The Evolution and Devolution of Hyphae
We are often told that fungi are organisms that are made up of an oddball filamentous cell type known as hyphae. Hyphae are the basis of most fungal life—strands that grow through the soil or other substrate, releasing digestive and binding enzymes, and re-absorbing the resulting nutrients along with water. A mass of hyphae will grow visibly as either undifferentiated mycelium or as a fruiting body with various degrees of tissue differentiation. This indeed describes most fungi, but if one pauses to think of other examples, one might remember that the fungi also include a variety of single-celled yeasts, notably the all-important fermenter Sacchromyces cerevisiae, as well as many other yeast species. And if you’ve studied biology, you might also remember a group of “primitive” fungi known as chytrids, a protozoa-like group existing mainly in the form of motile flagellate zoospores, much analogous to the single-celled flagellate ancestors of animals or single-celled green algal plant ancestors—all simple marine life forms which gave rise to an array of more complex multicellular organisms that colonized the land.
But how did this variation in fungal growth form come to be? The revolution in molecular biology is telling us much about the fungal kingdom, both in terms of molecular phylogenetics revealing the details of the “fungal tree of life”, and genomic and gene expression studies revealing how fungal structures and functions are genetically encoded and how they have evolved.
The overall fungal tree of life shows a general evolutionary pattern that might tell us about the disappearance of flagellate zoospores and the appearance of hyphae. Most phylogenies show the Chytridiomycota or “true” chytrids as the first branch away from all other fungi at the base of the fungal tree, with the next divergence being between another chytrid group, the Blastocladiomycota and the remaining, largely terrestrial fungi, the zygo-, asco-, and basidiomycetes with which we are more familiar.
Most Chytridiomycota lack true hyphae. Such chytrids reproduce either by direct cellular fusion and production of progeny zoospores, or by morphing from zoospore to reproductive sporangium, then reproducing by means of fusion of simple rhizoids that branch off of the sporangium. These rhizoids are not true hyphae in that they do not contain regular nuclei or organelles that would allow more complete cellular function, but rather simply allow the passage and exchange of reproductive nuclei – in some ways analogous to the role of a pollen tube in a flowering plant. Rhizoids, however, may very well be the evolutionary predecessors of regular nucleate hyphae.
At the other extreme are the majority of fungal species, which are mainly hyphal through their life cycle and have lost zoospores entirely. The Blastocladiales, of which the soil fungus Allomyces is perhaps the best known example, seem to be an intermediate step between the two. These fungi are “hyphal chytrids”, alternating between a hyphal phase produced from germinating zoospores, or zygotes from fused zoospores, and the production of new zoospores from sporangia at the terminal ends of their hyphal branches.
This would seem to point to a stepwise pattern of the emergence of vegetative hyphae and the loss of motile zoospores. Ah, but if things were so simple! First, there are also hyphal chytrids within the “true chytrid” clade as well, which would indicate that hyphae may have arisen from rhizoids more than once. A further complication is that, based upon repeated and robust molecular phylogenetic findings, it seems that there is an entirely non-hyphal chytrid, a plant root parasite called Olpidium, whose closest relatives, both ancestrally and in sister groups, are entirely-hyphal species of fungi that more or less fall into in the zygomycete group. (I hesitate to say “line” or “clade”, because it’s unclear at this point whether the zygomycetes form a real group with a single direct common ancestor.)
To make things even more complicated, one recent molecular phylogeny seems to show a group of hyphal chytrids known as the Monoblepheraceae as the earliest branch at the base of the fungal tree of life, an earlier branching than even Chytridiomycota. (I should note that this placement of the Monoblepheraceae is at odds with all other phylogenies of the fungal kingdom found so far—most place this group within the Chytridiomycota.)
Does this indicate that the ancestral state of the fungi was perhaps the “hyphal chytrid” form, with some branches retaining the zoosporic state and losing hyphae, while the great majority of fungal species did the opposite? Perhaps, but as we often say in science, “More data is needed.”
However hyphae originated among the chytrids, we know that 99%+ of fungal species are non-zoosporic and that the emergence of a totally hyphal form was critical to the “advance of the fungi” onto land and into the many niches that fungi occupy. (As was the later emergence of hyphal septa, which allowed a more differentiated and often complex morphology.) But where does that leave single-celled yeasts? Yeasts are in fact widespread in the fungal kingdom—two primary branches of the Ascomycota, the Taphrinomycotina and the better-known Saccharomycotina, consist mostly of yeasts. There are other small groups of yeasts found in many other places in the fungal kingdom, including many fungi with yeast and hyphal stages at different stages of their life cycle.
Phylogeny points to a clear pattern—within the fungal tree of life, yeasts inevitably show a multicellular hyphal ancestor. In fact, sometimes they are very close relatives—Ashbya gossypii is in the same family as the yeast S. cerevisiae and the two share 95% identity between their genomes, yet the former species is entirely hyphal in growth form, without a known yeast stage. Single-celled yeasts are a derived form, a good example of evolution from a complex to a seemingly simpler form.
Research on the growth of hyphae has led to a better understanding of the development of yeasts. Septate hyphae grow by continually elongating at the growing tip, then branching off or laying down septa (cross-walls) downstream. Some alterations of this process will produce yeasts. Initial budding of a yeast cell resembles hyphal branching (albeit, without the emergence of the characteristic “Spitzenkorper” characteristic of the hyphal growth tip). This “branch” polarizes and extends, but its further polarization and tip growth is terminated soon after it lays down a septa dividing itself from the parent cell. Finally, the newly formed yeast cell splits off from the parent. Likewise, yeast sexual conjugation is similar in many ways to hyphal merging. Under the right conditions, yeasts like S. cerevisiae will even produce short hyphal segments sometimes called “pseudohyphae”.
There is much that remains to be understood about the development of fungal morphology, notably how fleshy, differentiated fruiting bodies (aka, mushrooms) emerged from a basic vegetative mycelial state. Indeed, only a few whole genomes of mushroom-producing species (Coprinopsis cinerea and Laccaria laccata) are even fully sequenced. Fungal “evo-devo” (evolutionary developmental biology) is still in its infancy, but will yield many fascinating insights in the years to come.
References:
- Harris SD. 2011. Hyphal morphogenesis: an evolutionary perspective. Fungal Biology 115(6):475-484. doi:10.1016/j.funbio.2011.02.002. (Abstract available online.)