Evolution and Phylogeny of Fungi

Fungi have ancient origins, with evidence indicating they likely first appeared
about one billion years ago, though the fossil record of fungi is scanty. Fungal hyphae
evident within the tissues of the oldest plant fossils confirm that fungi are an extremely
ancient group. Indeed, some of the oldest terrestrial plant-like fossils known,
called Prototaxites, which were common in all parts of the world throughout
the Devonian Period (419.2 million to 358.9 million years ago), are interpreted as large
saprotrophic fungi (possibly even Basidiomycota). Fossils of Tortotubus protuberans, a
filamentous fungus, date to the early Silurian Period (440 million years ago) and are
thought to be the oldest known fossils of a terrestrial organism. However, in the absence
of an extensive fossil record, biochemical characters have served as useful markers in
mapping the probable evolutionary relationships of fungi. Fungal groups can be related
by cell wall composition (i.e., presence of both chitin and alpha-1,3 and
alpha-1,6-glucan), organization of tryptophan enzymes, and synthesis of lysine (i.e., by
the aminoadipic acid pathway). Molecular phylogenetic analyses that became possible
during the 1990s have greatly contributed to the understanding of fungal origins and
evolution. At first, these analyses generated evolutionary trees by comparing a single
gene sequence, usually the small subunit ribosomal RNA gene (SSU rRNA). Since then,
information from several protein-coding genes has helped correct discrepancies, and
phylogenetic trees of fungi are currently built using a wide variety of data largely, but not
entirely, molecular in nature.

Kingdom Fungi is a monophyletic group, meaning that all modern fungi can be traced to
a single ancestral organism.
Larry C. Moon/Tom Stack & Associates
Until the latter half of the 20th century, fungi were classified in the plant kingdom
(subkingdom Cryptogamia) and were separated into four classes: Phycomycetes,
Ascomycetes, Basidiomycetes, and Deuteromycetes (the latter also known as Fungi
Imperfecti because they lack a sexual cycle). These traditional groups of fungi were
largely defined by the morphology of sexual organs, by the presence or absence of hyphal
cross walls (septa), and by the degree of chromosome repetition (ploidy) in the nuclei of
vegetative mycelia. The slime molds, all grouped in the subdivision Myxomycotina, were
also included in Division Fungi.

In the middle of the 20th century the three major kingdoms of multicellular eukaryotes,
kingdom Plantae, kingdom Animalia, and kingdom Fungi, were recognized as being
absolutely distinct. The crucial character difference between kingdoms is the mode of
nutrition: animals (whether single-celled or multicellular) engulf food;
plants photosynthesize; and fungi excrete digestive enzymes and absorb externally
digested nutrients. There are other notable differences between the kingdoms. For
example, whereas animal cell membranes contain cholesterol, fungal cell membranes
contain ergosterol and certain other polymers. In addition, whereas plant cell walls
contain cellulose (a glucose polymer), fungal cell walls contain chitin (a glucosamine
polymer). One exception to this rule is a group of fairly ubiquitous microscopic fungi
(referred to as the cryptomycota), members of which average about 3 to 5 μm (1 μm is
about 0.000039 inch) in length, have cell walls lacking chitin, and possess a flagellum.
Phylogenetic analyses of ribosomal RNA in this clade suggest that it is an ancient fungal
group.

Genomic surveys show that plant genomes lack gene sequences that are crucial in animal
development, animal genomes lack gene sequences that are crucial in plant development,
and fungal genomes have none of the sequences that are important in controlling
multicellular development in animals or plants. Such fundamental genetic differences
imply that animals, plants, and fungi are very different cellular organisms. Molecular
analyses indicate that plants, animals, and fungi diverged from one another almost one
billion years ago.

Although fungi are not plants, formal recognition of fungal nomenclature is governed by
the International Code of Botanical Nomenclature. In addition, the taxon “phylum” is
used in fungal nomenclature, having been adopted from animal taxonomy. The
phylogenetic classification of fungi is designed to group fungi on the basis of their
ancestral relationships, also known as their phylogeny. The genes possessed by
organisms in the present day have come to them through the lineage of their ancestors. As
a consequence, finding relationships between those lineages is the only way of
establishing the natural relationships between living organisms. Phylogenetic
relationships can be inferred from a variety of data, traditionally including fossils,
comparative morphology, and biochemistry, although most modern phylogenetic
trees (evolutionary trees, or cladograms) depend on molecular data coupled with these
traditional forms of data.

Kingdom Fungi, one of the oldest and largest groups of living organisms, is a
monophyletic group, meaning that all modern fungi can be traced back to a single
ancestral organism. This ancestral organism diverged from a common ancestor with the
animals about 800 million to 900 million years ago. Today many organisms, particularly
among the phycomycetes and slime molds, are no longer considered to be true fungi,
even though mycologists might study them. This applies to the water molds (e.g., the
plant pathogen Phytophthora, the cause of potato late blight), all of which have been
reclassified within the kingdom Chromista (phylum Oomycota). Similarly, the
Amoebidales, which are parasitic or commensal on living arthropods and were previously
thought to be fungi, are considered to be protozoan animals. None of the slime molds are
placed in kingdom Fungi, and their relationship to other organisms, especially animals,
remains unclear.

Kingdom Fungi has gained several new members on the basis of molecular phylogenetic
analysis, notably Pneumocystis, the Microsporidia, and Hyaloraphidium. Pneumocystis
jirovecii causes pneumonia in mammals, including humans with weakened immune
systems; pneumocystis pneumonia (PCP) is the most common opportunistic infection in
people with human immunodeficiency virus (HIV) and has been a major cause of death
in people with AIDS. Pneumocystis was initially described as a trypanosome, but
evidence from sequence analyses of several genes places it in the fungal subphylum
Taphrinomycotina in the phylum Ascomycota. The Microsporidia were thought to be a
unique phylum of protozoa for many years; however, molecular studies have shown that
these organisms are fungi. The Microsporidia are obligate intracellular parasites of
animals and lack mitochondria. Most infect insects, but they are also responsible for
common diseases of crustaceans and fish and have been found in most other animal
groups, including humans (probably transmitted through contaminated food or
water). Hyaloraphidium curvatum was previously classified as a colourless green alga;
however, it has since been recognized as a fungus on the basis of molecular sequence
data, which show it to be a member of the order Monoblepharidales in the phylum
Chytridiomycota.

Outline of classification of fungi

Since the 1990s, dramatic changes have occurred in the classification of fungi. Improved
understanding of relationships of fungi traditionally placed in the
phyla Chytridiomycota and Zygomycota has resulted in the dissolution of outmoded
taxons and the generation of new taxons. The Chytridiomycota is retained but in a
restricted sense. One of Chytridiomycota’s traditional orders, the Blastocladiales, has
been raised to phylum status as the Blastocladiomycota. Similarly, the group of anaerobic
rumen chytrids, previously known as order Neocallimastigales, has been recognized as a
distinct phylum, the Neocallimastigomycota. The phylum Zygomycota is not accepted in
the phylogenetic classification of fungi because of remaining doubts about relationships
between the groups that have traditionally been placed in this phylum. The consequences
of this decision are the recognition of the phylum Glomeromycota and of four
subphyla incertae sedis (Latin for “of uncertain position”): Mucoromycotina,
Kickxellomycotina, Zoopagomycotina, and Entomophthoromycotina.
The true fungi, which make up the monophyletic clade called kingdom Fungi, comprise
seven Phyla: Chytridiomycota, Blastocladiomycota,
Neocallimastigomycota, Microsporidia, Glomeromycota, Ascomycota,
and Basidiomycota (the latter two being combined in the subkingdom Dikarya). The
group of ancestral fungi is thought to be represented by the present-day Chytridiomycota,
although the Microsporidia may be an equally ancient sister group. The first major steps
in the evolution of higher fungi were the loss of the chytrid flagellum and the
development of branching, aseptate fungal filaments, which occurred as terrestrial fungi
diverged from water moulds 600 million to 800 million years ago. Septate filaments
evolved as the Glomeromycota diverged from a combined clade of pre-basidiomycota
and pre-ascomycota fungi about 500 million years ago. Hyphae with the characteristic
appearance of modern Basidiomycota can be seen in some of the earliest known
specimens of plant fossils. Therefore, Ascomycota and Basidiomycota probably diverged
as so-called sister groups, which are placed together in subkingdom Dikarya, about 300
million years ago. The easily recognizable mushroom fungi probably diversified 130
million to 200 million years ago, soon after flowering plants became an important part of
the flora and well before the age of dinosaurs. A relatively recent evolutionary radiation,
perhaps 60 million to 80 million years ago, of anaerobic Chytridiomycota occurred
as grasses and grazing mammals became more abundant; the chytrid fungi serve as
symbionts within the rumen of such animals, thereby enabling the grazing mammals to
digest grasses.