Spongiforma squarepantsii – what’s in a name? and what’s the underlying biology?

by Thomas D. Bruns and Dennis E. Desjardin

 

The original species of Spongiforma: S. thailandica, a new genus and species described in 2009 from material collected in Khao Yai National Park in central Thailand. Photo by Dennis Desjardin.

The original species of Spongiforma: S. thailandica, a new genus and species described in 2009 from material collected in Khao Yai National Park in central Thailand. Photo by Dennis Desjardin.

Recently we had the opportunity to describe a new species of fungus (Desjardin et al 2011). This may sound like a rare thing, but as it turns out there are many such undescribed fungi that await description. In fact, conservative estimates suggest that roughly 19 out of 20 fungi still need names (Hawksworth 2001).

The new Spongiforma: S. squarepantsii, a new species described recently from material collected in Borneo. Photo by Tom Bruns.

The new Spongiforma: S. squarepantsii, a new species described recently from material collected in Borneo. Photo by Tom Bruns.

Part of the reason that many remain unnamed is that they are often hard to see and they may exhibit very subtle differences from their close relatives. Typically such species are only found by mycologists that know how to look for the particular fungi due to their familiarity with related species. In addition, there is often difficulty in determining if a species has been described before. The scientific literature is vast and in multiple languages, and if a species was described prior to computerized indexing it can be easily missed. Even with a description it may be difficult to tell if the fungus in hand is the same or different from one described prior to the days of good imagery, good preservation, and DNA sequence analysis. As it happened these potential problems were not issues with the fungus we found because it had a unique morphology that placed it firmly into the genus Spongiforma, a genus that one of us described just two years earlier (Desjardin et al 2009) and that contained only one species, S. thailandica, known only from the type location in central Thailand.

Scanning electron micrographs of the basidiospores of Spongiforma squarepantsii. Note the surface ornamentation and pore at the end of each spore. Scale bar = 1 µm. Photo by Dennis Desjardin.

Scanning electron micrographs of the basidiospores of Spongiforma squarepantsii. Note the surface ornamentation and pore at the end of each spore. Scale bar = 1 µm. Photo by Dennis Desjardin.

Taxonomically inclined mycologists, however, did not find the fungus. Instead it was stumbled upon, almost literally, by Peter Kennedy, Kabir Peay, and Tom Bruns, who were in Borneo (Sarawak, Malaysia) to conduct ecological work on ectomycorrhizal fungi in the dipterocarp forests. When they first collected this fungus, it was not clear that it was even a member of the Basidiomycota, as the convoluted sponge-like shape could easily have been some sort of apothecium – similar in general design to morels. However Bruns had heard Desjardin give a talk on Spongiforma thailandica the previous year, and thought that the Borneo fungus might be related.

Upon returning to California, Peay sequenced the DNA of the specimens for two diagnostic loci, nrLSU and ITS, and found that the fungus was indeed related to S. thailandica, yet distinctly different from it. Other differences included the smell, which was fruity, and the color, which was orangish; these features contrasted with its coal-tar smelling, brownish grey relative from Thailand.

Emails flew back and forth between Bruns and Desjardin, and the specimens were sent across the San Francisco Bay from UC Berkeley to San Francisco State. Upon careful microscopic examination Desjardin found that the new species was almost identical in micromorphology to his earlier described species, S. thailandica. Differences were only apparent when he employed a scanning electron microscope to examine the spore surface. However, because this micromorphological difference was coupled with differences in color, smell and DNA sequence, it was obvious that the Borneo fungus was a new species.

Finally, a newly discovered mushroom species that can actually introduce itself!

Finally, a newly discovered mushroom species that can actually introduce itself!

Shakespeare was making the point that names don’t matter, but in the case of Spongiforma squarepantsii, he was clearly wrong. Although the name does seem to describe the fungus well (particularly, as you can see, after help from Photoshop), it could have been given a wide variety of other descriptive names. However, if we had named it something else, the odds are high that you would not be reading about it right now. Nor would the BBC, NPR, FOX or any other of the other news agencies or blogs have picked up the story like they did. Within 24 hours of its publication in the online version of Mycologia, there were over 24,000 links to “SpongeBob mushroom”. The truth is that a new fungus from Borneo that looks like a sponge is probably not enough to capture the public’s interest.

We’d like to say that we were smart enough to anticipate the excitement that the name produced, but the truth is we were just having fun. Why not name a sponge-shaped mushroom after the only famous sponge in our culture? In fact, when we submitted our manuscript, the reviewers gave us not one but two answers to that question: “it’s not correct Latin”, and “it’s frivolous”. Fortunately, Jeff Stone, the editor-in-chief of Mycologia, was willing to be persuaded by our arguments: “the Latinization of an honorarium name was in fact correct and within standard usage”, and “yes, it was a little frivolous, but lighten up, science should be fun”. Nevertheless he was not a big fan of the name, yet he let it go forward because he believed it was our right as authors to name the fungus anything we pleased as long as the name conformed to botanical nomenclature. Although the reviewers would have preferred that we translate the epithet into Latin, we felt quadratopanteloni just didn’t ring like squarepantsii! Stone has come around on the name since publication. He confessed to Bruns at the recent MSA meeting that online downloads of Mycologia articles doubled because of our paper, and so it’s hard not to like the name now. But we were not trying to sell deodorant, designer jeans, new cars, or even Mycologia, we were just trying to do good science and have some fun at the same time. This led to our unexpected Warholean 15 minutes of public fame, but while we are still basking in it, and you are still reading about it, let’s bring the science side back into discussion to make a couple of points about the specific biology of Spongiforma species, and about the state of mycological research.

Scanning electron micrographs of the smooth basidiospores of Spongiforma thailandica. Photo by Dennis Desjardin.

Scanning electron micrographs of the smooth basidiospores of Spongiforma thailandica. Photo by Dennis Desjardin.

Both species of Spongiforma have some interesting but poorly known biology associated with their spore dispersal. Unlike, mushrooms and polypores, Spongiforma species do not actively discharge their spores from their basidia. To translate that into plain English, they don’t shoot their spores off from the cells on which they are produced. In this feature they are like “gasteromycetes”: puffballs, false truffles, stinkhorns, bird’s nest fungi, and others. What we know about gasteromycetes from many previous studies is that they are not an evolutionary unit, or to employ the correct scientific terminology they are not “monophyletic” — they share no common ancestor. Multiple groups or lineages of gasteromycetes have been independently derived from mushroom ancestors (Hibbett et al. 1997). In the case of Spongiforma, we know from DNA sequence analysis that its closest relatives are boletes, probably near Porphyrellus or Strobilomyces (Desjardin et al. 2009). The lack of spore discharge is an evolutionary loss of function in all gasteromycetes, including Spongiforma, but in most other gasteromycetes the loss of active spore discharge is coupled with new ways to achieve spore dispersal. Puffballs developed bellows to puff their spores; false truffles, like Rhizopogon, attract mammals to eat their spores and disperse them; and stinkhorns have enlisted flies to disperse their spores.

This brings us to the obvious question: how does Spongiforma disperse its spores? We speculate that just like false truffles Spongiforma attracts animals to eat its fruiting body and disperse its spores. This mode of spore dispersal would be consistent with the distinctive odors of the two species, although it’s unclear what type of animals are involved. Southeast Asia and Malaysia offer many options: rodents, pigs, monkeys, and civets all come to mind, but it could be insects instead, and until more observations are made there is really no way to be sure. In any case, animal dispersal does not explain the sponge-like morphology.

And where do the spores need to go? This is a question that we cannot answer in a specific way for Spongiforma, but we have a good general guess: they need to find fine roots of trees in the Dipterocarpaceae. We say this because related members of the Boletaceae are ectomycorrhizal (i.e., they are symbiotically associated with the fine roots of trees), and both Spongiforma species were found in forests dominated by trees in the Dipterocarpaceae, a family known to be dependent on ectomycorrhizal associations with fungi. Just like the animal spore dispersal speculation, the ectomycorrhizal association fits the available evidence but needs more observations (e.g., colonized roots) in order to be verified.

Now let’s return from exotic settings back to North America to make one final point. It’s probably not surprising to anyone that Borneo or Thailand has undescribed fungi and that the basic biology of species there is poorly known. But what is more surprising (and a little embarrassing) is that we can go right in our own backyards and still find many undescribed mushrooms, and the basic biology of most fungi is not much better known than that of Spongiforma species. For example, in the last several years, three new species of mushrooms have been discovered from Pt Reyes National Seashore, which is about 50 miles from our two campuses. This may not sound like a lot of new species, but the work of describing these was done as unfunded side projects, so only the most obvious ones were focused on. However, we know from sequence analysis of collections from Pt. Reyes and Yosemite National Park that many of our common, “well-known” species (e.g., Inocybe geophyllum, Pluteus cervinus, and others) are actually undescribed North American species masquerading under European names (Vellinga and Bruns 2011).

Beyond the problem of discovering new species, we also face the challenge of documenting what our existing species do and where they occur. It is indicative of our collective state of ignorance that there is not a regional or state mycoflora (or mycobiota if you prefer) for any part of our continent; contrast this with plants or animals, where we have fairly detailed knowledge of distributions. In fact, we rarely have any significant knowledge of the fungi even in our National Parks, where surveying the biodiversity is a congressional mandate (although an unfunded one!). In Pt. Reyes and Yosemite for example, the fungal species list for each park contained fewer than 200 species. With help from the public we were able to more than double the species list of Yosemite National Park in a single year of collecting, and at Pt Reyes a multi-year effort with public involvement increased the species list by over four fold (Vellinga and Bruns 2011). These examples are clearly the tip of the iceberg, as all across North America we have only a very crude knowledge of our fungal flora. This brings up a point that Bruns (2011) recently made elsewhere: Assembling a North American mycoflora is long overdue and it will require significant participation from the informed public to accomplish it. This seems like a great message to end with because the readers of Mushroom the Journal are a likely set of participants.

Bibliography

Bruns, T. D. (2011). “President’s Corner: Working toward a North American Mycobiota for macrofungi — what’s stopping us?” Inoculum 62(4): 1-3.

Desjardin, D. E., M. Binder, S. Roekring, T. Flegel. (2009). “Spongiforma, a new genus of gasteroid boletes from Thailand”. Fungal Diversity 37: 1-8.

Desjardin, D. E., K. Peay, Bruns, T.D. (2011). “Spongiforma squarepantsii, a new species of gasteroid bolete from Borneo”. Mycologia 103: 1119-1123

Hawksworth, D. L. (2001). “The magnitude of fungal diversity: the 1.5 million species estimate revisited”. Mycological Research 105: 1422-1432.

Hibbett, D. S., E. M. Pine, E. Langer, G. Langer, M. J. Donoghue. (1997). “Evolution of gilled mushrooms and puffballs inferred from ribosomal DNA sequences.” Proceedings of the National Academy of Sciences of the United States of America 94(22): 12002-12006.

Vellinga, E. C. and T. D. Bruns (2011). “The mycota of two national parks in California – inventory, identification, sequencing, and data dissemination”. [Abstract]. Inoculum 62(3): 45