Review
Some like it hot, some not – Tropical and arctic mushrooms

https://doi.org/10.1016/j.fbr.2018.04.001Get rights and content

Highlights

  • Characterisation of arctic and tropical rainforest biomes.

  • Traits of arctic and tropical mushrooms.

  • Stress responses.

  • Morphological and physiological adaptations.

  • Modes of dispersal.

  • Pheno- and genotypic plasticity.

Abstract

Fungi are of pivotal importance for terrestrial ecosystems. They occur globally and show extremely high species diversities. In this review, we compiled information about the adaptability of pileate basidiomycetes by illustrating their habits in contrasting biomes, the arctic regions and tropical lowland rainforests. Mushrooms are faced with differing stress factors and levels in the two ecozones. They fight such challenges by using, by and large, similar physiological and morphological toolkits. They make them fit for extreme environmental conditions, by expressing traits according to biome characteristics. This way, fungal assemblages are formed and pheno- and genotypic plasticity is capitalised. Still, many questions remain open and need further clarification, such as trade-offs between thermal protection and predator defence, prevailing dispersal modes in the main ecozones, interactions with animals and the mechanisms that create genetic plasticity.

Introduction

Ectomycorrhizal and saprobic fungi occur in almost all climate belts and are essential drivers of ecosystem processes (Allen, 1991, Cooke and Rayner, 1984). Saprotrophic basidiomycetes are with more than 80,000 species (Hawksworth and Lücking, 2017) eminently important as decomposers and recyclers of organic material (Dighton and Boddy, 1989, Swift, 1982). The ectomycorrhizal guild as a symbiotic group relies with varying specificity on woody plants as hosts for carbon supply (photosynthate). Carbon is traded mainly for nitrogen and phosphorus extracted from soil-borne, predominantly organic sources in (mineral) nitrogen-limited habitats (Smith and Read, 2008). There are estimates that speak of 20,000 ectomycorrhizal species (van der Heijden et al., 2015), of which ca. 60 % are basidiomycetes, the rest mainly ascomycetes (Tedersoo et al., 2010). In this review, we focus on pileate basidiomycetes.

Like any other organismal group, mushrooms are first of all challenged by climate conditions, particularly thermal and hydrological extremes (Gostinčar et al., 2010). In addition, soil properties play a major role in the habitability of environments (Voroney, 2007). Mushrooms need to disperse and reproduce. To reach a suitable substrate or host, mushrooms not only use wind as dispersal agent, but a number of vectors (arthropods, molluscs, mammals and more), or transport by percolating water (Halbwachs and Bässler, 2015). Biome-related conditions may have significant impacts on dispersal and reproductive modes (Lawrey, 1980, Peay and Bruns, 2014). Moreover, disease and predation are likely to show different patterns in different biomes.

These circumstances raise questions about mushroom diversity, abundance and life strategies in distinct biomes. Biotic and abiotic differences imply adaptations and/or marked pheno- and genotypic plasticity, i.e. stress tolerance. To illustrate the complex factors implicated, we are going to look into two extremely contrasting ecozones, tropical lowland rainforests and alpine/boreal/(sub-)arctic tundras, in the following “arctic” for short (Fig. 1).

We will first compare general geographical and ecological characteristics of the two biomes, followed by a description of fungal responses to environmental stress. Finally, we identify knowledge gaps and suggest further lines of research.

Section snippets

Terrae cognitae: general characteristics of tropical and arctic biomes

The extremely different climatic conditions in arctic and tropical ecozones are best illustrated by the climate charts after Walter and Lieth (1967). These diagrammes show the relationship and interplay between seasonal variations of temperature and precipitation. In Fig. 2, two examples from contrasting biomes are shown.

However, there is obviously more to consider than temperature and precipitation when appreciating these biomes. To highlight the diverse environmental conditions for fungal

Latitudinal contrasts: environmental conditions in rainforests of the tropics versus arctic biomes

Here, we assess the impact of each environmental factor on mushrooms as listed above (lettering follows Table 1).

a, b) Excessive temperatures, be they low or high, pose threats to mushrooms as ectothermic organisms. This mainly applies to the cellular level with its intricate metabolism and membrane architecture (Cooke and Whipps, 1993, Jennings, 1993). Are temperatures too low, the chemical, and under extreme conditions (rupture due to ice crystals), the physical integrity of membranes is

Equipped for adverse environmental conditions

Major constraints, basidiomycete mushrooms have to adjust to, are abiotic, though biotic biome characteristics certainly mould assemblages, too. Conspicuous abiotic differences between the two ecozones compared in our review are temperature (air and soil), wind, UV radiation, nutrient availability and seasonality. Precipitation characteristics starkly differ, too, but not humidity regimes (Holdridge, 1967). Important biotic interactions relate to animals as predators and vectors.

The fungal toolbox

We have discussed a number of fungal responses to environmental peculiarities of two starkly contrasting biomes. Still, there are commonalities in the toolbox of mushrooms to cope with extreme environments (Table 2).

Two issues can be observed: Many of the tools and traits expressed by mushrooms (1) serve several purposes, and (2) apply in both biomes we have compared. This tells us something about the impressive versatility of the fungal lifestyle, and about the economy of fungal adaptations.

Conflict of interest

None.

Acknowledgements

We sincerely thank Claus Bässler (Bavarian Forest National Park) and Dominik Begerow (Ruhr University, Bochum) for their helpful feed-backs on the manuscript.

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

References (121)

  • R. Agerer

    Exploration types of ectomycorrhizae

    Mycorrhiza

    (2001)
  • R. Agerer et al.

    DEEMY – an Information System for Characterization and Determination of Ectomycorrhizae

    (2005–2011)
  • M.F. Allen

    The Ecology of Mycorrhizae

    (1991)
  • J.H. Andrews

    Comparative Ecology of Microorganisms and Macroorganisms

    (2017)
  • W. Barthlott et al.

    Geographic patterns of vascular plant diversity at continental to global scales

    Erdkunde

    (2007)
  • C. Bässler et al.

    Mean reproductive traits of fungal assemblages are correlated with resource availability

    Ecol. Evol.

    (2016)
  • C. Bässler et al.

    Effects of resource availability and climate on the diversity of wood-decaying fungi

    J. Ecol.

    (2010)
  • A.A. Bell et al.

    Biosynthesis and functions of fungal melanins

    Annu. Rev. Phytopathol.

    (1986)
  • M. Bjorbaekmo et al.

    High diversity of root associated fungi in both alpine and arctic Dryas octopetala

    BMC Plant Biol.

    (2010)
  • L.O. Björn et al.

    Effects of enhanced UV-B radiation on subarctic vegetation

  • L. Boddy et al.

    Ecology of Saprotrophic Basiodiomycetes

    (2008)
  • L. Boddy et al.

    Wood decay communities in angiosperm wood

  • W.d. Boer et al.

    Enzymes of saprotrophic basidiomycetes

  • V.S. Bondar et al.

    Luminescence of higher mushrooms

    J. Sib. Fed. Univ. Biol.

    (2012)
  • N.C. Brady et al.

    The Nature and Properties of Soils

    (2002)
  • J.H. Brown

    Why are there so many species in the tropics?

    J. Biogeogr.

    (2014)
  • M. Bush et al.

    Fire, climate change and biodiversity in Amazonia: a Late-Holocene perspective

    Phil. Trans. Biol. Sci.

    (2008)
  • T.V. Callaghan et al.

    Arctic Tundra and Polar Desert Ecosystems, Arctic Climate Impact Assessment

    (2005)
  • S. Cantrell

    Fungi in extreme and stressful environments

  • F. Carlsson et al.

    Increased heat resistance in mycelia from wood fungi prevalent in forests characterized by fire: a possible adaptation to forest fire

    Fungal Biol.

    (2012)
  • G. Certini

    Effects of fire on properties of forest soils: a review

    Oecologia

    (2005)
  • S. Chacón et al.

    Observations on the phenology of ten fungal species in the subtropical forests at Xalapa, Mexico

    Mycol. Res.

    (1995)
  • A. Claridge et al.

    Mycophagy by small mammals in the coniferous forests of North America: nutritional value of sporocarps of Rhizopogon vinicolor, a common hypogeous fungus

    J. Comp. Physiol. B Biochem. Syst. Environ. Physiol.

    (1999)
  • R.C. Cooke et al.

    Ecology of Saprotrophic Fungi

    (1984)
  • R.C. Cooke et al.

    Ecophysiology of Fungi

    (1993)
  • R.J.B. Cordero et al.

    Functions of fungal melanin beyond virulence

    Fungal Biol. Rev.

    (2017)
  • R.T. Corlett et al.

    Tropical Rain Forests: an Ecological and Biogeographical Comparison

    (2011)
  • F. Cox et al.

    Not poles apart: Antarctic soil fungal communities show similarities to those of the distant Arctic

    Ecol. Lett.

    (2016)
  • R.M.M. Crawford

    Habitat fragility as an aid to long-term survival in arctic vegetation

  • L.G. Czigány

    The use of hallucinogens and the shamanistic tradition of the Finno-Ugrian people

    Slavonic East Eur. Rev.

    (1980)
  • J. Deacon

    Fungal Biology

    (2006)
  • D.E. Desjardin et al.

    Fungi bioluminescence revisited

    Photochem. Photobiol. Sci.

    (2008)
  • J. Dighton

    Fungi in Ecosystem Processes

    (2016)
  • J. Dighton et al.

    Role of fungi in nitrogen, phosphorus and sulphur cycling in temperate forest ecosystems

  • J.C. Elliott

    Reproduction in Fungi – Genetic and Physiological Aspects

    (1994)
  • M. Fablet et al.

    Evolvability, epigenetics and transposable elements

    Biomol. Concepts

    (2011)
  • FAO

    World Reference Base for Soil Resources 2015, World Soil Resources Reports

    (2015)
  • N. Fierer et al.

    The diversity and biogeography of soil bacterial communities

    Proc. Natl. Acad. Sci. U.S.A.

    (2006)
  • N. Fierer et al.

    Global patterns in belowground communities

    Ecol. Lett.

    (2009)
  • P.V. Fine

    Ecological and evolutionary drivers of geographic variation in species diversity

    Annu. Rev. Ecol. Evol. Systemat.

    (2015)
  • E.A. Fitzpatrick

    Arctic soils and permafrost

  • C.M. Foust et al.

    Population Epigenetics, Nuclear Functions in Plant Transcription, Signaling and Development

    (2015)
  • M. Gardes et al.

    Mycorrhizal diversity in arctic and alpine tundra: an open question

    New Phytol.

    (1996)
  • J. Geml et al.

    An arctic community of symbiotic fungi assembled by long-distance dispersers: phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA

    J. Biogeogr.

    (2012)
  • G.S. Gilbert et al.

    Polypore fungal diversity and host density in a moist tropical forest

    Biodivers. Conserv.

    (2002)
  • C. Gostinčar et al.

    Extremotolerance in fungi: evolution on the edge

    FEMS Microbiol. Ecol.

    (2010)
  • H. Halbwachs et al.

    Gone with the wind – a review on basidiospores of lamellate agarics

    Mycosphere

    (2015)
  • H. Halbwachs et al.

    Hyphae of waxcap fungi colonise plant roots

    Fungal Ecol.

    (2013)
  • H. Halbwachs et al.

    Mean spore size and shape in ectomycorrhizal and saprotrophic assemblages show strong responses under resource constraints

    Fungal Ecol.

    (2017)
  • H. Halbwachs et al.

    Tales and mysteries of fungal fruiting: How morphological and physiological traits affect a pileate lifestyle

    Fungal Biol. Rev.

    (2016)
  • Cited by (10)

    • A geographical traceability method for Lanmaoa asiatica mushrooms from 20 township-level geographical origins by near infrared spectroscopy and ResNet image analysis techniques

      2022, Ecological Informatics
      Citation Excerpt :

      Moreover, the solute will become sticky and the ion levels inside and outside the membrane will be imbalanced, all of which can be the cause of protein inactivation. ( Halbwachs and Simmel, 2018). Therefore, lower temperatures may affect the quality of mushrooms from the aspects of metabolism and the intricate cellular level of membrane structure.

    • Functional traits of stipitate basidiomycetes

      2021, Encyclopedia of Mycology
    • Polysaccharides obtained from natural edible sources and their role in modulating the immune system: Biologically active potential that can be exploited against COVID-19

      2021, Trends in Food Science and Technology
      Citation Excerpt :

      These microorganisms reproduce sexually by the joining of hyphae, however other reproductive forms can also be observed, and for this reason they are considered sexually promiscuous. Mushrooms contain a wide variety of shapes, colors, and sizes, and can also be found in various habitats (Halbwachs & Simmel, 2018). Currently, several species of edible mushrooms are known, and only a part of the known edible mushrooms is commercialized.

    • Occurrence and possible roles of polysaccharides in fungi and their influence on the development of new technologies

      2020, Carbohydrate Polymers
      Citation Excerpt :

      It is worth mentioning that the process of evolution from the type of bipolar to tetrapolar reproduction is linked to relevant changes in the production of polysaccharides by fungi. The evolution of the type of mating forced changes in the entire glycobiology of fungi, leading to considerable changes in the biology, biochemistry, and lifestyle of these organisms (Halbwachs & Simmel, 2018). Studies such as Phadke, Feretzaki, and Heitman (2013), suggest that gradual changes in the type of mating contributed to changes in the morphology of primitive single-celled species for hypha-producing organisms.

    View all citing articles on Scopus
    View full text