Of Flies and Fungi

© Else C. Vellinga
Lab
Original publication: Mycena News, April 2005

I had never thought that I would be thrilled by mini-fungi growing in fly guts. I have still to see one but these Trichomycetes are fascinating creatures!

Trichomycetes really do not look like any other fungus, and are only found growing in or on arthropods (insects, crabs, millipedes and sow bugs to name a few). They occur in masses that look like miniature velvet mats, whence the name Trichomycetes, which literally means hair fungi.

All the usual questions and problems arise with this group of fungi. How do we recognize species, what are the bigger groupings, and are these groups monophyletic (an ensemble of everything derived from one common ancestor - you can guess the answer, especially because these things do not abound in characters to tell them apart); what kind of life cycle do they go through; what role do they play for their hosts, do they specialize in some particular part of the animal; and how do they get around from one place to another?

The discovery of these organisms was made by Leidy in the mid 19th century. He declared “that plants may grow in the interior of the healthy animal as a normal condition”, mistaking what he had found within the guts of millipedes and beetles for a colourless alga.

In the 20th century researchers in France and in the USA put Trichomycetes on the mycological map as a class belonging to the Zygomycota; bread mold and the beautiful Pilobolus are other members of the Zygomyccota that may be more familiar. At first four different orders were recognized within the Trichomycetes but two of these orders have now been shown to be out of place, in fact one of them is at the base of the animal-fungus split in the big tree of life. Of the two orders that remain in the Trichomycetes, Harpellales is the better known, and we focus on it for the rest of our fly-and-fungus story. Its members actually live within the aquatic larvae of black flies, stone flies and may flies. The fungi are completely adapted to life within the larvae and are very hard to grow outside their hosts.

To take an example, black fly larvae are found in flowing water as little tubes attached to the streambed; they have two brushes on top for filter-feeding. These larvae are small, and the fungi living within the guts are very small, the individuals not reaching one tenth of a millimeter in length. How they are attached to the gut, the branching patterns of the hyphae, and the shape and size of the spores are crucial characters to distinguish the species. There isn’t much to go on so it won’t be a great surprise if classifications change when molecular methods are applied to the group. In addition to regular spores which bud off asexually Trichomycetes can form zygospores, sexually produced spores which, under the microscope, look like two-dimensional capand- stem mushrooms. What conditions lead to the formation of zygospores is still not known, and asexual spores are much more common.

The spores swim around with whip-like appendages to find their hosts. Spores get into the fly larva, germinate and a new fungal individual is formed. The fungal spores - both regular spores and zygospores - emerge to infest the larvae anew. The lining of the insect gut is actually not separate from the outside skin of the animal, and when these larvae molt the gut lining is shed as well. So the fungi have to reinfect their hosts over and over again, at least in those species which molt several times during their larval part of life; in other words a constant coming and going of fungi. Rarely, and in some species combinations, the female adults have the fungus as a parasite. In that case, the fungi form cysts in the ovaries of the female, so instead of eggs, clusters of spores are laid, which reinfect the larvae. This is a beautiful way of dispersal for the fungi, as those adult females fly upstream of the place where they were hatched themselves, to deposit their eggs. But when and why the fungus parasitizes the adults is one of the question marks of the life cycle.

The fungi are not just anywhere in the guts of the larvae, but are concentrated in the hind gut, and that may have to do with the conditions there. The spores only attach to the gut lining and germinate under a certain pH, and that is not available just anywhere inside the gut.

Everywhere where people have looked for the host insects, these fungi have also been found, including remote islands like the Crozet Islands in the southern part of the Indian Ocean, and the Galapagos Islands where blackflies, and apparently also their fungi, have been introduced. Even the pitcher plant mosquito larvae, occurring in isolated pitcher plants in the Carolinas for instance, have Trichomycetes. You have to wonder how the fungi got into these little pools of water. I have not found a publication devoted to the Californian species, but as there are black flies in California, there must be Trichomycetes as well.

The fungi feed from food the insects eat and, as Leidy already discovered, apparently cause their hosts no other harm. Indeed, in recent experiments with one particular host-fungus combination, starved and fungus-free larvae did much worse than starved larvae which were infected with Trichomycetes. Both starved groups did worse than others with full bellies and fungi. This means that the relationship between the insects and the fungi is not always commensal (no effect on either of the parties), but under some conditions (in this experiment, a lack of food) can become a mutualism (beneficial for both parties), and under other different, still unknown circumstances, can be parasitic (detrimental to one party, and beneficial to the other). We tend to think of these relationships as fixed and mutually exclusive, but nature is always in flux, and different conditions may produce different effects. This is also true for mycorrhizal fungi and their plant hosts. Fungi which are instrumental in the survival of a seedling during summer drought may not be essential when water or food are plentiful. The relationship depends on circumstance.

In fact, insects have many more organisms defining their circumstance than just those Trichomycetes. Every individual animal is a walking (or flying) assemblage of bacteria and fungi, some good, some bad, some neutral, but all being a part of a bigger whole. Wondering how the hair fungi found their particular niche in this interaction web, and how they have become so specialized still gives me a thrill.

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