2.8 The fungal phylogeny

A global phylogeny of fungi first emerged using data from several gene regions: 18S rRNA, 28S rRNA, 5.8S rRNA, elongation factor-1 (EF1), and RNA polymerase II subunits (RPB1 and RPB2). Data for all these gene regions were combined (a total number of 6,436 aligned nucleotides) for 199 fungi (James et al., 2006), and there have been several more genome level studies since this work was published, many of which were combined by McCarthy & Fitzpatrick (2017). The outcome is an enormous cladogram which we can’t reproduce here, but a highly simplified evolutionary tree is shown in Fig. 10 below.

Significantly, this extensive analysis generally supports the more traditional arrangement into: Ascomycota, Basidiomycota, various zygomycetes and Chytridiomycota, but it obviously adds 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 Glomeromycotina (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, as mentioned above, the ‘Zygomycota’ is demoted from rank as a formal taxon and becomes an informal name, at least for the time being.

Main branches in the fungal tree of life

Fig. 10. The main branches of the tree of life for Kingdom Fungi, as established by the AFTOL project and subsequent publications (referenced in the text). All the traditional phyla are represented: Ascomycota, Basidiomycota, zygomycetes (as Mucoromycota, which includes Glomeromycotina, and Zoopagomycota), and Chytridiomycota (see discussion in the text of this chapter and Chapter 3 for Blastocladiomycota and Neocallimastigomycota). 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 (‘dikaryons’). The closest relatives of these two sister groups are the Glomeromycotina. The multigene phylogeny of fungi established by the AFTOL project placed the Glomeromycotina (using the name Glomeromycota) in a basal position as a sister group of Asco- and Basidiomycota (together called subkingdom Dikarya); this relationship to Dikarya is only slightly changed by the realignment of the group as a subphylum. Although, in formal terms, it is now phylum Mucoromycota that shared a most recent common ancestor with Dikarya, the Glomeromycotina was the first lineage of Mucoromycota to diverge (Spatafora et al., 2016).

Note the microsporidia and Rozella (Cryptomycota) 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, though whole genome analyses are beginning to aid understanding (Reynolds et al., 2017). A significant contribution to the problem is that horizontal gene transfer has been a significant factor in fungal evolution (Richards et al., 2011) and, of course, 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. As we mentioned in Section 1.7 above, it is estimated that the kingdom contains 2.2 to 3.8 million species (Hawksworth & Lücking, 2017), but only about 3 to 8% 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 in 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 was a trend to suggest that the first terrestrial eukaryotes might have been fungal. A few titles will illustrate this: ‘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). For mycologists this was certainly a refreshing development because, prior to this, fungi have always been ignored when theorists pondered the origin and early emergence of life on this planet. The complete version of what we like to call ‘The Mycologists’ Tale’ appeared in the book entitled Fungal Biology in the Origin and Emergence of Life (Moore, 2013).

This book offers a new interpretation (illustrated here in Fig. 11) of the early radiation of eukaryotes based on the emergence of major innovations in cell biology that apply uniquely to present day fungi. These emphasised: increasingly detailed management of the positioning and distribution of membrane-bound compartments (vacuoles, vesicles and microvesicles) by the filamentous components of the cytoskeleton (microfilaments, intermediate filaments and microtubules); culminating, as far as filamentous fungi are concerned, with emergence of the Spitzenkörper and apical hyphal extension. These features of present day fungi are described in detail elsewhere in this book (Chapter 5, Sections 5.10 and 5.11) and we will reference where we describe other features as we mention them.

The mycologist's tree of life

Fig. 11. The mycologist’s tree of life. The lower part of this diagram is based on Cavalier-Smith’s tree of life (Cavalier-Smith, 2010a; his Fig. 6), which emphasises major evolutionary changes in membrane topology and chemistry, except that the most ancient bacteria are shown here to be heterotrophic descendants of LUCA (the last universal common ancestor of all current life on Earth). Eukaryotes diverge from actinobacterial ancestors about 1,500 Mya (million years ago) and the bulk of this illustration deals with eukaryote evolution. The most ancient stem eukaryotes are considered to exhibit characteristics that would today be thought of as applying to primitive fungi. Their evolution emphasises increasingly detailed management of the positioning and distribution of membrane-bound compartments (vacuoles, vesicles and microvesicles) by the filamentous components of the cytoskeleton (microfilaments, intermediate filaments and microtubules); culminating, as far as filamentous fungi are concerned, with emergence of the Spitzenkörper and apical hyphal extension. Uniquely among present day eukaryotes, the fungi maintain their nuclear membrane intact as the nuclear division progresses. The subsequent evolution of Kingdom Fungi is outlined in the Resources Box above.

The interpretation suggests that the last universal common ancestor of all current life on Earth (usually known by the acronym LUCA) was a heterotrophic, mesophilic prokaryote, essentially a ‘bacterial’ cell with the cell enveloped by two distinct lipid bilayer membranes. The earliest prokaryotes used prebiotically synthesised organic carbon compounds as nutrients but, as these supplies diminished, they were outstripped by the anoxygenically photosynthetic Chlorobacteria as the most primitive surviving prokaryotic phylum. This interpretation follows the deep phylogeny of the tree of life published by Cavalier-Smith (2006, 2010a & b), who argued that thermophiles evolved late, making Archaebacteria the youngest bacterial phylum and the sisters, rather than ancestors of eukaryotes (in contrast to the interpretations described in Section 2.4 above), which themselves diverged from actinobacterial ancestors. Eukaryotes are generally thought to have appeared about 1.5 billion years ago, so, for a total of about 2 billion years the only living organisms on the planet were prokaryotes together, presumably, with their associated viruses. CLICK HERE to download the full text PDF of our article entitled 'A fungal root for the eukaryote tree'.

The primitive eukaryotic stem featured primitive nuclear structures (including the nuclear membrane remaining intact as the nuclear division progresses, which is a unique characteristic of present day fungi) (Chapter 5, Section 5.7), added the mitochondrion by enslavement of a bacterium (Chapter 5, Section 5.10); and evolved those aspects of the endomembrane system and cytoskeletal architecture that are also unique characteristics of present day fungi, in the following probable temporal sequence:

This last is a possible branch point from chytrid level fungi to animals (of the sort presently called choanozoa). The animal stem gradually lost its wall and adapted cytoskeletal organisation/vesicle trafficking originally used in wall synthesis to the new function of phagocytosis. Animals also developed disassembly of the nuclear envelope as the division spindle forms; and adopted cholesterol as the predominant sterol for membrane fluidity, as well as equatorially contractile cell division. Ivarsson et al. (2020) also argue, in their ‘alternative view on hyphal development’, that septal formation was an important step in the evolution of multicellularity in fungi, but they place the events ‘in the deep biosphere’. We do not see the necessity of removing the evolution of filamentous hyphae to ‘the deeps’ from surface biofilms and believe that most of the points discussed by Ivarsson et al. could equally well apply to biofilms on rock surfaces (Moore, 2013).

Through this sequence of events filamentous fungi emerged 1.5 billion years ago as the first crown group of eukaryotes. They emerged to exploit the components of the biofilms in which they lived and the debris left by 2 billion years of prokaryote growth, and they’ve been cleaning up the planet ever since (Moore, 2013; and see Halbwachs, 2019b).

Finally, to illustrate the ancient importance of fungi, and maybe suggest something that accounts for their success through the rest of geological time we offer a few quotations, which relate to the Permian-Triassic (P-Tr) extinction event that occurred approximately 251 million years ago. The evolution of life on Earth has been interrupted by several mass extinction events. The P-Tr event, 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 in Siberia about the size of the present continent of 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 was resulted as the world-wide dust cloud produced by the impact settled to the ground. 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 (and see our discussion of patterns of evolution of mushrooms in Section 3.8).

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.

21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

2.8 The fungal phylogeny