inspired adaptive network design. Science 327:439–442CrossRefPubMedGoogle Scholar
  41. Torneman N, Yang XH, Baath E, Bengtsson G (2008) Spatial covariation of microbial community composition and polycyclic aromatic hydrocarbon concentration in a creosote-polluted soil. Environ Toxicol Chem 27:1039–1046CrossRefPubMedGoogle Scholar
  42. Ul Haq I, Zhang MZ, Yang P, van Elsas JD (2014) The interactions of bacteria with fungi in soil: emerging concepts. In: Sariaslani S, Gadd GM (eds) Advances in applied microbiology, vol 89. Elsevier/Academic, San Diego, pp 185–215Google Scholar
  43. Ullrich R, Hofrichter M (2007) Enzymatic hydroxylation of aromatic compounds. Cell Mol Life Sci 64:271–293CrossRefPubMedGoogle Scholar
  44. Verdin A, Sahraoui ALH, Newsam R, Robinson G, Durand R (2005) Polycyclic aromatic hydrocarbons storage by Fusarium solani in intracellular lipid vesicles. Environ Pollut 133:283–291CrossRefPubMedGoogle Scholar
  45. Warmink JA, van Elsas JD (2008) Selection of bacterial populations in the mycosphere of Laccaria proxima: is type III secretion involved? ISME J 2:887–900CrossRefPubMedGoogle Scholar
  46. Warmink JA, van Elsas JD (2009) Migratory response of soil bacteria to Lyophyllum sp strain Karsten in soil microcosms. Appl Environ Microbiol 75:2820–2830CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wessels JGH (1997) Hydrophobins: proteins that change the nature of the fungal surface. In: Poole RK (ed) Advances in microbial physiology, vol 38. Academic/Elsevier, London, pp 1–45Google Scholar
  48. Worrich A, Konig S, Miltner A, Banitz T, Centler F, Frank K et al (2016) Mycelium-like networks increase bacterial dispersal, growth, and biodegradation in a model ecosystem at various water potentials. Appl Environ Microbiol 82:2902–2908CrossRefPubMedPubMedCentralGoogle Scholar
  49. Worrich A, Stryhanyuk H, Musat N, König S, Banitz T, Centler F, Frank K, Thullner M, Harms H, Richnow HH, Miltner A, Kästner M, Wick LY (2017) Mycelium-mediated transfer of water and nutrients stimulates bacterial activity in dry and oligotrophic environments. Nat. Commun. 8:15472CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wosten HAB, van Wetter MA, Lugones LG, van der Mei HC, Busscher HJ, Wessels JGH (1999) How a fungus escapes the water to grow into the air. Curr Biol 9:85–88CrossRefPubMedGoogle Scholar
  51. Zhang MZ, Silva M, Maryam CD, van Elsas JD (2014) The mycosphere constitutes an arena for horizontal gene transfer with strong evolutionary implications for bacterial-fungal interactions. FEMS Microbiol Ecol 89:516–526CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Environmental MicrobiologyHelmholtz Centre for Environmental Research – UFZLeipzigGermany

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