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The Dish on Deliquescence in Coprinus Species

Good grief, who would have thought that a blog on fungi would be so full of disgusting things? Seems like every fungus is out to make its own kind of mess: molds turn your strawberries to mush, stinkhorns turn your mulch into putrescence, and inky caps (genus Coprinus) turn themselves into a black goo as you see here. I gotta say, I love mushrooms but I wouldn’t want to have to clean up after them.

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A time lapse study of Coprinopsis growing on a cube of poop by Kent Loeffler.

 

But don’t judge a fungus by its hygiene–the inky caps are some cool ‘shrooms! One species, tippler’s bane (Coprinus atramentarius) contains a chemical that will make you sick if and only if you drink alcohol. Another, shaggy mane (Coprinus comatus) is one you can savor battered and fried, but only if you can detect this delicacy before it deliquesces!1

To deliquesce is to liquefy. Most mushrooms don’t last more than a few days, but inky caps are usually here and gone in less than 24 hours! They have the fairly rare property of autodigestion, a habit of destroying themselves with their own enzymes once the mushroom has released its single round of spores. I’m a big fan of things that are even more slovenly than I am, so I’ve decided to make the why and how of deliquescence the topic of this blog post.

Ink from a deliquesced Coprinus comatus
The Benefits of Digesting One’s Self

Inky caps are not mushrooms you want to carry home in your shirt pocket! The mushrooms appear in wet conditions, but then the same moisture that brought life to the new tissue facilitates death: the inky caps digest themselves via hydrolytic enzymes, tiny biologic machines that use water to break down molecules. The slopfest takes just a few hours, from pileus to puddle. Then the once-mighty Coprinus comatus turns from a mushroom that can split asphalt into a thin liquid. You can actually use this liquid as a semi-permanent ink . . . it’s only a matter of time before the practical joke industry discovers inky caps.

But why would a living organism destroy part of itself? One reason is a bit like why the husk of a milkweed fruit becomes brittle and cracks once the feathery seeds within are mature. It’s a selective-death process that get useless tissue out of the way of the babies, letting them escape to as far from the parent as possible before they begin their new lives (it’s a little like college). As an inky cap deliquesces, the tightly packed gills separate and curl back, allowing some spores to float out into the air.

Self-sacrifice by the parent is not unknown in the animal world either (as those paying for college know). Ever heard of how praying mantis females eat the males after mating? Some entomologists believe that he sacrifices himself to provide additional nutrients to the mother and her eggs, and C. lagopus and C. curius are actually similar. These inky caps (and probably other species too) transport all of their sugars out of the fruiting body and into their spores just before sending them off. By the time deliquescence begins, there’s virtually no food left in the cap or gills; it’s all gone to the spores.2

The Disgusting Details of Deliquescence

If it’s worth it to you to get a little technical to learn even more about how mushrooms turn to muck, this section is for you.

Gooey Coprinus Mass

We already mentioned that hydrolytic enzymes are responsible for breaking an inky cap down into goo (“goo” is a technical term). Hydrolytic enzymes are not unusual; fungi secrete them to digest complex organic molecules into a nutrient slurry that their root-like mycelia can drink in.

What makes inky caps special is how they make and use another kind of hydrolytic enzyme. It’s chitinase, a group of enzymes that break down chitin, which is a complex sugar in fungal cell walls that makes them sturdy. Chitinase is not found in the fungus at all until just after meiosis has produced spores. At this point, about two hours before spore-release, chitinase is made, but only in the mushroom cap and gills, never in the mycelia or stem.3

Since chitin is present in all the cell walls of a fungus, you can imagine what chitinase, the chitin destroyer, does to an inky cap once it gets going. Deliquescence is a chain reaction, starting with the end of the gills closest to the mushroom stem. Spores are released from here first, and then autodiestion of gill cells there takes place, releasing a liquid that is a potent digestive. The liquid is taken up by the neighboring cells, which are turned into more liquid, and the wave of destruction travels along the gills just behind the region of maturing spores. Thus the mushroom is digested from the center to its fringe.4

If you were intently worried about the future of the Coprinus race, this story might raise a few concerns for you. If chitinase is sweeping down the gills at such a rate, why isn’t it destroying the spores before they can be released? It may be that many spores are caught in the liquid and perhaps destroyed (though the literature is silent on this point), but the fact that enough are dispersed to perpetuate the species might have something to do with the unusually high degree of coordination in spore development in at least some species of inky caps [see Editor’s note below]. In Coprinus cinereus, 60 to 85% of all the basidia (spore-bearing cells) in one cap will be in the same stage of development. That requires a remarkable deal of communication, and researchers suspect the coordination utilizes light signals: it is known that the mushrooms require light to develop normally.5
Coprinus comatus, deliquesced

Deliquescence in Poetry

Here’s something totally weird: even though chitinase digests chitin, and chitin is present in the walls of all fungal cells, Coprinus chitinases don’t seem to be effective on the cell walls of the mycelia or stipe. When the mushroom cap melts, these parts remain, as you can see in the picture at left.4, 5

This mystery has given us at least one work of art. Percy Bysshe Shelley is believed to have been inspired by an inky cap when he wrote

Their mass rotted off them flake by flake
Til the thick stalk stuck like a murderer’s take,
Where rags of loose flesh yet tremble on high
Infecting the winds that wander by.
   –”from “The Sensitive Plant,” Percy Bysshe Shelley, 18206

See how the “thick stalk” is left behind? Only the gills and cap are digested; their ragged remains and the untouched stipe are left behind in Shelley’s vision.5

References and Notes

  1. Lincoff, Gary H. National Audobon Society Field Guide to North American Mushrooms. Alfred A. Knopf, New York, 2006.
  2. Bonner, John Tyler; Hoffman, Allan A.; Morioka, Wilfred T. & Chiquoine, Duncan A. (1957). The Distribution of Polysaccharides and Basophilic Substances During the Development of the Mushroom Coprinus. The Biological Bulletin, 112 (1), 1-6.
  3. Hideyo Miyake, Tsuneo Takemaru and Tatsuo Ishikawa (1980). Sequential production of enzymes and basidiospore formation in fruiting bodies of Coprinus macorhizus. Archives of Microbiology, 126 (3), 201-205.
  4. Iten, W. & Matile, P. (1970). Role of chitinase and other lysosomal enzymes of Coprinus lagopus in the autolysis of fruiting bodies. Journal of General Microbiology, 61, 301-9.
  5. Shelley, Percy Bysshe. The Complete Poetical Works of Percy Bysshe Shelley Volume II. Thomas Hutchinson, ed., 1914 retrieved October 22, 2007 from http://www.gutenberg.org/dirs/etext03/shly210.txt
  6. Though a number of books talking about inky caps and deliquescence love to quote this verse, they don’t include a little tidbit about it that I, an English major in my pre-mycological life, cannot leave unmentioned. Shelley wrote these four lines around 1820, and they were printed that year as one stanza in the much longer poem “The Sensitive Plant.” But when he died two years later his wife, Mary Shelley, took control of his works and she had some ideas of her own. She left all of “The Sensitive Plant” intact except our stanza; this she crossed out before sending it to print. Thus in 1839 our stanza, the only one in the poem describing deliquescence, melted right out of the verse!4

Images by Kent Loeffler (time lapse); Kathie Hodge, Blog Editor (ink in a plastic cup); hr.icio (disgusting stand of Coprinus); and pete_vn52 (melted mushroom triad). The latter two images are licensed under Creative Commons 2.0.

Editor’s Musings:

Note that some of the mushrooms we’ve called Coprinus for a long time are no longer considered Coprinus species, and have been moved to genera of their own. One would think that that whole thing of having black spores and digesting yourself might have evolved only once, but no, there’s good evidence that all that evolved independently in several different groups of fungi. You can read a nice explication by Michael Kuo, here.

And another thing. It baffled me that the chitinases these mushrooms make can annihilate the fruiting bodies but leave the spores viable. After all, spore cell walls contain chitin too. I put this question to a couple of pros without much luck. Then Jason Stajich asked Ursula Kues about it, and she pointed out that spores have more layers in their cell walls that other tissues, the first being a tough one that can survive the onslaught. I feel better now.

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Most people don't pay much attention to fungi, which include things like mushrooms, molds, yeasts, and mildews. Here at Cornell we think they're pretty fascinating. In fact, even the most disgusting foot diseases and moldy strawberries are dear to our hearts. We'd like to talk to you about fungi, so that like us, you too can tell gross stories at the dinner table. Afterwards, maybe you'll notice some things you would have overlooked before, and we think this could be good for the planet.

Kathie T. Hodge, Editor

Beneath Notice, our book of borescopic mycology.

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