Impudence, Thy Name is Mushroom

This fall we've had some rude visitors out by the front door. One morning a strangely foul smell wafted through the windows. When we looked outside for a dead animal, we found nothing. But we noticed some downright obscene growths foisting themselves out of the flower beds. Thus I got my first introduction to the stinkhorn.

Stinkhorns are pornographic mushrooms. They form large underground webs of threads, which feed on dead and dying plant matter. At scattered points in the stinkhorn network, white rubbery spheres grow. Inside each of them is a pre-formed stinkhorn, which can then spring forth. The stinkhorns that grew outside our front door are called Phallus impudicus--Latin for the impudent penis. The stinkhorn expands with hydraulics that resemble the sort found in the human male anatomy. Water surges into honeycombed spaces, expanding the shaft out of its jellied egg. Stinkhorns can grow six inches an hour, with enough force to break through asphalt.

The stinkhorn looks like its phallic namesake, down to the small hole at the tip. Out of that hole comes The slimy mass on top of the mushrooms releases a stinky smell, carried by molecules that mimic the odor of corpses. Slugs and flies and other insects come from all around, swarming across the stinkhorn and feeding on its slime. They swallow the stinkhorn's spores as well, which they will later release with their own excrement.

This was all new to me. For enlightenment, I turned to some mycologists--scientists who study mushrooms and other fungi for a living. (One of them, Nicholas Money, is the author of several books on fungi that I'd recommend.) To me, stinkhorns are further proof that fungi are the weirdest, most mysterious bunch of species one could imagine. Compared to fungi, even the most bizarre animals are easy to grok: they are like us in the basics, searching for food to ingest. Plants may be profoundly different than we are, harnessing the energy from the sun rather than finding living matter to devour. Still there's something comfortable and soothing in the sight of a sunflower or a blossoming dogwood.

Fungi, on the other hand, are fundamentally alien. They send up stinkhorns and puffballs and fairy rings. They join with algae to form scab-like lichens. They are truffles and bread mold, Shitake mushrooms and yeast infections. Some lurk in the Earth, spreading out over hundreds of acres. Others live inside insects, forcing them to climb to the tip of a blade of grass, so that they can shower their spores down on new victims. Instead of ingesting their food, fungi dump their digestive enzymes into their surroundings and suck up the ensuing goo. Their reproductive cycles are like labyrinths. And of the estimated 1.5 million species of fungi on Earth, scientists have identified only five percent.

When scientists try to understand the diversity of any big group of species--animals, plants, or fungi to name three--they try to reconstruct its evolutionary tree. The pattern of its branches offers clues to the ancestry of the group, and to the transformations that took place as the major lineages split. Unfortunately for mycologists, the big fungal picture has long been blurry. Mycologists could recognize a few features that all fungi had, such as cell walls made of a tough substance called chitin. They could also recognize that certain kinds of fungi were united by some other traits, such as having a stage in their life cycle when their cells carried two nuclei instead of one. But it was very difficult to determine which group evolved from which based on cells and body shapes alone.

Analyzing DNA helped, but only a little at first. Scientists found that when they compared a single gene from a range of fungi, they couldn't get enough information to say how they are related with much confidence. The trouble is that the rate of mutations can change, speeding up and slowing down through time. It may be very hard to figure out the branches of an evolutionary tree if they all split up very rapidly a long time ago.

This trouble is not unique to fungi. Botanists faced a similar challenge in finding the evolutionary tree of plants. But they've made huge strides. Their successes have come from turning evolutionary trees into big science, with dozens of scientists pooling their research and using supercomputers to sort through the vast number of possible relationships plants may have. Now the evolutionary tree of plants is pretty well understood. It helps to shed light on how some green algae moved on land 450 million years ago, and how its descendants diversified into everything from mosses to redwoods.

Now it's the fungi's turn. A network of mycologists has been working for several years to build a fungal tree. They've published their initial results in today's issue of Nature. The seventy co-authors analyzed six genes in 199 species of fungi. They've created a rough guide to the history of the fungal kingdom--a history that may extend back a billion years.

The funny thing about fungi is that while they may seem alien, they're actually relatively close kin. A stinkhorn is more closely related to you than it is to a skunk cabbage. Animals and fungi share a common ancestor that was probably a single-celled protozoan, which probably swam around in water with whip-like tails called flagella. Some of those protozoans later began to live in colonies, which later gave rise to multicellular animals. Other protozoans gave rise to the fungi.

The oldest lineages of living fungi still carry those flagella. They are extremely rare, making up only two percent of the described species of fungi. They live as single cells, or in clusters of a few cells at most. No stinkhorns among them--let alone any other large terrestrial species. Such early fungi gave rise to a range of new forms. Some were parasitic (one kind of fungi, called microsporidia, evolved a harpoon with whic it fires spores into host cells). After these ancient lineage had split off, a new fungus began evolving in webs of threads. This was a major innovation, allowing fungi to increase the surface area through which they could release their enzymes and suck up food.

On at least four separate occassions, early fungi lost their tails. They were acquiring new ways to reproduce that no longer required them to swim around. Instead, they might disperse their spores in the air--often by producing mushrooms and other above-ground structures. These ancient transformation probably took place as fungi were colonizing land. Some studies suggest that fungi came ashore long before plants and animals. Plants owe their success on land to fungi, in fact, because they formed partnerships with some species. The fungi supplied nutrients from the soil and the plants supplied energy from the sun. It's a partnership on which our crops still depend today.

The new fungal tree is a starting point, rather than the last word. After all, the scientists only studied a tiny fraction of all the fungus species on Earth. And some of the branches on the tree they ended up still have only a low level of statistical support. If previous experience is any guide, the uncertainty will shrink with new species, new genes, or new methods. As mycologists continue to improve the tree, they will not only be able to better understand the origin of fungi, but their subsequent history. How did some fungi end up as yeast, while others form toadstool? Do fungi tend to evolve from free-living forms into parasites, or vice versa? Some members of the Nature team have focused on the species that include stinkhorns (their paper is in press). They find that stinkhorns probably evolved from truffle-like ancestors which grew underground. It was a clever transformation, allowing stinkhorns to use insects to spread their spores--a strategy that flowering plants hit upon on their own. How exactly the stinkhorns lifted themselves up in all their obscence glory is a question for future generations to ponder, fingers clasped over noses.

References:

Timothy Y. James et al 2006. Reconstructing the early evolution of Fungi using a six gene phylogyny. Nature, 443:818

Kentaro Hosaka et al 2006. Molecular phylogenetics of the gomphoid-phalloid fungi with an establishment of the new subclass Phallomycetidae and two new orders. Mycologia, in press.