Chapter Three - Stone-Eating Fungi: Mechanisms in Bioweathering and the Potential Role of Laccases in Black Slate Degradation With the Basidiomycete Schizophyllum commune

https://doi.org/10.1016/bs.aambs.2017.01.002Get rights and content

Abstract

Many enzymes, such as laccases, are involved in the saprotrophic lifestyle of fungi and the effects of those may be linked to enhanced bioweathering on stone surfaces. To test this hypothesis, we studied the decomposition of kerogen-enriched lithologies, especially with black slate containing up to 20% of Corg. Indeed, a formation of ditches with attached hyphal material could be observed. To address enzymes involved, proteomics was performed and one group of enzymes, the multicopper oxidase family members of laccases, was specifically investigated. A role in bioweathering of rocks containing high contents of organic carbon in the form of kerogen could be shown using the basidiomycete Schizophyllum commune, a white rot fungus that has been used as a model organism to study the role of filamentous basidiomycete fungi in bioweathering of black slate.

Introduction

Bioweathering of rocks is an important field in geomicrobiology (Burford et al., 2003, Gadd, 2010, Konhauser, 2009). The mechanisms involved, such as hyphal penetration resulting in enhanced biomechanical weathering, or the production and excretion of organic and inorganic acids as well as siderophores leading to enhanced biochemical weathering, can effect different rocks and minerals (Favero-Longo et al., 2009, Hoffland et al., 2004, Sterflinger, 2000). However, other mechanisms involved in bioweathering such as the secretion of enzymes and their contribution to weathering are not fully understood and it is not clear, which enzymes may take part in the degradation process. Within the kingdom of fungi, especially basidiomycetes secrete a broad range of enzymes for the degradation of organic matter. They are able to degrade complex structures such as lignocellulose and can cause white or brown rot in wood (Cragg et al., 2015, Fernández-Fueyo et al., 2016, Sánchez, 2009, Sergentani et al., 2016). Since organic fractions in stones such as black slates are forming supramolecular structures resembling lignin, the investigation of the activities of a white rot fungus seems indicated. Thus, it seems appropriate to address enzymes produced when the fungus is growing in the presence of kerogen-containing rock material. A molecular model organism of this class of basidiomycetes is Schizophyllum commune (Ohm et al., 2010). A prominent enzyme involved in lignin degradation excreted by S. commune is laccase (EC 1.10.3.2). This multicopper oxidase exhibits a broad substrate spectrum and is involved in the oxidative degradation of other substrates beyond lignin. Therefore, laccases may play an active role in the degradation of rocks and minerals.

Section snippets

Bioweathering

Living organisms may induce the erosion, decay, and decomposition of rocks and minerals, a process defined as bioweathering (Burford et al., 2003). Rock-inhabiting organisms such as cyanobacteria, algae, fungi, and lichens are well known for their degradation potential (Dakal & Cameotra, 2012). The different mechanisms by which they attack and decompose different rocks can be roughly classified into biomechanical and biochemical weathering.

The first class of bioweathering organisms uses the

Ecological Significance of Rock-Inhabiting Fungi

The importance of organisms and their degradation potential were described for the attack of rocks by lichens, a mutualistic symbiosis of fungi and algae or cyanobacteria (Sollas, 1880). A role of fungi can also be deduced from their occurrence on a wide range of rocks, including limestone, sandstone, marble, granite, and basalt (Diakumaku et al., 1995, Sterflinger, 2000, Verrecchia, 2000). The microbial colonization of rocks depends on various environmental factors such as water availability,

Genes Involved in Rock Degradation

Two fungal strains isolated from brown coal, one producing Mn-peroxidase and the other one laccases and peroxidases, were shown to secrete oxidative enzymes shortly before the coal started to dissolve (Willmann & Fakoussa, 1997). The addition of coal powder to the growth medium enhanced fungal growth, implicating that nutrients and organic carbon were mobilized from the coal and utilized for fungal metabolism. This demonstrates the role of laccases and peroxidases as microbial enzymes in coal

Multicopper Oxidases in the Environment

White rot fungi are known to secrete high amounts of enzymes including MCOs to degrade lignin. These enzymes are also involved in attacking rocks containing high yields of organic carbon or kerogen (Hoegger, Kilaru, James, Thacker, & Kües, 2006). MCOs, and especially laccases, act unspecifically on a wide variety of substrates and therefore participate in many ecological processes including adsorption of metals, dissolution of existing and formation of new minerals, detoxification of organic

Laccases in Soil and Interaction With Minerals

Soil basidiomycetes, and specifically their laccases, have been shown to play a role in the decomposition of leaf litter and the oxidation and degradation of soil organic matter (Chen et al., 2013, Courty et al., 2009, Luis et al., 2004). In soil, minerals and organic matter exhibit strong binding capacities for immobilizing extracellular enzymes (Zimmerman & Ahn, 2010). In particular, soil iron and aluminum adsorb high amounts of laccase produced by the white rot fungus Trametes versicolor (Wu

Stress Response in Bioweathering

Fungi are well known to inhabit extreme environments such as contaminated sites, deserts, and rocks. Minerals in these rocks can also contain toxic metals which are released during fungal attack. Several studies showed a correlation between an increased extracellular laccase activity and heavy metal stress (Baldrian and Gabriel, 2002, Lorenzo et al., 2006). Since the active center of a laccase contains Cu atoms, it is likely that the addition of Cu ions promotes laccase production. This could

Conclusions

The microarray analysis clearly shows how S. commune responds to black slate and accelerates weathering through changed gene expression. A variety of proteins, including multicopper oxidases, are produced to attack the rock and cause weathering. Molecular mechanisms involved in the production of organic acids or other metabolites exhibiting rock degrading potential were elucidated. To cope with the consequences of black slate degradation such as the release of toxic metals, genes involved in

Acknowledgments

The authors would like to thank Profs. R. Gaupp, U. Lüttge and C. Fischer and Drs. F. Friedrich and H. Pohl. This work was supported by the German Research Foundation through GRK 1257 and JSMC.

References (90)

  • Y. Liu et al.

    Structure and function of SLC4 family transporters

    Frontiers in Physiology

    (2015)
  • M. Lorenzo et al.

    Inhibition of laccase activity from Trametes versicolor by heavy metals and organic compounds

    Chemosphere

    (2005)
  • M. Lorenzo et al.

    Effect of heavy metals on the production of several laccase isoenzymes by Trametes versicolor and on their ability to decolourise dyes

    Chemosphere

    (2006)
  • P. Luis et al.

    Diversity of laccase genes from basidiomycetes in a forest soil

    Soil Biology and Biochemistry

    (2004)
  • R.R. Mendel et al.

    Cell biology of molybdenum

    Biochimica et Biophysica Acta

    (2006)
  • K. Murugesan et al.

    Effect of metal ions on reactive dye decolorization by laccase from Ganoderma lucidum

    Journal of Hazardous Materials

    (2009)
  • P.M. Romão et al.

    Biodeterioration on megalithic monuments. Study of lichens' colonization on Tapadão and Zambujeiro dolmens (southern Portugal)

    International Biodeterioration and Biodegradation

    (1996)
  • C. Sánchez

    Lignocellulosic residues: Biodegradation and bioconversion by fungi

    Biotechnology Advances

    (2009)
  • A.G. Sergentani et al.

    Lignocellulose degradation potential of Basidiomycota from Thrace (NE Greece)

    International Biodeterioration and Biodegradation

    (2016)
  • R.L. Sinsabaugh et al.

    Nitrogen deposition and dissolved organic carbon production in northern temperate forests

    Soil Biology and Biochemistry

    (2004)
  • K. Sterflinger

    Fungi: Their role in deterioration of cultural heritage

    Fungal Biology Reviews

    (2010)
  • T. Warscheid et al.

    Biodeterioration of stone: A review

    International Biodeterioration and Biodegradation

    (2000)
  • M. Wengel et al.

    Degradation of organic matter from black shales and charcoal by the wood-rotting fungus Schizophyllum commune and release of DOC and heavy metals in the aqueous phase

    The Science of the Total Environment

    (2006)
  • G. Willmann et al.

    Extracellular oxidative enzymes of coal-attacking fungi

    Fuel Processing Technology

    (1997)
  • Y. Wu et al.

    Adsorption of Trametes versicolor laccase to soil iron and aluminum minerals: Enzyme activity, kinetics and stability studies

    Colloids and Surfaces B: Biointerfaces

    (2014)
  • Y. Wu et al.

    Potential role of polycyclic aromatic hydrocarbons (PAHs) oxidation by fungal laccase in the remediation of an aged contaminated soil

    Soil Biology and Biochemistry

    (2008)
  • B. Xiao et al.

    Gene transcription response to weathering of K-bearing minerals by Aspergillus fumigatus

    Chemical Geology

    (2012)
  • S.L. Alper

    Molecular physiology and genetics of Na+-independent SLC4 anion exchangers

    Journal of Experimental Biology

    (2009)
  • P. Baldrian

    Interactions of heavy metals with white-rot fungi

    Enzyme and Microbial Technology

    (2003)
  • P. Baldrian

    Fungal laccases − Occurrence and properties

    FEMS Microbiology Reviews

    (2006)
  • P. Baldrian et al.

    Degradation of cellulose by basidiomycetous fungi

    FEMS Microbiology Reviews

    (2008)
  • A.A. Bell et al.

    Biosynthesis and functions of fungal melanins

    Annual Review of Phytopathology

    (1986)
  • G. Brouwers et al.

    Stimulation of Mn2+ oxidation in Leptothrix discophora SS-1 by Cu2+ and sequence analysis of the region flanking the gene encoding putative multicopper oxidase MofA

    Geomicrobiology Journal

    (2000)
  • E.P. Burford et al.

    Fungal involvement in bioweathering and biotransformation of rocks and minerals

    Mineral Magazine

    (2003)
  • X. Chen et al.

    Comparative analysis of basidiomycetous laccase genes in forest soils reveals differences at the cDNA and DNA levels

    Plant and Soil

    (2013)
  • A.J. Clutterbuck

    The genetics of conidiophore pigmentation in Aspergillus nidulans

    Microbiology

    (1990)
  • C. Compagno et al.

    Alterations of the glucose metabolism in a triose phosphate isomerase-negative Saccharomyces cerevisiae mutant

    Yeast

    (2001)
  • P.-E. Courty et al.

    Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor

    New Phytologist

    (2009)
  • T.C. Dakal et al.

    Microbially induced deterioration of architectural heritages: Routes and mechanisms involved

    Environmental Sciences Europe

    (2012)
  • H.L. Ehrlich

    Geomicrobiology: Relative roles of bacteria and fungi as geomicrobial agents

  • E. Fernández-Fueyo et al.

    A secretomic view of woody and nonwoody lignocellulose degradation by Pleurotus ostreatus

    Biotechnology for Biofuels

    (2016)
  • M. Fomina et al.

    Fungal deterioration of barrier concrete used in nuclear waste disposal

    Geomicrobiology Journal

    (2007)
  • G.M. Gadd

    Metals, minerals and microbes: Geomicrobiology and bioremediation

    Microbiology

    (2010)
  • G.M. Gadd

    Geomycology

  • G.M. Gadd et al.

    Biosorption of copper by fungal melanin

    Applied Microbiology and Biotechnology

    (1988)
  • Cited by (16)

    • Assessing the role of lichens in the prevention of dust emission in dryland: Case study at north-eastern Iran

      2021, Aeolian Research
      Citation Excerpt :

      There are some findings in recent years regarding biocrusts role on soil stability and combating degradation (Chock et al., 2019; Rossi et al., 2018; Sepehr et al., 2019; Zhang et al., 2018), but in relation to influences of lichen species on aridisols in desert environments, the studies are limited to the rocky lichens. Previous studies on rocky lichens have examined the effect of this crust on biological weathering, especially an effective role of lichen crusts on bio-weathering of rocks in arid and semi-arid areas (Wierzchos, 1998; Adamo and Violante, 2000; Gadd, 2017; Kirtzel et al., 2017; Zhang et al., 2019). But so far, no study has been done on the effect of soil lichens on dust capture and biodegradation in Iran.

    • Survival of the basidiomycete Schizophyllum commune in soil under hostile environmental conditions in the Chernobyl Exclusion Zone

      2021, Journal of Hazardous Materials
      Citation Excerpt :

      Although a fungus was chosen that is not common in soil, S. commune is still able to survive saprotrophically and therefore exist in organic soil layers. The lignicolous life-style includes laccase formation, which may induce changes even in mineral composition (Kirtzel et al., 2017), and hence bioavailability of radionuclides and other heavy metals (Günther et al., 2014). The reduced bioavailability, in turn, could explain survival even at high levels of metals or radionuclides present in soil (Krauße et al., 2019).

    • Fungal resources: Current utilization, future prospects, and challenges

      2020, New and Future Developments in Microbial Biotechnology and Bioengineering: Recent Advances in Application of Fungi and Fungal Metabolites: Current Aspects
    View all citing articles on Scopus
    View full text