2.8 The fungal phylogeny

A global phylogeny of fungi is emerging from the ‘Assembling the Fungal Tree of Life’ (AFTOL) project funded by the U.S. National Science Foundation (visit: http://www.aftol.org/).

Resources Box

Research-level phylogenetic classification of fungi

The November/December 2006 issue of the journal Mycologia published 24 papers that together provide an initial synthesis of a working phylogenetic classification of fungi emerging from the AFTOL project.

CLICK HERE to visit a page providing details of these.

This international consortium of 71 researchers recently produced a new tree of life for Kingdom Fungi by using data from six gene regions: 18S rRNA, 28S rRNA, 5.8S rRNA, elongation factor-1 (EF1), and two RNA polymerase II subunits (RPB1 and RPB2). They combined data for all six genes (a total number of 6,436 aligned nucleotides) for 199 fungi (James et al., 2006). This obviously results in an enormous cladogram which we can’t reproduce here, but a highly simplified evolutionary tree is shown in Fig. 10 below.

The main branches of the tree of life for Kingdom Fungi
Fig. 10. The main branches of the tree of life for Kingdom Fungi, derived from combined data for six genes (a total number of 6,436 aligned nucleotides) of 199 fungi (James et al., 2006). All the traditional phyla are represented: Ascomycota, Basidiomycota, Glomeromycota, Zygomycota and Chytridiomycota (see discussion in text). Ascomycota and Basidiomycota are united as the Dikarya, fungi in which at least part of the life cycle is characterised by cells with paired nuclei. The closest relatives of these two sister goups are the Glomeromycota. Neither the Zygomycota nor the Chytridiomycota are monophyletic groups; they have representatives in different clades or branches of the tree that are grouped into those phyla by their shared primitive morphologies (such groups are called paraphyletic). Note the microsporidia and Rozella branches, which come out as basal to all other fungi in this analysis. Redrawn after Bruns (2006).

Significantly, this extensive analysis generally supports the more traditional arrangement into: Ascomycota, Basidiomycota, Glomeromycota, Zygomycota and Chytridiomycota, but it then goes on to add new detail to that traditional structure. Ascomycota and Basidiomycota are united as the Dikarya, fungi in which at least part of the life cycle is characterised by cells with paired nuclei. The closest relatives of these two sister groups are the Glomeromycota (which was for a long time included as the Glomales within the Zygomycota). Neither the Zygomycota nor the Chytridiomycota are monophyletic groups; they have representatives in different clades or branches of the tree that are grouped into those phyla by their shared primitive morphologies (such groups are called paraphyletic). This is why in the latest classification (see Chapter 3) the Chytridiomycota is redefined and the Zygomycota is demoted from rank as a formal taxon and becomes an informal name, at least for the time being.

Note the microsporidia and Rozella branches in Fig. 10, which come out as basal to all other fungi in this analysis. Rozella, a genus of chytrid that is parasitic on other Chytridiomycota, seems to be one of the most primitive fungi. Microsporidia, which are parasites of animals, seem to be derived from an endoparasitic chytrid ancestor similar to Rozella, on the earliest diverging branch of the fungal phylogenetic tree.

The fungi, animals and plants are the only three eukaryotic kingdoms of life that developed multicellular tissues in terrestrial environments. They are thought to have diverged from each other roughly one billion years ago. This study continues to support the view that the ancestors of fungi were simple aquatic cells with flagellated spores, similar to current chytrids. What it changes is the idea that there was a single loss of the chytrid flagellum as terrestrial fungi diversified. Rather, the study argues for at least four independent losses of the flagellum during early evolution of Kingdom Fungi, coinciding with the evolution of new mechanisms of spore dispersal.

Estimating the historical time of appearance of the major fungal groups remains a major problem; a study that includes 6 genes in 199 species is a monumental achievement, but it only scratches the surface. A significant contributing point to the problem is that fungi have been so successful in the billion years or so of their existence.

Today’s fungal kingdom is arguably the most abundant and diverse group of organisms on Earth. Fungi are found in every terrestrial ecosystem as mutualist partners, pathogens, parasites, or saprotrophs. It is estimated that the kingdom contains 1.5 million species (Hawksworth, 2001), but only about 5% of these have been described. If most of the unknowns are members of the traditional taxa, then current phylogenetic inferences will be unchallenged by additional discoveries.  However, novel fungal groups could be awaiting discovery by DNA-based environmental sampling, which is already starting to reveal microscopic, undescribed, and unculturable fungi. Because unknowns are unknowns, we can't predict how such discoveries might affect our understanding of fungal origins and evolution. A quotation we’d like to associate with this summary is: ‘...evidence accumulates to support the long-held view that the history of fungi is not marked by change and extinctions but by conservatism and continuity...’ (Pyrozynski, 1976). In other words, fungal evolution is based on the principle: if it works...don't fix it. Our current understanding of the broad sweep of fungal evolution is summarised in the next Resources Box.

Resources Box

A summary of fungal evolution

The phylogenetic tree that you can download from this resource summarises current ideas about the broad sweep of fungal evolution, and puts it into context by showing some markers of geological time and animal and plant evolutionary features.

CLICK HERE to visit this resource page.

An interesting development in the first few years of the 21st century has been the growing trend to suggest that the first terrestrial eukaryotes might have been fungal. A few titles will illustrate this, and we’ll leave you to read the original papers for greater detail. ‘Terrestrial life – fungal from the start?’ (Blackwell, 2000); ‘Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a Tree of Genomes revisited’ (Martin et al., 2003); and ‘Devonian landscape heterogeneity recorded by a giant fungus’ (Boyce et al., 2007).

Finally, to illustrate the ancient importance of fungi, and maybe suggest something that accounts for their success throughout geological time we offer a few quotations, which relate to the Permian-Triassic (P-Tr) extinction event that occurred approximately 251 million years ago. This, informally known as the Great Dying, was the Earth's most severe extinction event (so far!), with about 96% of all marine species and 70% of terrestrial vertebrates becoming extinct.

This catastrophic ecological crisis was triggered by the effects of severe changes in atmospheric chemistry arising from the largest volcanic eruption in the past 500 million years of Earth’s geological history, which formed what are now known as the Siberian Traps flood basalts. When first formed these are thought to have covered an area the size of present-day Australia. Plants suffered massive extinctions as well as animals: ‘…excessive dieback of arboreous vegetation, effecting destabilisation and subsequent collapse of terrestrial ecosystems with concomitant loss of standing biomass...’ occurred ‘throughout the world’.

However, the result of all this death and destruction is that ‘…sedimentary organic matter preserved in latest Permian deposits is characterised by unparalleled abundances of fungal remains, irrespective of depositional environment (marine, lacustrine [= lake sediments], fluviatile [=river/stream deposits]), floral provinciality, and climatic zonation.’ The quotations were taken from Visscher et al. (1996).

The Cretaceous-Tertiary (K-T) extinction of 65 million years ago is another one that we all know a little bit about, because it was caused by a meteor collision that caused the Chicxulub crater in Mexico and is blamed for the extinction of the dinosaurs. The K-T boundary is characterised by high concentration of the element iridium, which is rare on Earth but common in space debris, such as asteroids and meteors. Current understanding is that a meteor hit the Earth at the end of the Cretaceous and the iridium-rich layer is the settled world-wide dust cloud produced by the impact. As the Cretaceous is the last geological period in which dinosaur fossils are found, the belief is that the meteor collision at Chicxulub caused the extinction of the dinosaurs. There was also widespread deforestation right at the end of the Cretaceous, which is assumed to be due to post-impact conditions of high humidity (caused by widespread rain), decreased sunlight and cooler global temperatures resulting from increased atmospheric sulfur aerosols and dust.

However, coincident with all this death and destruction of animal and plant life at the K-T boundary there is a massive proliferation of fungal fossils. Vajda & McLoughlin (2004) put it like this: ‘…This fungi-rich interval implies wholesale dieback of photosynthetic vegetation at the K-T boundary in this region. The fungal peak is interpreted to represent a dramatic increase in the available substrates for [saprotrophic] organisms (which are not dependent on photosynthesis) provided by global forest dieback after the Chixculub impact.’

So it is the same story as at the P-Tr extinction boundary: while the rest of the world was dying, the fungi were having a party! But that might not be the full significance of this anecdote, because Casadevall (2005) suggests that the massive increase in the number of fungal spores in the atmosphere of the time caused fungal diseases that ‘…could have contributed to the demise of dinosaurs and the flourishing of mammalian species…’ The impact of fungi on our own origins is as great as their impact on the world habitat.

Updated December 16, 2016